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_:vb552698457 _:vb552698458 _:vb552698459
n2:pmcid: PMC0
bibo:doi: 10.1016%2Fj.semcdb.2014.05.003
n7:contains: _:vb31245553 _:vb31245493 _:vb31245475 _:vb31245469 _:vb31245464

Subject Item: _:vb31245464
rdf:type: n7:Section
dc:title: introduction
n7:contains: _:vb31245468 _:vb31245465 _:vb31245466 _:vb31245467

Subject Item: _:vb31245465
rdf:type: n2:Context
rdf:value: The molecular dissection of the Hedgehog (Hh)-Gli signal transduction pathway in insects (e.g. [1–>>7<<]) and vertebrates (e.g. [8–16]), has revealed it to be complex and context-dependent with a surprising number of distinct cellular outputs.
n2:mentions: n3:11731473 n3:1394430 n3:1340474 n3:1280560 n3:10529809 n3:2797178

Subject Item: _:vb31245466
rdf:type: n2:Context
rdf:value: The molecular dissection of the Hedgehog (Hh)-Gli signal transduction pathway in insects (e.g. [1–7]) and vertebrates (e.g. [8–>>16<<]), has revealed it to be complex and context-dependent with a surprising number of distinct cellular outputs.
n2:mentions: n3:9216996 n3:8124714 n3:21502959 n3:20362092 n3:8269518 n3:8269519 n3:7916661 n3:15803137

Subject Item: _:vb31245467
rdf:type: n2:Context
rdf:value: ligands or of Gli proteins (as in zebrafish), or constraint HH signaling to primary clia in some species and tissues is unclear but likely to have important clues to speciation and the evolution of the morphogenetic plan (reviewed in [>>15<<]).
n2:mentions: n3:21502959

Subject Item: _:vb31245468
rdf:type: n2:Context
rdf:value: Whereas other reviews and papers address key aspects of the morphogenetic function of HH ligands (e.g. [17–>>20<<]) we elect to focus this review on 3 key points of the highly context-dependent nature of the HH-GLI pathway, where the history and the molecular make-up of the receiving cell determines the qualitative and quantitative output and
n2:mentions: n3:23673359 n3:23831049 n3:23719536 n3:17126548

Subject Item: _:vb31245469
rdf:type: n7:Section
dc:title: outlook
n7:contains: _:vb31245470 _:vb31245471 _:vb31245472 _:vb31245473 _:vb31245474

Subject Item: _:vb31245470
rdf:type: n2:Context
rdf:value: Whereas great progress has been made to understand how the GLI proteins act (e.g., reviewed in [7,21,58,59,64,>>163<<]), much remains to be understood.
n2:mentions: n3:20083481 n3:16406505 n3:22391298 n3:9244291 n3:10529809

Subject Item: _:vb31245471
rdf:type: n2:Context
rdf:value: Indeed, the involvement of HH-GLI signaling in normal stem cell lineages and in cancer stem cells [>>54<<] raises the possibility that novel molecular approaches to block positive GLI function, reverting the GLI code, could be highly beneficial.
n2:mentions: n3:12044012

Subject Item: _:vb31245472
rdf:type: n2:Context
rdf:value: signaling (see above) as part of the oncogenic load and, importantly, as druggable GLI modulators has already pointed out possible ways of how to design novel combination treatments with improved therapeutic benefit [64,65,90,98,164,>>165<<]. However, despite the increasing number of studies of GLI regulation in health and disease, we are only beginning to realize the remarkable complexity of context-dependent regulatory processes affecting the GLI code.
n2:mentions: n3:20083481 n3:24154871 n3:22294553 n3:22439934 n3:17392427

Subject Item: _:vb31245473
rdf:type: n2:Context
rdf:value: This will also open therapeutic opportunities to tackle the problem of relapse and drug resistance, as exemplified by the successful targeting of aPKC in SMOH inhibitor-resistant basal cell carcinomas [>>156<<].
n2:mentions: n3:23446420

Subject Item: _:vb31245474
rdf:type: n2:Context
rdf:value: Targeting transcription factors for cancer therapy has long been considered not effective, but clearly the number of recent examples such as those mentioned above along with the identification of small molecule GLI antagonists [166,>>167<<] provide ample proof-of-concept for the therapeutic relevance of such an approach.
n2:mentions: n3:21183792 n3:17494766

Subject Item: _:vb31245475
rdf:type: n7:Section
dc:title: the gli code
n7:contains: _:vb31245480 _:vb31245481 _:vb31245482 _:vb31245483 _:vb31245484 _:vb31245485 _:vb31245486 _:vb31245487 _:vb31245476 _:vb31245477 _:vb31245478 _:vb31245479 _:vb31245488 _:vb31245489 _:vb31245490 _:vb31245491 _:vb31245492

Subject Item: _:vb31245476
rdf:type: n2:Context
rdf:value: The GLI code model [21,>>22<<] considers the total GLI function as a balance of positive activator (GLIA) and negative repressive (GLIR) activities with GLI1 being mostly a positive transcription factor and GLI3 mostly a transcriptional repressor.
n2:mentions: n3:9244291 n3:17845852

Subject Item: _:vb31245477
rdf:type: n2:Context
rdf:value: GLI1 (originally GLI) was first identified as an amplified gene in a human glioblastoma cell line [23,>>24<<]. Later on and independently, what turned out to be its fly homolog, Cubitus interruptus (Ci) was identified and placed in the Hh pathway [7,25–27]. GLI1 was not linked to the vertebrate Hh pathway until later [12,28]. While the Drosophila
n2:mentions: n3:2832761 n3:3563490

Subject Item: _:vb31245478
rdf:type: n2:Context
rdf:value: Later on and independently, what turned out to be its fly homolog, Cubitus interruptus (Ci) was identified and placed in the Hh pathway [7,25–>>27<<]. GLI1 was not linked to the vertebrate Hh pathway until later [12,28]. While the Drosophila genome encodes only one GLI protein, the mouse and human genomes comprise three: GLI1, GLI2 and GLI3.
n2:mentions: n3:9215627 n3:8769644 n3:8658135 n3:10529809

Subject Item: _:vb31245479
rdf:type: n2:Context
rdf:value: GLI1 was not linked to the vertebrate Hh pathway until later [12,>>28<<]. While the Drosophila genome encodes only one GLI protein, the mouse and human genomes comprise three:
n2:mentions: n3:9216996 n3:9118802

Subject Item: _:vb31245480
rdf:type: n2:Context
rdf:value: One of the most remarkable features of GLI proteins is that in canonical HH signaling they can act as both transcriptional activators and repressors [29–>>33<<]. The situation is likely to be complex as all GLI proteins can act as activators or repressors in a stage-dependent and target gene-dependent manner [34].
n2:mentions: n3:10375510 n3:10976059 n3:10693759 n3:16611981 n3:14723851

Subject Item: _:vb31245481
rdf:type: n2:Context
rdf:value: The situation is likely to be complex as all GLI proteins can act as activators or repressors in a stage-dependent and target gene-dependent manner [>>34<<]. However, the basic idea of the GLI code is useful as a framework and generally considers GLI1 as an activator and GLI3 mostly as a repressor.
n2:mentions: n3:15983404

Subject Item: _:vb31245482
rdf:type: n2:Context
rdf:value: In the absence of HH pathway activity positive GLI function is off, GLI1 is not transcribed [>>12<<] and the GLI code is tipped toward a GLIR output, thus leading to pathway silencing.
n2:mentions: n3:9216996

Subject Item: _:vb31245483
rdf:type: n2:Context
rdf:value: There is also evidence for GLI1 isoforms but how these are produced is not clear [>>35<<].
n2:mentions: n3:19214186

