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n2:pmcid: PMC0
bibo:doi: 10.1101%2Fgad.256693.114
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Subject Item: _:vb40624422
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb40624428 _:vb40624429 _:vb40624430 _:vb40624431 _:vb40624424 _:vb40624425 _:vb40624426 _:vb40624427 _:vb40624423

Subject Item: _:vb40624423
rdf:type: n2:Context
rdf:value: Lox-stop-Lox-TetOn-Lin28 and conditional Lin28a and Lin28b double-knockout mice were previously generated in our laboratory (Zhu et al. >>2011<<; Shinoda et al. 2013).
n2:mentions: n3:21962509

Subject Item: _:vb40624424
rdf:type: n2:Context
rdf:value: Lox-stop-Lox-TetOn-Lin28 and conditional Lin28a and Lin28b double-knockout mice were previously generated in our laboratory (Zhu et al. 2011; Shinoda et al. >>2013<<). Villin-Cre (stock no. 004586) and ApcMin/+ (stock no. 002020) animals were obtained from Jackson Laboratory. For transgene induction, 1 g/L doxycycline (Sigma) was administered to the drinking water at different time points to induce
n2:mentions: n3:23666760

Subject Item: _:vb40624425
rdf:type: n2:Context
rdf:value: To achieve co-overexpression of Lin28 and Let7, we crossed Villin-cre mice with TRE-7S21L (“iLet-7”) (described in Zhu et al. >>2011<<) mice and then crossed the Villin-cre; iLet-7 mice with Lox-stop-Lox-TetOn-LIN28 mice.
n2:mentions: n3:21962509

Subject Item: _:vb40624426
rdf:type: n2:Context
rdf:value: These variants were annotated with ANNOVAR (Wang et al. >>2010<<) using mouse mm10 genome assembly and curated by literature reviews.
n2:mentions: n3:20601685

Subject Item: _:vb40624427
rdf:type: n2:Context
rdf:value: of two United States nationwide prospective cohort studies: the Nurses’ Health Study (NHS; N = 121,700 women observed since 1976) and the Health Professionals Follow-Up Study (HPFS; N = 51,500 men observed since 1986) (Liao et al. 2012a). Participants were sent follow-up biennial questionnaires to update information on diet and lifestyle factors and identify newly diagnosed cancers and other diseases.
n2:mentions: n3:23094721

Subject Item: _:vb40624428
rdf:type: n2:Context
rdf:value: The type of tumor growth pattern at the tumor margin was examined at low-power magnification and categorized as expansile, intermediate, or infiltrative (Morikawa et al. >>2012<<). Diagnostic biopsy specimens from rectal cancer patients who received preoperative therapy were collected in order to avoid treatment-related artifacts. Patients were observed until death or January 2013, whichever came first. Written
n2:mentions: n3:22189472

Subject Item: _:vb40624429
rdf:type: n2:Context
rdf:value: Tissue microarray blocks were constructed as previously described (Chan et al. >>2009<<). Methods of immunohistochemical staining and interpretations for TP53 and CTNNB1 have been described previously (Baba et al. 2011; Morikawa et al. 2011).
n2:mentions: n3:19671906

Subject Item: _:vb40624430
rdf:type: n2:Context
rdf:value: Methods of immunohistochemical staining and interpretations for TP53 and CTNNB1 have been described previously (Baba et al. >>2011<<; Morikawa et al. 2011).
n2:mentions: n3:21425139

Subject Item: _:vb40624431
rdf:type: n2:Context
rdf:value: Methods of immunohistochemical staining and interpretations for TP53 and CTNNB1 have been described previously (Baba et al. 2011; Morikawa et al. >>2011<<). For LIN28A and LIN28B immunostaining, deparaffinized tissue sections were heated in a microwave for 15 min in antigen retrieval citra solution at pH 6 (BioGenex Laboratories). Tissue sections were incubated with dual endogenous enzyme
n2:mentions: n3:21521850

