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n2:pmcid: PMC0
bibo:doi: 10.1101%2Fgad.224659.113
n5:contains: _:vb25873399 _:vb25873380 _:vb25873378

Subject Item: _:vb25873378
rdf:type: n5:Section
dc:title: materials and methods
n5:contains: _:vb25873379

Subject Item: _:vb25873379
rdf:type: n2:Context
rdf:value: Crypt villus epithelial fractionation for RT–PCR was carried out as described previously (Flint et al. >>1991<<). For analysis of mTOR signaling by immunoblots, ∼5 cm of proximal jejunum was incubated in ice-cold CMF-HBSS containing 0.5 mM DTT and 10 mM EDTA on a rocking platform for 45 min. Intestine epithelium was isolated as above, and crypts
n2:mentions: n3:1747105

Subject Item: _:vb25873380
rdf:type: n5:Section
dc:title: results
n5:contains: _:vb25873396 _:vb25873397 _:vb25873398 _:vb25873392 _:vb25873393 _:vb25873394 _:vb25873395 _:vb25873381 _:vb25873382 _:vb25873383 _:vb25873388 _:vb25873389 _:vb25873390 _:vb25873391 _:vb25873384 _:vb25873385 _:vb25873386 _:vb25873387

Subject Item: _:vb25873381
rdf:type: n2:Context
rdf:value: Analysis of Lgr5-positive cells, which marks a population of intestinal epithelial stem cells (Sato et al. >>2009<<; Barker and Clevers 2010), revealed that Lin28b is not expressed at significantly higher level in this population, consistent with immunohistochemistry (IHC) showing expression primarily in the upper region of the crypt (Supplemental Fig.
n2:mentions: n3:19329995

Subject Item: _:vb25873382
rdf:type: n2:Context
rdf:value: Analysis of Lgr5-positive cells, which marks a population of intestinal epithelial stem cells (Sato et al. 2009; Barker and Clevers >>2010<<), revealed that Lin28b is not expressed at significantly higher level in this population, consistent with immunohistochemistry (IHC) showing expression primarily in the upper region of the crypt (Supplemental Fig.
n2:mentions: n3:20417836

Subject Item: _:vb25873383
rdf:type: n2:Context
rdf:value: Transgenic mice were generated to target high-level expression of Lin28b to the intestinal epithelium using the 13-kb mouse Vil1 promoter (Madison et al. >>2002<<). Four lines of Vil-Lin28b mice were generated, with three exhibiting continuous expression at three different levels (low, medium, and high) and one line exhibiting variegated expression (Fig.
n2:mentions: n3:12065599

Subject Item: _:vb25873384
rdf:type: n2:Context
rdf:value: chromosome 15) and Let-7a3 (at 22q13.31 in humans) share an atypical terminal loop, which lacks both the GRAG motif (recognized by the CCHC domain of LIN28B) and the GNGAY motif (recognized by the CSD domain of LIN28B) (Nam et al. >>2011<<). Let-7b, which is normally expressed at very high levels, is also moderately affected by LIN28B expression (Fig.
n2:mentions: n3:22078496

Subject Item: _:vb25873385
rdf:type: n2:Context
rdf:value: 2A; Chi et al. >>2009<<; Zhang and Darnell 2011). Samples were prepared from colonic epithelia of Vil-Lin28bMed mice (two replicates), Caco-2 cells (three replicates), and DLD1 and Lovo cell lines (one replicate each) with a doxycycline-inducible LIN28B (Fig.
n2:mentions: n3:19536157

Subject Item: _:vb25873386
rdf:type: n2:Context
rdf:value: 2A; Chi et al. 2009; Zhang and Darnell >>2011<<). Samples were prepared from colonic epithelia of Vil-Lin28bMed mice (two replicates), Caco-2 cells (three replicates), and DLD1 and Lovo cell lines (one replicate each) with a doxycycline-inducible LIN28B (Fig.
n2:mentions: n3:21633356

Subject Item: _:vb25873387
rdf:type: n2:Context
rdf:value: To identify sites of intimate contact between RNA and protein, we exploited the phenomenon whereby UV cross-linking generates an irreversible adduct between an aromatic amino acid and the base of RNA or DNA (Zhang and Darnell >>2011<<). RT frequently bypasses this covalently linked amino acid, resulting in a cross-link-induced mutation site (CIMS); these sites are almost exclusively deletions. We also performed CLIP-seq on isolated jejunum crypts from Vil-Lin28bHi mice
n2:mentions: n3:21633356