Subject Item: _:vb31245484
rdf:type: n2:Context
rdf:value: GLI processing in the absence of HH signaling is triggered by sequential phosphorylation of Ci or GLI2/3 by Protein Kinase A (PKA), Glycogen Synthase Kinase 3-beta (GSK3β) and Casein Kinase 1 (CK1) [>>36<<] followed by proteasomal degradation of the C-terminal region [31,33]. Truncated Ci/GLI repressor binds to GLI sites in HH target promoters, thereby shutting off target gene expression (e.g. [37–39] (reviewed in [16,40])).
n2:mentions: n3:11955435

Subject Item: _:vb31245485
rdf:type: n2:Context
rdf:value: HH signaling is triggered by sequential phosphorylation of Ci or GLI2/3 by Protein Kinase A (PKA), Glycogen Synthase Kinase 3-beta (GSK3β) and Casein Kinase 1 (CK1) [36] followed by proteasomal degradation of the C-terminal region [31,>>33<<]. Truncated Ci/GLI repressor binds to GLI sites in HH target promoters, thereby shutting off target gene expression (e.g. [37–39] (reviewed in [16,40])).
n2:mentions: n3:10693759 n3:16611981

Subject Item: _:vb31245486
rdf:type: n2:Context
rdf:value: Truncated Ci/GLI repressor binds to GLI sites in HH target promoters, thereby shutting off target gene expression (e.g. [37–>>39<<] (reviewed in [16,40])).
n2:mentions: n3:10862738 n3:18832070 n3:17442700

Subject Item: _:vb31245487
rdf:type: n2:Context
rdf:value: Truncated Ci/GLI repressor binds to GLI sites in HH target promoters, thereby shutting off target gene expression (e.g. [37–39] (reviewed in [16,>>40<<])).
n2:mentions: n3:21801010

Subject Item: _:vb31245488
rdf:type: n2:Context
rdf:value: It is also unclear how the GLI proteins act since there is evidence that the GLI code will be highly refined and meticulously regulated given that GLI1, GLI2 and GLI3 can act in a combinatorial manner [30,34,41–>>43<<].
n2:mentions: n3:16571630 n3:10375510 n3:15983404 n3:9584120 n3:10725236

Subject Item: _:vb31245489
rdf:type: n2:Context
rdf:value: importance of the critical and tight regulation of the GLI code is illustrated on the one hand by the fact that varying levels of HH-GLI will induce different numbers of neural stem cells in normal development and homeostasis [35,44–>>48<<], and also induce different cell fates in the ventral neural tube in response to a morphogenetic gradient of HH ligands [8,9,11,49–51].
n2:mentions: n3:15604099 n3:16208373 n3:12971894 n3:19214186 n3:12469128 n3:14681189

Subject Item: _:vb31245490
rdf:type: n2:Context
rdf:value: will induce different numbers of neural stem cells in normal development and homeostasis [35,44–48], and also induce different cell fates in the ventral neural tube in response to a morphogenetic gradient of HH ligands [8,9,11,49–>>51<<]. On the other hand, genetic and/or epigenetic changes leading to irreversible activation of GLIA, and GLI1 [52], can drive a variety of malignant states ranging from cancers of the brain, skin, breast, prostate and digestive tract to
n2:mentions: n3:8124714 n3:15741323 n3:8269519 n3:18046410 n3:7916661 n3:22265416

Subject Item: _:vb31245491
rdf:type: n2:Context
rdf:value: On the other hand, genetic and/or epigenetic changes leading to irreversible activation of GLIA, and GLI1 [>>52<<], can drive a variety of malignant states ranging from cancers of the brain, skin, breast, prostate and digestive tract to malignancies of the hematopoietic system (e.g. [16,52–60]).
n2:mentions: n3:9349822

Subject Item: _:vb31245492
rdf:type: n2:Context
rdf:value: leading to irreversible activation of GLIA, and GLI1 [52], can drive a variety of malignant states ranging from cancers of the brain, skin, breast, prostate and digestive tract to malignancies of the hematopoietic system (e.g. [16,52–>>60<<]).
n2:mentions: n3:17360475 n3:11748155 n3:20085802 n3:16406505 n3:22391298 n3:17196391 n3:15549094 n3:9349822 n3:12044012

Subject Item: _:vb31245493
rdf:type: n7:Section
dc:title: regulation of the gli code by non-hh signals and by the oncogenic load
n7:contains: _:vb31245494 _:vb31245495 _:vb31245496 _:vb31245497 _:vb31245498 _:vb31245499 _:vb31245500 _:vb31245501 _:vb31245502 _:vb31245503 _:vb31245552 _:vb31245536 _:vb31245537 _:vb31245538 _:vb31245539 _:vb31245540 _:vb31245541 _:vb31245542 _:vb31245543 _:vb31245544 _:vb31245545 _:vb31245546 _:vb31245547 _:vb31245548 _:vb31245549 _:vb31245550 _:vb31245551 _:vb31245520 _:vb31245521 _:vb31245522 _:vb31245523 _:vb31245524 _:vb31245525 _:vb31245526 _:vb31245527 _:vb31245528 _:vb31245529 _:vb31245530 _:vb31245531 _:vb31245532 _:vb31245533 _:vb31245534 _:vb31245535 _:vb31245504 _:vb31245505 _:vb31245506 _:vb31245507 _:vb31245508 _:vb31245509 _:vb31245510 _:vb31245511 _:vb31245512 _:vb31245513 _:vb31245514 _:vb31245515 _:vb31245516 _:vb31245517 _:vb31245518 _:vb31245519

Subject Item: _:vb31245494
rdf:type: n2:Context
rdf:value: Indeed, GLI1 transcription is so far the only general biomarker of a cell's response to HH ligands [>>12<<], it can be a diagnostic tool for HH pathway activity [52] and is used to measure the efficiency of SMOH blockers in clinical samples [61–63].
n2:mentions: n3:9216996

Subject Item: _:vb31245495
rdf:type: n2:Context
rdf:value: Indeed, GLI1 transcription is so far the only general biomarker of a cell's response to HH ligands [12], it can be a diagnostic tool for HH pathway activity [>>52<<] and is used to measure the efficiency of SMOH blockers in clinical samples [61–63].
n2:mentions: n3:9349822

Subject Item: _:vb31245496
rdf:type: n2:Context
rdf:value: GLI1 transcription is so far the only general biomarker of a cell's response to HH ligands [12], it can be a diagnostic tool for HH pathway activity [52] and is used to measure the efficiency of SMOH blockers in clinical samples [61–>>63<<].
n2:mentions: n3:24493717 n3:22670904 n3:19726763

Subject Item: _:vb31245497
rdf:type: n2:Context
rdf:value: However, surprising data revealed that the GLI1 code and activity can also be modulated by non-HH signals [64,>>65<<]. Such regulation occurs in normal and in disease contexts and here we highlight key examples (Fig.
n2:mentions: n3:20083481 n3:17392427

Subject Item: _:vb31245498
rdf:type: n2:Context
rdf:value: The first example of tumor suppressors regulating normal GLI activity came from the work on p53, where p53 negatively regulates GLI1 [>>35<<]. Interestingly, GLI1 also regulates p53 [35,66], thus creating a regulatory loop in which the GLI code is subjected to the precise regulation by p53.
n2:mentions: n3:19214186

Subject Item: _:vb31245499
rdf:type: n2:Context
rdf:value: Interestingly, GLI1 also regulates p53 [35,>>66<<], thus creating a regulatory loop in which the GLI code is subjected to the precise regulation by p53.
n2:mentions: n3:18359851 n3:19214186

Subject Item: _:vb31245500
rdf:type: n2:Context
rdf:value: Modulation of p53 by GLI1 takes place through MDM factors [35,>>66<<] and it remains unclear how p53 represses GLI1 although it involves okadaic acid-sensitive protein phosphatases, possibly PP2A [35].
n2:mentions: n3:18359851 n3:19214186

Subject Item: _:vb31245501
rdf:type: n2:Context
rdf:value: Modulation of p53 by GLI1 takes place through MDM factors [35,66] and it remains unclear how p53 represses GLI1 although it involves okadaic acid-sensitive protein phosphatases, possibly PP2A [>>35<<].
n2:mentions: n3:19214186