Subject Item: _:vb40624432
rdf:type: n5:Section
dc:title: results
n5:contains: _:vb40624436 _:vb40624437 _:vb40624438 _:vb40624439 _:vb40624433 _:vb40624434 _:vb40624435 _:vb40624444 _:vb40624445 _:vb40624446 _:vb40624447 _:vb40624440 _:vb40624441 _:vb40624442 _:vb40624443 _:vb40624452 _:vb40624448 _:vb40624449 _:vb40624450 _:vb40624451

Subject Item: _:vb40624433
rdf:type: n2:Context
rdf:value: were expressed at high levels in the early embryonic gut followed by a rapid decline after embryonic day 13.5 (E13.5), which coincides with a critical transition in intestinal epithelial differentiation (Gregorieff and Clevers >>2005<<). The expression of Lin28a and Lin28b was undetectable in the adult small intestine and colon (Fig.
n2:mentions: n3:15833914

Subject Item: _:vb40624434
rdf:type: n2:Context
rdf:value: Our conclusion that Lin28b expression is lacking in the adult gut contrasts with a recent study in which Lin28b staining was detected in the adult small intestine and colon by immunohistochemistry (Madison et al. >>2013<<). Using the same Lin28b antibody used in this prior study and examining control tissues from Lin28b knockout animals (Shinoda et al. 2013), we conclude that Lin28b expression is lacking in the adult gut (Supplemental Fig. 1B).
n2:mentions: n3:24142874

Subject Item: _:vb40624435
rdf:type: n2:Context
rdf:value: Using the same Lin28b antibody used in this prior study and examining control tissues from Lin28b knockout animals (Shinoda et al. >>2013<<), we conclude that Lin28b expression is lacking in the adult gut (Supplemental Fig.
n2:mentions: n3:23666760

Subject Item: _:vb40624436
rdf:type: n2:Context
rdf:value: 2A,B; Urbach et al. >>2014<<). To model reactivation, we fed doxycycline to adult mice but noted rapid deterioration and death in most of the iLin28a mice (Supplemental Fig.
n2:mentions: n3:24732380

Subject Item: _:vb40624437
rdf:type: n2:Context
rdf:value: Descendants of the TA progenitors exit the cell cycle and differentiate into specific epithelial lineages, including enterocytes, Paneth cells, goblet cells, neuroendocrine cells, M cells, and tuft cells (Clevers >>2013<<). During differentiation, cells migrate out of the crypts to the villi compartments, except for the Paneth cells, which migrate to the crypt base, where they intercalate with the ISCs and provide a favorable niche that sustains ISC
n2:mentions: n3:23870119

Subject Item: _:vb40624438
rdf:type: n2:Context
rdf:value: cells migrate out of the crypts to the villi compartments, except for the Paneth cells, which migrate to the crypt base, where they intercalate with the ISCs and provide a favorable niche that sustains ISC self-renewal (Sato et al. >>2011<<). Strikingly, intestinal induction of LIN28 expression resulted in strong perturbations to the highly ordered intestinal epithelia.
n2:mentions: n3:21113151

Subject Item: _:vb40624439
rdf:type: n2:Context
rdf:value: 2C–E), which are markers for invasive tumors and are often associated with metastatic CRC (Kikuchi et al. >>2000<<; Kusaba et al. 2005; Schwitalla et al. 2013).
n2:mentions: n3:10901373

Subject Item: _:vb40624440
rdf:type: n2:Context
rdf:value: 2C–E), which are markers for invasive tumors and are often associated with metastatic CRC (Kikuchi et al. 2000; Kusaba et al. >>2005<<; Schwitalla et al. 2013).
n2:mentions: n3:16049285

Subject Item: _:vb40624441
rdf:type: n2:Context
rdf:value: 2C–E), which are markers for invasive tumors and are often associated with metastatic CRC (Kikuchi et al. 2000; Kusaba et al. 2005; Schwitalla et al. >>2013<<). Notably, we failed to observe distal metastasis as late as 18 mo after doxycycline. The levels of the LIN28 proteins in the tumors were comparable with those in ESCs (Supplemental Fig. 3B,C), and, importantly, the tumors expressed
n2:mentions: n3:23273920