Subject Item: _:vb25873388
rdf:type: n2:Context
rdf:value: as determined by microarray and CLIP-seq analysis (enriched transcripts [black]; enriched transcripts with CIMSs [red]) of Vil-Lin28b colonic epithelium (D) and DLD1 and Lovo cells (E) (DLD1 and Lovo microarrays from King et al. 2011a). (F) Kyoto Encyclopedia of Genes and Genomics (KEGG) (Ogata et al. 1999) and WikiPathway (Pico et al. 2008) categories enriched for CLIP-seq target sets identified from Vil-Lin28b jejunum crypts, Vil-Lin28b colon epithelium, and Caco-2,
n2:mentions: n3:21512136

Subject Item: _:vb25873389
rdf:type: n2:Context
rdf:value: (F) Kyoto Encyclopedia of Genes and Genomics (KEGG) (Ogata et al. >>1999<<) and WikiPathway (Pico et al. 2008) categories enriched for CLIP-seq target sets identified from Vil-Lin28b jejunum crypts, Vil-Lin28b colon epithelium, and Caco-2, DLD1, and Lovo cells.
n2:mentions: n3:9847135

Subject Item: _:vb25873390
rdf:type: n2:Context
rdf:value: (F) Kyoto Encyclopedia of Genes and Genomics (KEGG) (Ogata et al. 1999) and WikiPathway (Pico et al. >>2008<<) categories enriched for CLIP-seq target sets identified from Vil-Lin28b jejunum crypts, Vil-Lin28b colon epithelium, and Caco-2, DLD1, and Lovo cells.
n2:mentions: n3:18651794

Subject Item: _:vb25873391
rdf:type: n2:Context
rdf:value: De novo motif analysis (MEME) (Bailey et al. >>2006<<) of robust CIMSs from Caco-2 cells yielded two motifs, one of which resembles the GGAG or GAAG consensus binding site found in the preE region of Let-7 pre-miRNAs (Supplemental Fig.
n2:mentions: n3:16845028

Subject Item: _:vb25873392
rdf:type: n2:Context
rdf:value: This contrasts previous studies in HEK293 cells reporting that LIN28B modestly augments target mRNA levels but does not likely affect mRNA translation (Hafner et al. >>2013<<).
n2:mentions: n3:23481595

Subject Item: _:vb25873393
rdf:type: n2:Context
rdf:value: 3A,B), and an intestinal epithelial cell knockout (IEC-KO) was generated by crosses to Vil-Cre mice (Fig. 3C; Madison et al. >>2002<<), referred to here as Let7IEC-KO mice.
n2:mentions: n3:12065599

Subject Item: _:vb25873394
rdf:type: n2:Context
rdf:value: We suspected that increased mucosal growth occurred via increased rates of crypt fission, a process of gland division that occurs during intestinal growth (St Clair and Osborne >>1985<<; Li et al. 1994).
n2:mentions: n3:3986870

Subject Item: _:vb25873395
rdf:type: n2:Context
rdf:value: We suspected that increased mucosal growth occurred via increased rates of crypt fission, a process of gland division that occurs during intestinal growth (St Clair and Osborne 1985; Li et al. >>1994<<). Quantification in Let7IEC-KO weanlings revealed an increased fraction of fissile crypts (Fig. 1J). This partial recapitulation of the Vil-Lin28b phenotype indicated that Let-7 controls intestinal growth. An increased rate of crypt
n2:mentions: n3:7535783

Subject Item: _:vb25873396
rdf:type: n2:Context
rdf:value: The ability to promote both proliferation and apoptosis (or senescence) is a hallmark of oncogenes such as MYC or mutant KRAS (Evan et al. >>1992<<; Brooks et al. 2001).
n2:mentions: n3:1555236

Subject Item: _:vb25873397
rdf:type: n2:Context
rdf:value: The ability to promote both proliferation and apoptosis (or senescence) is a hallmark of oncogenes such as MYC or mutant KRAS (Evan et al. 1992; Brooks et al. >>2001<<). This phenomenon indicates the presence of a signaling circuitry that provides negative feedback, perhaps to remove aberrant cells and prevent uncontrolled proliferation.
n2:mentions: n3:11360198