Subject Item: _:vb31245502
rdf:type: n2:Context
rdf:value: Loss of p53 is a common occurrence in human tumors and this provokes the unregulated up-modulation of GLI1, thus leading to increased tumor cell proliferation and increased self-renewal of cancer stem cells [>>35<<]. Similarly, PTEN negatively regulates GLI1 activity in different human tumors that include melanomas [65].
n2:mentions: n3:19214186

Subject Item: _:vb31245503
rdf:type: n2:Context
rdf:value: Similarly, PTEN negatively regulates GLI1 activity in different human tumors that include melanomas [>>65<<]. This activity may flow through the action of AKT, which positively regulates GLI1 (see below) and is itself negatively modulated by PTEN [65,67], a repressor of AKT (see below). Many other tumor suppressors have since been found to
n2:mentions: n3:17392427

Subject Item: _:vb31245504
rdf:type: n2:Context
rdf:value: This activity may flow through the action of AKT, which positively regulates GLI1 (see below) and is itself negatively modulated by PTEN [65,>>67<<], a repressor of AKT (see below).
n2:mentions: n3:16537363 n3:17392427

Subject Item: _:vb31245505
rdf:type: n2:Context
rdf:value: Many other tumor suppressors have since been found to regulate GLI. For example, loss of the SNF5 or Menin leads to activation of GLI1 [68,>>69<<].
n2:mentions: n3:21076395 n3:23928057

Subject Item: _:vb31245506
rdf:type: n2:Context
rdf:value: Not only do common tumor suppressors repress GLI1 but common oncogenes, including RAS, MEK, MYC and AKT, positively regulate GLI1 in different tumor types [65,>>70<<]. Moreover, regulation of cMYC [71,72] and possibly of AKT [73] by GLI1, may establish positive feed-forward loops.
n2:mentions: n3:20049737 n3:17392427

Subject Item: _:vb31245507
rdf:type: n2:Context
rdf:value: Moreover, regulation of cMYC [71,>>72<<] and possibly of AKT [73] by GLI1, may establish positive feed-forward loops.
n2:mentions: n3:23525267 n3:20941789

Subject Item: _:vb31245508
rdf:type: n2:Context
rdf:value: Moreover, regulation of cMYC [71,72] and possibly of AKT [>>73<<] by GLI1, may establish positive feed-forward loops.
n2:mentions: n3:23580656

Subject Item: _:vb31245509
rdf:type: n2:Context
rdf:value: has led to the idea that it is the stepwise gain of oncogenic events and loss of tumor suppressors – named the oncogenic load – that leads to the acquisition of higher and higher GLI1 levels and thus higher and higher levels of GLIA [>>64<<]. These increases then drive GLIA beyond thresholds that induce changes in cell fate and behavior, such as the acquisition of metastatic behavior [64,70,71,74].
n2:mentions: n3:20083481

Subject Item: _:vb31245510
rdf:type: n2:Context
rdf:value: These increases then drive GLIA beyond thresholds that induce changes in cell fate and behavior, such as the acquisition of metastatic behavior [64,70,71,>>74<<].
n2:mentions: n3:20083481 n3:20049737 n3:20941789 n3:15013214

Subject Item: _:vb31245511
rdf:type: n2:Context
rdf:value: Note that one key contribution to the oncogenic load in a number of cancers, such as basal cell carcinomas, is the oncogenic mutation of the HH-GLI pathway itself, often through loss of PTCH1 in familial tumors [75,>>76<<], or loss of PTCH1, gain of SMOH activity or increase of SHH levels in sporadic cancers [52,53,56,65,70,77–86].
n2:mentions: n3:8681379 n3:8658145

Subject Item: _:vb31245512
rdf:type: n2:Context
rdf:value: cell carcinomas, is the oncogenic mutation of the HH-GLI pathway itself, often through loss of PTCH1 in familial tumors [75,76], or loss of PTCH1, gain of SMOH activity or increase of SHH levels in sporadic cancers [52,53,56,65,70,77–>>86<<].
n2:mentions: n3:11748155 n3:16909105 n3:20049737 n3:21983857 n3:15361885 n3:14520411 n3:9262482 n3:17196391 n3:12629553 n3:9349822 n3:8782823 n3:15314219 n3:17392427 n3:9422511 n3:15482598

Subject Item: _:vb31245513
rdf:type: n2:Context
rdf:value: Interestingly, initial evidence for non-HH signaling regulating the GLI code came from studies with frog embryos where GLI2 was found to act in the FGF-Brachyury loop in the early mesoderm [>>87<<]. In a separate study, the growth of mouse brain neurospheres was found to be dependent on both EGF and Sonic HH (SHH) signaling but only after decreasing their levels [46,47].
n2:mentions: n3:11003839

Subject Item: _:vb31245514
rdf:type: n2:Context
rdf:value: In a separate study, the growth of mouse brain neurospheres was found to be dependent on both EGF and Sonic HH (SHH) signaling but only after decreasing their levels [46,>>47<<]. This synergism between EGF and SHH [47], together with the regulation of GLI2 by FGF [87], and the regulation of GLI1 by RAS-MEK-AKT [65] opened a new chapter on the regulation of the GLI code, in this case by non-HH signals. These
n2:mentions: n3:15604099 n3:14681189

Subject Item: _:vb31245515
rdf:type: n2:Context
rdf:value: This synergism between EGF and SHH [>>47<<], together with the regulation of GLI2 by FGF [87], and the regulation of GLI1 by RAS-MEK-AKT [65] opened a new chapter on the regulation of the GLI code, in this case by non-HH signals.
n2:mentions: n3:14681189

Subject Item: _:vb31245516
rdf:type: n2:Context
rdf:value: This synergism between EGF and SHH [47], together with the regulation of GLI2 by FGF [>>87<<], and the regulation of GLI1 by RAS-MEK-AKT [65] opened a new chapter on the regulation of the GLI code, in this case by non-HH signals.
n2:mentions: n3:11003839

Subject Item: _:vb31245517
rdf:type: n2:Context
rdf:value: This synergism between EGF and SHH [47], together with the regulation of GLI2 by FGF [87], and the regulation of GLI1 by RAS-MEK-AKT [>>65<<] opened a new chapter on the regulation of the GLI code, in this case by non-HH signals.
n2:mentions: n3:17392427

Subject Item: _:vb31245518
rdf:type: n2:Context
rdf:value: Such a funnel idea [>>22<<] (Fig. 3) has strong implications for understanding the logic of signaling but also places the GLI code, and GLI1 in particular, in the line of fire for the development of novel therapies against cancer.
n2:mentions: n3:17845852

Subject Item: _:vb31245519
rdf:type: n2:Context
rdf:value: Additional work has shown that oncogenic RAS can regulate GLI1 in the apparent absence of Smo in pancreatic cancer in mice [>>88<<] being required for RAS-mediated tumorigenesis [89], and that EGF signaling cannot only synergize with HH-GLI outputs but also modify its outputs [90–93].
n2:mentions: n3:19136624

Subject Item: _:vb31245520
rdf:type: n2:Context
rdf:value: Additional work has shown that oncogenic RAS can regulate GLI1 in the apparent absence of Smo in pancreatic cancer in mice [88] being required for RAS-mediated tumorigenesis [>>89<<], and that EGF signaling cannot only synergize with HH-GLI outputs but also modify its outputs [90–93].
n2:mentions: n3:22493246

Subject Item: _:vb31245521
rdf:type: n2:Context
rdf:value: RAS can regulate GLI1 in the apparent absence of Smo in pancreatic cancer in mice [88] being required for RAS-mediated tumorigenesis [89], and that EGF signaling cannot only synergize with HH-GLI outputs but also modify its outputs [90–>>93<<]. Many other proto-oncogenic and oncogenic inputs have since been shown to regulate the GLI code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,97], the mTOR/S6K1 axis [98], WNT
n2:mentions: n3:22294553 n3:16880536 n3:19190345 n3:23762360