Subject Item: _:vb40624442
rdf:type: n2:Context
rdf:value: crossed iLIN28B animals with an inducible let-7 strain (iLet-7) engineered to express a chimeric pre-let-7g carrying the loop region of mir-21, thus rendering it refractory to LIN28 regulation (Supplemental Fig 3D; Piskounova et al. >>2008<<; Zhu et al. 2011). Strikingly, coexpression of the engineered let-7g almost completely reversed LIN28B-mediated tumorigenesis (Fig.
n2:mentions: n3:18550544

Subject Item: _:vb40624443
rdf:type: n2:Context
rdf:value: animals with an inducible let-7 strain (iLet-7) engineered to express a chimeric pre-let-7g carrying the loop region of mir-21, thus rendering it refractory to LIN28 regulation (Supplemental Fig 3D; Piskounova et al. 2008; Zhu et al. >>2011<<). Strikingly, coexpression of the engineered let-7g almost completely reversed LIN28B-mediated tumorigenesis (Fig.
n2:mentions: n3:21962509

Subject Item: _:vb40624444
rdf:type: n2:Context
rdf:value: this hypothesis, we performed targeted next-generation deep sequencing analysis of the nine most frequently mutated genes in human CRC—Apc, Tp53, Kras, Pik3ca, Fbxw7, Smad4, Tcf7L2, Nras, and Ctnnb1 (The Cancer Genome Atlas Network >>2012<<)—in 21 iLIN28 tumors (n = 10 for iLin28a, and n = 11 for iLIN28B).
n2:mentions: n3:22810696

Subject Item: _:vb40624445
rdf:type: n2:Context
rdf:value: 2L,M), all of which have been reported to play a role in β-catenin stabilization and Wnt hyperactivation in human CRC and other cancers (Koch et al. >>1999<<; Mirabelli-Primdahl et al. 1999).
n2:mentions: n3:9927029

Subject Item: _:vb40624446
rdf:type: n2:Context
rdf:value: 2L,M), all of which have been reported to play a role in β-catenin stabilization and Wnt hyperactivation in human CRC and other cancers (Koch et al. 1999; Mirabelli-Primdahl et al. >>1999<<). Other than Ctnnb1, we did not detect somatic mutations in the other eight genes sequenced. The heterozygous allele frequencies of Ctnnb1 in the mutated tumors ranged from 11.6% to 26% (Fig. 2M), indicating that 23.2%–52% of the tumor
n2:mentions: n3:10416591

Subject Item: _:vb40624447
rdf:type: n2:Context
rdf:value: As a previous report concluded that activated Wnt signaling up-regulates Lin28a in breast cancer cells (Cai et al. >>2013<<), we determined the levels of Lin28a in the ApcMin/+ tumors and failed to detect expression (Supplemental Fig.
n2:mentions: n3:23613467

Subject Item: _:vb40624448
rdf:type: n2:Context
rdf:value: In addition, we examined Lin28a/b status in the dextran sulfate sodium (DSS)/azoxymethane (AOM)-induced colon tumors, which manifest activated Wnt pathways (Rosenberg et al. >>2009<<). Similar to the ApcMin/+ tumors, reactivation of Lin28a or Lin28b was not observed (Supplemental Fig. 4B). Furthermore, intestine-specific conditional Lin28a and Lin28b double-knockout animals are equally susceptible to DSS/AOM-induced
n2:mentions: n3:19037092

Subject Item: _:vb40624449
rdf:type: n2:Context
rdf:value: By gene set enrichment analysis (GSEA) (Subramanian et al. >>2005<<), we detected enhanced molecular signatures related to cell cycle and WNT in iLIN28B; ApcMin/+ tumors (Supplemental Fig.
n2:mentions: n3:16199517