Subject Item: _:vb31245522
rdf:type: n2:Context
rdf:value: Many other proto-oncogenic and oncogenic inputs have since been shown to regulate the GLI code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,>>95<<], TGFβ signaling [96,97], the mTOR/S6K1 axis [98], WNT signaling [99] (although WNT genes can also be targets and mediators of GLI function [100,101]) and WIP1 [102].
n2:mentions: n3:18084326 n3:19189974

Subject Item: _:vb31245523
rdf:type: n2:Context
rdf:value: Many other proto-oncogenic and oncogenic inputs have since been shown to regulate the GLI code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,>>97<<], the mTOR/S6K1 axis [98], WNT signaling [99] (although WNT genes can also be targets and mediators of GLI function [100,101]) and WIP1 [102].
n2:mentions: n3:17638910 n3:19797115

Subject Item: _:vb31245524
rdf:type: n2:Context
rdf:value: Many other proto-oncogenic and oncogenic inputs have since been shown to regulate the GLI code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,97], the mTOR/S6K1 axis [>>98<<], WNT signaling [99] (although WNT genes can also be targets and mediators of GLI function [100,101]) and WIP1 [102].
n2:mentions: n3:22439934

Subject Item: _:vb31245525
rdf:type: n2:Context
rdf:value: proto-oncogenic and oncogenic inputs have since been shown to regulate the GLI code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,97], the mTOR/S6K1 axis [98], WNT signaling [>>99<<] (although WNT genes can also be targets and mediators of GLI function [100,101]) and WIP1 [102].
n2:mentions: n3:18057099

Subject Item: _:vb31245526
rdf:type: n2:Context
rdf:value: code in different contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,97], the mTOR/S6K1 axis [98], WNT signaling [99] (although WNT genes can also be targets and mediators of GLI function [100,>>101<<]) and WIP1 [102].
n2:mentions: n3:11378387 n3:19165927

Subject Item: _:vb31245527
rdf:type: n2:Context
rdf:value: contexts, such as for instance the EWS/FLI1 fusion oncoprotein [94,95], TGFβ signaling [96,97], the mTOR/S6K1 axis [98], WNT signaling [99] (although WNT genes can also be targets and mediators of GLI function [100,101]) and WIP1 [>>102<<].
n2:mentions: n3:23146903

Subject Item: _:vb31245528
rdf:type: n2:Context
rdf:value: Finally, interactions between pathways may be balanced by direct transcription factor binding such as that between GLI repressors and SMAD proteins, the latter being the mediators of normal and oncogenic BMP and TGFβ signaling [103,>>104<<].
n2:mentions: n3:9843199 n3:21266411

Subject Item: _:vb31245529
rdf:type: n2:Context
rdf:value: The integration of HH and EGF signaling [46,47,>>92<<] has been intensely studied given its developmental interest and its high therapeutic relevance.
n2:mentions: n3:15604099 n3:16880536 n3:14681189

Subject Item: _:vb31245530
rdf:type: n2:Context
rdf:value: SHH can transactivate the EGF receptor (EGFR) [>>105<<]. In addition, EGF activates the RAS-MEK cascade and this can superactivate GLI1 [65].
n2:mentions: n3:24133411

Subject Item: _:vb31245531
rdf:type: n2:Context
rdf:value: In addition, EGF activates the RAS-MEK cascade and this can superactivate GLI1 [>>65<<]. Moreover, both pathways can converge on the level of common target gene promoters resulting in selective and synergistic modulation of gene expression (reviewed in [59,106]).
n2:mentions: n3:17392427

Subject Item: _:vb31245532
rdf:type: n2:Context
rdf:value: Moreover, both pathways can converge on the level of common target gene promoters resulting in selective and synergistic modulation of gene expression (reviewed in [59,>>106<<]).
n2:mentions: n3:22391298

Subject Item: _:vb31245533
rdf:type: n2:Context
rdf:value: classes of target gene responses: (i) genes responding to HH-GLI only, (ii) genes activated or repressed by EGFR only and (iii) genes only or at least preferentially responding to combined and simultaneous activation of both pathways [>>92<<]. Notably, class III genes, also referred to as HH-EGFR target genes or cooperation response genes, contain functional GLI binding sites in their promoters, suggesting that signal integration occurs at the level of HH-EGFR target gene
n2:mentions: n3:16880536

Subject Item: _:vb31245534
rdf:type: n2:Context
rdf:value: class III genes, also referred to as HH-EGFR target genes or cooperation response genes, contain functional GLI binding sites in their promoters, suggesting that signal integration occurs at the level of HH-EGFR target gene promoters [>>92<<]. It is important to note that signal cooperation is a selective process as classical HH-GLI target genes such as PTCH1 or HHIP are not affected by parallel EGF signaling in keratinocytes [90,92,93].
n2:mentions: n3:16880536

Subject Item: _:vb31245535
rdf:type: n2:Context
rdf:value: It is important to note that signal cooperation is a selective process as classical HH-GLI target genes such as PTCH1 or HHIP are not affected by parallel EGF signaling in keratinocytes [90,92,>>93<<].
n2:mentions: n3:22294553 n3:16880536 n3:19190345

Subject Item: _:vb31245536
rdf:type: n2:Context
rdf:value: factor is the critical event at the terminal end of the EGFR cascade, inducing binding of activated JUN and GLI to common HH-EGFR target promoters, thereby cooperatively regulating target gene expression and transformation [92,>>93<<]. It is noteworthy that although basically all receptor tyrosine (RTK) pathways (e.g., HGF, VEGF or FGF) activate MEK/ERK, this is context-dependent as not all of them synergize with HH-GLI in human keratinocytes, possibly because they
n2:mentions: n3:16880536 n3:19190345

Subject Item: _:vb31245537
rdf:type: n2:Context
rdf:value: all receptor tyrosine (RTK) pathways (e.g., HGF, VEGF or FGF) activate MEK/ERK, this is context-dependent as not all of them synergize with HH-GLI in human keratinocytes, possibly because they fail to activate JUN/AP1 in these cells [>>90<<]. So far, only EGFR and PDGFRA [107] signaling have been identified as being able to stimulate both MEK/ERK and JUN/AP1 and synergize with HH-GLI in basal cell carcinoma (BCC) (Fig.
n2:mentions: n3:22294553

Subject Item: _:vb31245538
rdf:type: n2:Context
rdf:value: So far, only EGFR and PDGFRA [>>107<<] signaling have been identified as being able to stimulate both MEK/ERK and JUN/AP1 and synergize with HH-GLI in basal cell carcinoma (BCC) (Fig.
n2:mentions: n3:23041331

Subject Item: _:vb31245539
rdf:type: n2:Context
rdf:value: Importantly, the beneficial effect of EGFR blockade in HH-driven BCC and pancreatic cancer models can be synergistically improved by combined targeting of both pathways [90,93,>>108<<].
n2:mentions: n3:22294553 n3:20716670 n3:19190345

Subject Item: _:vb31245540
rdf:type: n2:Context
rdf:value: A second example involves the interaction between HH and WNT signaling in human colon cancer [>>71<<]. In this context, enhanced GLl1 represses WNT-TCF targets and repression of WNT-TCF targets via dominant-negative dnTCF leads to enhanced HH-GLI targets [71].
n2:mentions: n3:20941789

Subject Item: _:vb31245541
rdf:type: n2:Context
rdf:value: In this context, enhanced GLl1 represses WNT-TCF targets and repression of WNT-TCF targets via dominant-negative dnTCF leads to enhanced HH-GLI targets [>>71<<]. This mutually inhibitory interaction is distinct from that seen in other contexts between these two pathways (e.g. [100,109]) and is relevant in the context of the metastatic transition of human colon cancers. Patients with metastases,
n2:mentions: n3:20941789

Subject Item: _:vb31245542
rdf:type: n2:Context
rdf:value: This mutually inhibitory interaction is distinct from that seen in other contexts between these two pathways (e.g. [100,>>109<<]) and is relevant in the context of the metastatic transition of human colon cancers.
n2:mentions: n3:11378387 n3:10769232

Subject Item: _:vb31245543
rdf:type: n2:Context
rdf:value: Patients with metastases, but not those without, harbor local intestinal tumors that display repressed WNT-TCF and enhanced HH-GLI pathways as assessed by target gene signatures [>>71<<]. This switch, from high WNT-TCF, which drives initial intestinal tumorigenesis (e.g. [110]), to low WNT-TCF and enhanced HH-GLI in advanced and metastatic tumors was totally unexpected and is critical as experimental repression of WNT-TCF
n2:mentions: n3:20941789

Subject Item: _:vb31245544
rdf:type: n2:Context
rdf:value: This switch, from high WNT-TCF, which drives initial intestinal tumorigenesis (e.g. [>>110<<]), to low WNT-TCF and enhanced HH-GLI in advanced and metastatic tumors was totally unexpected and is critical as experimental repression of WNT-TCF or enhancement of HH-GLI in xenografts leads to increased metastases in mice [70,71].
n2:mentions: n3:12408868

Subject Item: _:vb31245545
rdf:type: n2:Context
rdf:value: [110]), to low WNT-TCF and enhanced HH-GLI in advanced and metastatic tumors was totally unexpected and is critical as experimental repression of WNT-TCF or enhancement of HH-GLI in xenografts leads to increased metastases in mice [70,>>71<<]. Blocking WNT-TCF in advanced cancers is thus not recommended.
n2:mentions: n3:20049737 n3:20941789

Subject Item: _:vb31245546
rdf:type: n2:Context
rdf:value: (e.g. [>>111<<]). However, while it is also required for advanced human colon cancer cells in vitro [110] it is not required in vivo [71].
n2:mentions: n3:8861899

Subject Item: _:vb31245547
rdf:type: n2:Context
rdf:value: However, while it is also required for advanced human colon cancer cells in vitro [>>110<<] it is not required in vivo [71].
n2:mentions: n3:12408868

Subject Item: _:vb31245548
rdf:type: n2:Context
rdf:value: However, while it is also required for advanced human colon cancer cells in vitro [110] it is not required in vivo [>>71<<]. Moreover, HH-GLI is dominant: enhanced GLI1 levels, or suppression of PTCH1, rescue the deleterious effects of TCF blockade by dnTCF [71]. There thus appears to be a functional cross-pathway switch at the metastatic transition. WNT-TCF
n2:mentions: n3:20941789

Subject Item: _:vb31245549
rdf:type: n2:Context
rdf:value: Moreover, HH-GLI is dominant: enhanced GLI1 levels, or suppression of PTCH1, rescue the deleterious effects of TCF blockade by dnTCF [>>71<<]. There thus appears to be a functional cross-pathway switch at the metastatic transition. WNT-TCF may keep tumors in a crypt-like state and enhanced HH-GLI together with repressed WNT-TCF may allow tumors to change fate and behavior and
n2:mentions: n3:20941789

Subject Item: _:vb31245550
rdf:type: n2:Context
rdf:value: WNT-TCF may keep tumors in a crypt-like state and enhanced HH-GLI together with repressed WNT-TCF may allow tumors to change fate and behavior and become metastatic [>>71<<].
n2:mentions: n3:20941789

Subject Item: _:vb31245551
rdf:type: n2:Context
rdf:value: Modeling such interactions in mice has revealed that Hh-Gli signaling is a parallel requirement since intestinal tumorigenesis can be initiated by loss of Apc but it is fully rescued by concomitant loss of Smo in the intestine [112,>>113<<].
n2:mentions: n3:19427313 n3:19861162

Subject Item: _:vb31245552
rdf:type: n2:Context
rdf:value: In the case of WNT-TCF signaling, there is evidence for binding of βCATENIN, the final output of canonical WNT pathway and both GLI3 C′-terminally deleted repressors and GLI1 [71,>>114<<]. Whether this interaction is the key mode of integration remains to be determined.
n2:mentions: n3:17331723 n3:20941789

Subject Item: _:vb31245553
rdf:type: n7:Section
dc:title: mechanisms of gli regulation
n7:contains: _:vb31245600 _:vb31245601 _:vb31245602 _:vb31245603 _:vb31245604 _:vb31245605 _:vb31245606 _:vb31245607 _:vb31245608 _:vb31245609 _:vb31245610 _:vb31245611 _:vb31245612 _:vb31245613 _:vb31245614 _:vb31245615 _:vb31245616 _:vb31245617 _:vb31245618 _:vb31245568 _:vb31245569 _:vb31245570 _:vb31245571 _:vb31245572 _:vb31245573 _:vb31245574 _:vb31245575 _:vb31245576 _:vb31245577 _:vb31245578 _:vb31245579 _:vb31245580 _:vb31245581 _:vb31245582 _:vb31245583 _:vb31245584 _:vb31245585 _:vb31245586 _:vb31245587 _:vb31245588 _:vb31245589 _:vb31245590 _:vb31245591 _:vb31245592 _:vb31245593 _:vb31245594 _:vb31245595 _:vb31245596 _:vb31245597 _:vb31245598 _:vb31245599 _:vb31245554 _:vb31245555 _:vb31245556 _:vb31245557 _:vb31245558 _:vb31245559 _:vb31245560 _:vb31245561 _:vb31245562 _:vb31245563 _:vb31245564 _:vb31245565 _:vb31245566 _:vb31245567

Subject Item: _:vb31245554
rdf:type: n2:Context
rdf:value: GLI proteins regulate target gene promoters by binding the consensus sequence GACCACCCA [115,>>116<<]. The two cytosines flanking the central adenine in the consensus sequence are essential for binding, while the other positions allow a certain degree of variation (Fig.
n2:mentions: n3:2105456 n3:16413481

Subject Item: _:vb31245555
rdf:type: n2:Context
rdf:value: The two cytosines flanking the central adenine in the consensus sequence are essential for binding, while the other positions allow a certain degree of variation (Fig. 5A) [117,>>118<<]. Sequence-specific DNA binding to the cis-regulatory region of a GLI target gene mainly involves zinc fingers 4 and 5 which make extensive base contacts within the 9-mer binding sequence, while fingers 2–3 mainly establish a few contacts
n2:mentions: n3:23249739 n3:20070907

Subject Item: _:vb31245556
rdf:type: n2:Context
rdf:value: Extensive protein–protein contacts between fingers 1 and 2 apparently contribute to the overall stability of the DNA binding domain [>>119<<] (Fig. 5B). Fingers 1 and 2 also provide protein–protein interaction sites to form GLI2, GLI3 and ZIC2 complexes [34].
n2:mentions: n3:8378770

Subject Item: _:vb31245557
rdf:type: n2:Context
rdf:value: Fingers 1 and 2 also provide protein–protein interaction sites to form GLI2, GLI3 and ZIC2 complexes [>>34<<].
n2:mentions: n3:15983404

Subject Item: _:vb31245558
rdf:type: n2:Context
rdf:value: Although global chromatin immunoprecipitation analyses and in vitro GLI-DNA binding screenings confirmed the consensus sequence as dominant binding site for GLIs [38,39,115,116,>>120<<], the importance of GLI binding sequences with 1–2 base pair substitutions is underappreciated and therefore possibly neglected or overseen in many studies.
n2:mentions: n3:18832070 n3:17442700 n3:2105456 n3:20460306 n3:16413481