Subject Item: _:vb40624450
rdf:type: n2:Context
rdf:value: It is worth noting that LIN28A or LIN28B expression predicted survival probability better than KRAS, BRAF, or PIK3CA mutation in the same cohort of samples (Imamura et al. >>2012<<; Liao et al. 2012b; Lochhead et al. 2013).
n2:mentions: n3:22753589

Subject Item: _:vb40624451
rdf:type: n2:Context
rdf:value: It is worth noting that LIN28A or LIN28B expression predicted survival probability better than KRAS, BRAF, or PIK3CA mutation in the same cohort of samples (Imamura et al. 2012; Liao et al. 2012b; Lochhead et al. 2013).
n2:mentions: n3:22357840

Subject Item: _:vb40624452
rdf:type: n2:Context
rdf:value: It is worth noting that LIN28A or LIN28B expression predicted survival probability better than KRAS, BRAF, or PIK3CA mutation in the same cohort of samples (Imamura et al. 2012; Liao et al. 2012b; Lochhead et al. >>2013<<). Taken together, our analysis demonstrates strong association of the LIN28 proteins with invasive tumor progression and poor prognosis and provides evidence for LIN28 as a prognostic tumor biomarker for CRC.
n2:mentions: n3:23878352

Subject Item: _:vb40624453
rdf:type: n5:Section
dc:title: discussion
n5:contains: _:vb40624454 _:vb40624455 _:vb40624456 _:vb40624457 _:vb40624458 _:vb40624459 _:vb40624460

Subject Item: _:vb40624454
rdf:type: n2:Context
rdf:value: While prior murine models have used LIN28B exclusively (King et al. 2011a,b; Madison et al. 2013; Pang et al. 2014), we demonstrated an equally potent role of LIN28A in tumorigenesis and progression in both our murine model and human CRC.
n2:mentions: n3:21625210 n3:21512136

Subject Item: _:vb40624455
rdf:type: n2:Context
rdf:value: While prior murine models have used LIN28B exclusively (King et al. 2011a,b; Madison et al. >>2013<<; Pang et al. 2014), we demonstrated an equally potent role of LIN28A in tumorigenesis and progression in both our murine model and human CRC.
n2:mentions: n3:24142874

Subject Item: _:vb40624456
rdf:type: n2:Context
rdf:value: While prior murine models have used LIN28B exclusively (King et al. 2011a,b; Madison et al. 2013; Pang et al. >>2014<<), we demonstrated an equally potent role of LIN28A in tumorigenesis and progression in both our murine model and human CRC.
n2:mentions: n3:25360631

Subject Item: _:vb40624457
rdf:type: n2:Context
rdf:value: While an earlier study concluded that LIN28 activation alone can drive intestinal tumorigenesis in the absence of canonical genetic alterations (Madison et al. >>2013<<), we show that aberrant LIN28 expression results in widespread alterations in intestinal epithelial proliferation and differentiation but only focal tumor formation after a long latency, indicating a need for cooperating oncogenic events
n2:mentions: n3:24142874

Subject Item: _:vb40624458
rdf:type: n2:Context
rdf:value: While rare tumors have been reported with translocations involving LIN28B, and LIN28 is included as an amplified locus in a small percentage (1%–3%) of cancers (Viswanathan et al. >>2009<<), in most cases, LIN28 overexpression has not been linked to mutation, suggesting that LIN28 is not a classical “mut driver” oncogene but rather an “epi driver” according to a recent classification of the cancer genome landscape
n2:mentions: n3:19483683

Subject Item: _:vb40624459
rdf:type: n2:Context
rdf:value: LIN28 overexpression has not been linked to mutation, suggesting that LIN28 is not a classical “mut driver” oncogene but rather an “epi driver” according to a recent classification of the cancer genome landscape (Vogelstein et al. >>2013<<).
n2:mentions: n3:23539594

Subject Item: _:vb40624460
rdf:type: n2:Context
rdf:value: of tumor formation is largely correlated with the number of stem cells residing in the respective tissues and that mouse small intestines contain higher numbers of cycling stem cells than mouse colons (Tomasetti and Vogelstein >>2015<<).
n2:mentions: n3:25554788

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