Subject Item: _:vb31245559
rdf:type: n2:Context
rdf:value: sequence while preserving functionality contribute to subtle differences in DNA–protein binding affinity and hence may have a significant impact on the transcriptional output in response to defined GLI activator levels [117,118,>>121<<]. For instance, substitution of the consensus cytosine at position 7 for adenine results in a GLI binding site with even enhanced transcriptional response compared to the consensus motif [117].
n2:mentions: n3:21653228 n3:23249739 n3:20070907

Subject Item: _:vb31245560
rdf:type: n2:Context
rdf:value: For instance, substitution of the consensus cytosine at position 7 for adenine results in a GLI binding site with even enhanced transcriptional response compared to the consensus motif [>>117<<].
n2:mentions: n3:20070907

Subject Item: _:vb31245561
rdf:type: n2:Context
rdf:value: Although all GLI proteins bind the 9-mer consensus sequence with comparable affinity, repressor and activator forms bind the same sites [>>37<<], and different GLI proteins affect the same target genes differently [34,41].
n2:mentions: n3:10862738

Subject Item: _:vb31245562
rdf:type: n2:Context
rdf:value: Although all GLI proteins bind the 9-mer consensus sequence with comparable affinity, repressor and activator forms bind the same sites [37], and different GLI proteins affect the same target genes differently [34,>>41<<]. For example, GLI2 induces expression of the direct GLI target BCL2 significantly more strongly than GLI1 and systematic analysis of the BCL2 promoter reveals that one of the three validated GLI binding sites accounts for the preferential
n2:mentions: n3:15983404 n3:9584120

Subject Item: _:vb31245563
rdf:type: n2:Context
rdf:value: expression of the direct GLI target BCL2 significantly more strongly than GLI1 and systematic analysis of the BCL2 promoter reveals that one of the three validated GLI binding sites accounts for the preferential response to GLI2 [>>122<<].
n2:mentions: n3:15520176

Subject Item: _:vb31245564
rdf:type: n2:Context
rdf:value: In line with the documented morphogenetic activity of HH-GLI signaling e.g., in the neural tube (reviewed in [123,>>124<<] variations in binding site affinity are likely to play a major role in the interpretation of threshold GLI activity levels above which a gene is transcribed or below which the very same gene remains silent.
n2:mentions: n3:16041759 n3:19197245

Subject Item: _:vb31245565
rdf:type: n2:Context
rdf:value: at both high and low levels of GLI activator activity, while targets with low affinity binding sites will respond to high GLI activity only, as demonstrated for the response of neural tube patterning genes controlled by GLI [>>118<<]. High affinity binding may be generated by GLI binding site sequence variants and/or multiple repeats of the binding motif.
n2:mentions: n3:23249739

Subject Item: _:vb31245566
rdf:type: n2:Context
rdf:value: This also suggests that not only quantitative differences in the absolute GLIA protein level or activity determine the context-dependent cellular responses to HH-GLI [50,51,>>125<<] but also differential epigenetic modifications of the cis-regulatory regions of GLI targets affecting GLI-DNA binding affinity.
n2:mentions: n3:22265416 n3:18046410 n3:23725799

Subject Item: _:vb31245567
rdf:type: n2:Context
rdf:value: Cell-type specific histone acetylations or methylations and/or CpG methylation patterns of GLI target gene promoters are thus likely to modulate both the qualitative and quantitative response to GLI [>>118<<], an area in the HH-GLI field that has not yet been explored in great detail.
n2:mentions: n3:23249739

Subject Item: _:vb31245568
rdf:type: n2:Context
rdf:value: Distinct combinatorial GLI function could also account for the substantial difference and context-dependency of GLI1 regulated gene networks in the early embryo [30,34,>>41<<], as well as in the normal developing cerebellum and in medulloblastoma [120].
n2:mentions: n3:15983404 n3:10375510 n3:9584120

Subject Item: _:vb31245569
rdf:type: n2:Context
rdf:value: combinatorial GLI function could also account for the substantial difference and context-dependency of GLI1 regulated gene networks in the early embryo [30,34,41], as well as in the normal developing cerebellum and in medulloblastoma [>>120<<]. A genome-wide survey of GLI1 binding locations revealed numerous GLI1 binding sites in both the normal and malignant tissues, though the location and expression pattern diverged significantly between normal and malignant cells [120].
n2:mentions: n3:20460306

Subject Item: _:vb31245570
rdf:type: n2:Context
rdf:value: A genome-wide survey of GLI1 binding locations revealed numerous GLI1 binding sites in both the normal and malignant tissues, though the location and expression pattern diverged significantly between normal and malignant cells [>>120<<].
n2:mentions: n3:20460306

Subject Item: _:vb31245571
rdf:type: n2:Context
rdf:value: Although global ChIP approaches successfully and reliably identified classical HH-targets in addition to novel targets, it should be noted that these studies were performed with epitope tagged and overexpressed GLI [38,39,118,>>120<<], which may fully mimic endogenous GLI function.
n2:mentions: n3:18832070 n3:17442700 n3:20460306 n3:23249739

Subject Item: _:vb31245572
rdf:type: n2:Context
rdf:value: An example of such an interplay with cofactors that regulates the GLI code is the functional interaction between Zic and Gli proteins [>>126<<] (Fig. 3). The Zic factors are nuclear proteins with a GLI-type 5 zinc finger domain [127] that can recognize GLI binding sites albeit with different affinities [128].
n2:mentions: n3:9634234

Subject Item: _:vb31245573
rdf:type: n2:Context
rdf:value: The Zic factors are nuclear proteins with a GLI-type 5 zinc finger domain [>>127<<] that can recognize GLI binding sites albeit with different affinities [128].
n2:mentions: n3:8557628

Subject Item: _:vb31245574
rdf:type: n2:Context
rdf:value: The Zic factors are nuclear proteins with a GLI-type 5 zinc finger domain [127] that can recognize GLI binding sites albeit with different affinities [>>128<<]. They modify GLI outputs [126,128] and can interact through the first two zinc fingers [34,129]. In the early neural plate of frog embryos, Zic2 is expressed in specific longitudinal bands that are adjacent to zones of primary
n2:mentions: n3:11053430

Subject Item: _:vb31245575
rdf:type: n2:Context
rdf:value: They modify GLI outputs [126,>>128<<] and can interact through the first two zinc fingers [34,129].
n2:mentions: n3:11053430 n3:9634234

Subject Item: _:vb31245576
rdf:type: n2:Context
rdf:value: They modify GLI outputs [126,128] and can interact through the first two zinc fingers [34,>>129<<]. In the early neural plate of frog embryos, Zic2 is expressed in specific longitudinal bands that are adjacent to zones of primary neurogenesis, which is triggered by GLI proteins expressed throughout the plate. The overlap leads to the
n2:mentions: n3:15983404 n3:11238441

Subject Item: _:vb31245577
rdf:type: n2:Context
rdf:value: The overlap leads to the repression of Gli proneurogenic function by Zic2 in restricted domains, thus leading to the definition of domains of neurogenic differentiation [>>126<<]. In this context, Zic2 mimics C-terminally truncated Gli repressors [126]. In a different context Zic2 may mimic positive GLI function as it is required for ventral forebrain fates: Loss of ZIC2 is associated with human holoprosencephaly
n2:mentions: n3:9634234

Subject Item: _:vb31245578
rdf:type: n2:Context
rdf:value: In this context, Zic2 mimics C-terminally truncated Gli repressors [>>126<<]. In a different context Zic2 may mimic positive GLI function as it is required for ventral forebrain fates:
n2:mentions: n3:9634234

Subject Item: _:vb31245579
rdf:type: n2:Context
rdf:value: In a different context Zic2 may mimic positive GLI function as it is required for ventral forebrain fates: Loss of ZIC2 is associated with human holoprosencephaly [>>130<<], paralleling the association of this malformation with loss of SHH [131] or GLI2 [132].
n2:mentions: n3:9771712

Subject Item: _:vb31245580
rdf:type: n2:Context
rdf:value: a different context Zic2 may mimic positive GLI function as it is required for ventral forebrain fates: Loss of ZIC2 is associated with human holoprosencephaly [130], paralleling the association of this malformation with loss of SHH [>>131<<] or GLI2 [132].
n2:mentions: n3:8896571

Subject Item: _:vb31245581
rdf:type: n2:Context
rdf:value: Zic2 may mimic positive GLI function as it is required for ventral forebrain fates: Loss of ZIC2 is associated with human holoprosencephaly [130], paralleling the association of this malformation with loss of SHH [131] or GLI2 [>>132<<].
n2:mentions: n3:14581620

Subject Item: _:vb31245582
rdf:type: n2:Context
rdf:value: As discussed above p53 negatively regulates GLI1 [>>35<<] and GLI1 negatively regulates p53 [35,66].
n2:mentions: n3:19214186

Subject Item: _:vb31245583
rdf:type: n2:Context
rdf:value: As discussed above p53 negatively regulates GLI1 [35] and GLI1 negatively regulates p53 [35,>>66<<]. p53 would appear to be active in most cells. However, a further layer of regulation is provided by the homeodomain and stemness factor NANOG, which forms a positive feed-forward loop with GLI1 [133]. Interestingly, this loop is also
n2:mentions: n3:19214186 n3:18359851

Subject Item: _:vb31245584
rdf:type: n2:Context
rdf:value: However, a further layer of regulation is provided by the homeodomain and stemness factor NANOG, which forms a positive feed-forward loop with GLI1 [>>133<<]. Interestingly, this loop is also regulated negatively by p53, establishing a highly dynamic node that will be affected by any input that will affect GLI1, NANOG and/or p53 [133] (Fig. 3). Regulatory mechanisms involve regulation of MDM
n2:mentions: n3:20581802

Subject Item: _:vb31245585
rdf:type: n2:Context
rdf:value: Interestingly, this loop is also regulated negatively by p53, establishing a highly dynamic node that will be affected by any input that will affect GLI1, NANOG and/or p53 [>>133<<] (Fig. 3). Regulatory mechanisms involve regulation of MDM proteins by GLI1, protein phosphatase action, direct GLI regulation of NANOG1 expression and the action of microRNAs [35,66,134,135]. Thus, in adult cells expressing NANOG, likely
n2:mentions: n3:20581802

Subject Item: _:vb31245586
rdf:type: n2:Context
rdf:value: Regulatory mechanisms involve regulation of MDM proteins by GLI1, protein phosphatase action, direct GLI regulation of NANOG1 expression and the action of microRNAs [35,66,134,>>135<<]. Thus, in adult cells expressing NANOG, likely stem cells and cancer stem cells, the GLI code will be modulated by additional positive mechanisms. As p53 is often lost in cancer, this is predicted to free the GLI1-NANOG loop from negative
n2:mentions: n3:19214186 n3:18359851 n3:20581804 n3:24076654

Subject Item: _:vb31245587
rdf:type: n2:Context
rdf:value: essential role of NANOG and HH-GLI is demonstrated by their regulation of clonogenic gliomaspheres and by their absolute requirement for the growth of primary human glioblastomas orthotopically engrafted in the brains of host mice [>>133<<].
n2:mentions: n3:20581802

Subject Item: _:vb31245588
rdf:type: n2:Context
rdf:value: Genetic and functional studies first carried out in the fruit fly and later in mammalian cells have identified CBP as essential co-factor for Ci and GLI3 mediated target gene activation [>>136<<]. Haploinsufficiency of CBP is associated with Rubinstein-Taybi syndrome, a genetic disorder characterized by several developmental anomalies with partially striking similarities to defects observed in patients suffering from Greig's
n2:mentions: n3:9109493

Subject Item: _:vb31245589
rdf:type: n2:Context
rdf:value: disorder characterized by several developmental anomalies with partially striking similarities to defects observed in patients suffering from Greig's cephalopolysyndactyly syndrome, which is caused by mutations in the GLI3 gene [136–>>139<<]. Given the intrinsic histone acetyl transferase (HAT) of CBP/p300 [140], CBP-GLI interactions are likely to cause epigenetic changes of the cis-regulatory region of GLI targets making them more accessible to other transcriptional
n2:mentions: n3:1650914 n3:9294190 n3:10077605 n3:9109493

Subject Item: _:vb31245590
rdf:type: n2:Context
rdf:value: Given the intrinsic histone acetyl transferase (HAT) of CBP/p300 [>>140<<], CBP-GLI interactions are likely to cause epigenetic changes of the cis-regulatory region of GLI targets making them more accessible to other transcriptional regulators.
n2:mentions: n3:11559745

Subject Item: _:vb31245591
rdf:type: n2:Context
rdf:value: In line with this hypothesis, histone acetyl transferase PCAF interacts with GLI1 and enhances HH-GLI target gene expression in medulloblastoma cells by promoting the level of H3K lysine modifications [>>141<<]. However, when functioning as ubiquitin ligase, PCAF can also negatively regulate GLI activity under genotoxic stress conditions [142].
n2:mentions: n3:23943798

Subject Item: _:vb31245592
rdf:type: n2:Context
rdf:value: However, when functioning as ubiquitin ligase, PCAF can also negatively regulate GLI activity under genotoxic stress conditions [>>142<<].
n2:mentions: n3:24013724

Subject Item: _:vb31245593
rdf:type: n2:Context
rdf:value: Recruitment of SAP18 to GLI via binding to the negative GLI regulator Suppressor of Fused (SUFU) [>>143<<] is crucial for efficient repression of GLI target genes [144,145].
n2:mentions: n3:10559945

Subject Item: _:vb31245594
rdf:type: n2:Context
rdf:value: Recruitment of SAP18 to GLI via binding to the negative GLI regulator Suppressor of Fused (SUFU) [143] is crucial for efficient repression of GLI target genes [144,>>145<<]. Like SAP18, Atrophin (Atro) has been identified in fish and flies as a GLI/Ci cofactor required for target gene repression via recruitment of histone deacetylases [146].
n2:mentions: n3:11960000 n3:14611647

Subject Item: _:vb31245595
rdf:type: n2:Context
rdf:value: Like SAP18, Atrophin (Atro) has been identified in fish and flies as a GLI/Ci cofactor required for target gene repression via recruitment of histone deacetylases [>>146<<].
n2:mentions: n3:24385484

Subject Item: _:vb31245596
rdf:type: n2:Context
rdf:value: TBP-associated factor 9 (TAF9) encodes a transcriptional co-activator that directly interacts with the GLI activator forms GLI1 and GLI2 via their transcriptional activation domain [>>147<<]. TAF9 has been shown to enhance the transcriptional activity of GLI, which may play an oncogenic role in lung cancer.
n2:mentions: n3:23686308

Subject Item: _:vb31245597
rdf:type: n2:Context
rdf:value: Both genetic and chemical inhibition of TAF9-GLI interactions dampen GLI target gene transcription, thus providing a possible therapeutic strategy to target oncogenic HH-GLI signaling downstream of the common HH drug target SMOH [>>147<<].
n2:mentions: n3:23686308

Subject Item: _:vb31245598
rdf:type: n2:Context
rdf:value: Furthermore, direct interaction of GLI3 with MED12, a subunit of the RNA Polymerase II transcriptional Mediator, enhances the transcriptional response to GLI activator by reversing the Mediator-regulated repression of HH target genes [>>148<<].
n2:mentions: n3:17000779

Subject Item: _:vb31245599
rdf:type: n2:Context
rdf:value: distinct from those enhancing GLI repressor formation promote association of 14-3-3 with GLI2 and GLI3, thereby repressing their transcriptional activity independent of the intrinsic N-terminal repressor domain of GLI2 and GLI3 [>>149<<].
n2:mentions: n3:19996099

Subject Item: _:vb31245600
rdf:type: n2:Context
rdf:value: of JUN expression as full transcriptional activation of these targets is likely to require co-occupancy of their promoter region by GLI and JUN/AP1, similar to the mechanism accounting for HH and EGF signal integration [90,93,>>150<<].
n2:mentions: n3:19219074 n3:22294553 n3:19190345

Subject Item: _:vb31245601
rdf:type: n2:Context
rdf:value: binding of transcription factors controls context-dependent HH output is illustrated by the finding that co-occupancy of selected GLI targets by GLI1 and SOX2 is required for full activation of a neural gene expression signature [>>118<<].
n2:mentions: n3:23249739

Subject Item: _:vb31245602
rdf:type: n2:Context
rdf:value: Motif enrichment analyses identified E-box sequences as frequently co-occurring with GLI binding sites in GLI target genes expressed in medulloblastoma [>>120<<]. It is therefore possible, that E-box binding bHLH transcription factors cooperate with GLI in the control of tissue specific target gene expression and cancer development, a model that still needs to be confirmed in future studies.
n2:mentions: n3:20460306

Subject Item: _:vb31245603
rdf:type: n2:Context
rdf:value: and ligand-receptor interactions down to the numerous molecular interactions and modifications of GLI proteins eventually determining the molecular phenotype by controlling gene expression in response to pathway activity [20,22,40,54,>>151<<].
n2:mentions: n3:23719536 n3:21801010 n3:12044012 n3:17845852 n3:23747033

Subject Item: _:vb31245604
rdf:type: n2:Context
rdf:value: At the level of GLI code, a number of post-translational modifications of GLI proteins play a fundamental role in its control by affecting GLI stability, subcellular localization and DNA binding ability [152–>>155<<] (reviewed in [20,40]). To remain focused on the topic of context-dependent GLI activity, we concentrate here on GLI modifications that directly affect the intrinsic GLI transcriptional activity.
n2:mentions: n3:12138125 n3:17115028 n3:15249678 n3:16421275

Subject Item: _:vb31245605
rdf:type: n2:Context
rdf:value: At the level of GLI code, a number of post-translational modifications of GLI proteins play a fundamental role in its control by affecting GLI stability, subcellular localization and DNA binding ability [152–155] (reviewed in [20,>>40<<]). To remain focused on the topic of context-dependent GLI activity, we concentrate here on GLI modifications that directly affect the intrinsic GLI transcriptional activity.
n2:mentions: n3:23719536 n3:21801010

Subject Item: _:vb31245606
rdf:type: n2:Context
rdf:value: 6) [156–>>158<<].
n2:mentions: n3:20081843 n3:23762415 n3:23446420

Subject Item: _:vb31245607
rdf:type: n2:Context
rdf:value: Of note, hyperactivation of aPKC in BCC can account for SMOH inhibitor resistance, rendering it a promising drug target for the treatment of cancer patients unresponsive to classical HH pathway inhibitors targeting SMOH [>>156<<]. aPKC (also referred to as PRKCI) can affect HH-GLI signaling also by phosphorylating the transcription factor SOX2. Phospho-SOX2 acts a potent transcriptional activator of HH acetyltransferase expression, leading to increased HH ligand
n2:mentions: n3:23446420

Subject Item: _:vb31245608
rdf:type: n2:Context
rdf:value: Phospho-SOX2 acts a potent transcriptional activator of HH acetyltransferase expression, leading to increased HH ligand production and cell-autonomous HH-GLI activation in lung squamous cell carcinoma [>>159<<].
n2:mentions: n3:24525231

Subject Item: _:vb31245609
rdf:type: n2:Context
rdf:value: In esophageal cancer cells, activation of mTOR/S6K1 signaling leads to S6K1-mediated phosphorylation of Ser85 in GLI1, enhancing GLI1 transcriptional activity by disrupting its interaction with the negative GLI regulator SUFU [>>98<<]. Of note, the S6K1 phosphorylation site at Ser85 of GLI1 is located in a D-site motif that serves as MAP kinase binding site required for phosphorylation and activation of GLI1 by JNK and ERK [160] (Fig.
n2:mentions: n3:22439934

Subject Item: _:vb31245610
rdf:type: n2:Context
rdf:value: Of note, the S6K1 phosphorylation site at Ser85 of GLI1 is located in a D-site motif that serves as MAP kinase binding site required for phosphorylation and activation of GLI1 by JNK and ERK [>>160<<] (Fig. 6). S6K1 phosphorylation may therefore not only interfere with SUFU binding but also modify GLI phosphorylation by MAP kinases.
n2:mentions: n3:20865152

Subject Item: _:vb31245611
rdf:type: n2:Context
rdf:value: PKA phosphorylation sites (ncPKA) in close proximity to the SUFU binding site has also been shown to regulate GLI2/3 activation, though the GLI activating kinase responsible for phosphorylating ncPKA sites has not been identified [>>161<<]. Whether phosphorylation of ncPKA sites activates GLI2/3 by disrupting the SUFU-GLI complex or by a different mode also needs to be addressed in future studies.
n2:mentions: n3:24373970

Subject Item: _:vb31245612
rdf:type: n2:Context
rdf:value: This suggests that the N-terminus of GLI proteins serves as integration domain for multiple signals from distinct pathways such as PI3K/AKT, mTOR/S6K or FGF/MEK/ERK signaling [65,98,>>162<<]. In line with an integration function of the N-terminal region, deletion of the GLI1 N-terminus abolishes its ectopic activation of FoxA2 (HNF3β) in the neural tube [30] and its hyperactivation in response to FGF treatment [162]. It
n2:mentions: n3:17392427 n3:16424016 n3:22439934

Subject Item: _:vb31245613
rdf:type: n2:Context
rdf:value: In line with an integration function of the N-terminal region, deletion of the GLI1 N-terminus abolishes its ectopic activation of FoxA2 (HNF3β) in the neural tube [>>30<<] and its hyperactivation in response to FGF treatment [162].
n2:mentions: n3:10375510

Subject Item: _:vb31245614
rdf:type: n2:Context
rdf:value: In line with an integration function of the N-terminal region, deletion of the GLI1 N-terminus abolishes its ectopic activation of FoxA2 (HNF3β) in the neural tube [30] and its hyperactivation in response to FGF treatment [>>162<<]. It follows that this integration domain plays a major role in the fine-tuning of GLI activity in normal tissues and importantly, also in the irreversible activation of GLI in cancer cells.
n2:mentions: n3:16424016

Subject Item: _:vb31245615
rdf:type: n2:Context
rdf:value: Acetylation of GLI2 at Lys757 by the histone acetyl transferase p300 is a critical negative regulatory modification in HH signaling [>>157<<]. Interestingly, acetylated GLI2 displays significantly reduced recruitment to chromatin and consequently only weak activator potential [157]. As the acetylation site is C-terminal of the DNA binding domain it is unlikely that acetylation
n2:mentions: n3:23762415

Subject Item: _:vb31245616
rdf:type: n2:Context
rdf:value: Interestingly, acetylated GLI2 displays significantly reduced recruitment to chromatin and consequently only weak activator potential [>>157<<]. As the acetylation site is C-terminal of the DNA binding domain it is unlikely that acetylation directly affects DNA binding affinity. Rather, deacetylation may favor the interaction of GLI with chromatin bound proteins and therefore
n2:mentions: n3:23762415

Subject Item: _:vb31245617
rdf:type: n2:Context
rdf:value: Indeed, HH signaling promotes deacetylation of GLI1/2 via inducing class I histone deacetylases (HDAC), which has been identified as important step in the activation of GLI target gene expression [157,>>158<<].
n2:mentions: n3:20081843 n3:23762415

Subject Item: _:vb31245618
rdf:type: n2:Context
rdf:value: Here, selected kinases (MAPK, S6K1 and aPKC) and deacetylases (HDAC) act as positive regulators, while acetylases (p300), PKA [>>161<<] and as yet unidentified phosphatases control the termination of HH signaling via GLI inactivation (Fig.
n2:mentions: n3:24373970

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