Subject Item: _:vb25873398
rdf:type: n2:Context
rdf:value: Previous reports have linked Let-7 to the regulation of the PI3K–Akt–mTOR signaling pathway (Zhu et al. >>2011<<), and RNA expression analysis of epithelium from Vil-Lin28b mice suggested that Lin28b may regulate genes involved in metabolism and caloric restriction (Supplemental Fig.
n2:mentions: n3:21962509

Subject Item: _:vb25873399
rdf:type: n5:Section
dc:title: discussion
n5:contains: _:vb25873416 _:vb25873417 _:vb25873418 _:vb25873419 _:vb25873408 _:vb25873409 _:vb25873410 _:vb25873411 _:vb25873412 _:vb25873413 _:vb25873414 _:vb25873415 _:vb25873400 _:vb25873401 _:vb25873402 _:vb25873403 _:vb25873404 _:vb25873405 _:vb25873406 _:vb25873407

Subject Item: _:vb25873400
rdf:type: n2:Context
rdf:value: This is consistent with human epidemiological data illustrating that increased LIN28B levels are observed at early stages of colorectal cancer (King et al. 2011a; Piskounova et al. 2011), with high expression at both stages I and II disease correlating inversely with patient survival and higher probability of recurrence (King et al. 2011a).
n2:mentions: n3:21512136

Subject Item: _:vb25873401
rdf:type: n2:Context
rdf:value: This is consistent with human epidemiological data illustrating that increased LIN28B levels are observed at early stages of colorectal cancer (King et al. 2011a; Piskounova et al. >>2011<<), with high expression at both stages I and II disease correlating inversely with patient survival and higher probability of recurrence (King et al. 2011a).
n2:mentions: n3:22118463

Subject Item: _:vb25873402
rdf:type: n2:Context
rdf:value: at early stages of colorectal cancer (King et al. 2011a; Piskounova et al. 2011), with high expression at both stages I and II disease correlating inversely with patient survival and higher probability of recurrence (King et al. 2011a).
n2:mentions: n3:21512136

Subject Item: _:vb25873403
rdf:type: n2:Context
rdf:value: While PI3K–mTOR signaling appears to regulate animal size via effects in myoblasts and muscle tissue (Zhu et al. >>2011<<), our data indicate that in the intestine, Let-7 is critical for repression of Hmga2, Igf2bp1, Igf2bp2, E2f5, Acvr1c, and Nr6a1.
n2:mentions: n3:21962509

Subject Item: _:vb25873404
rdf:type: n2:Context
rdf:value: In wild-type mouse crypts, we observed localization of LIN28B in the nucleus, where it likely sequesters Let-7 from the microprocessor machinery (Piskounova et al. >>2011<<). Indeed, Let-7 levels are lowest in the crypt, and the known Let-7 target Hmga2 exhibits an expression pattern highly similar to endogenous LIN28B (expression in the upper crypt with diminishing levels toward villus tips). The Let-7
n2:mentions: n3:22118463

Subject Item: _:vb25873405
rdf:type: n2:Context
rdf:value: The Let-7 target Hmga2 alone is capable of driving proliferation (Lee and Dutta >>2007<<) and has been reported to repress Ink4a/Arf (Cdkn2a) and potentiate E2F1 activity through the inhibition of Rb (Fedele et al. 2006; Nishino et al. 2008).
n2:mentions: n3:17437991

Subject Item: _:vb25873406
rdf:type: n2:Context
rdf:value: The Let-7 target Hmga2 alone is capable of driving proliferation (Lee and Dutta 2007) and has been reported to repress Ink4a/Arf (Cdkn2a) and potentiate E2F1 activity through the inhibition of Rb (Fedele et al. >>2006<<; Nishino et al. 2008).
n2:mentions: n3:16766265

Subject Item: _:vb25873407
rdf:type: n2:Context
rdf:value: The Let-7 target Hmga2 alone is capable of driving proliferation (Lee and Dutta 2007) and has been reported to repress Ink4a/Arf (Cdkn2a) and potentiate E2F1 activity through the inhibition of Rb (Fedele et al. 2006; Nishino et al. >>2008<<). In colorectal cancer, high Hmga2 expression correlates with metastasis and poor survival in patients (Wang et al. 2011).
n2:mentions: n3:18957199

Subject Item: _:vb25873408
rdf:type: n2:Context
rdf:value: Hmga2 is responsible for the mouse pygmy phenotype, which occurs independently of growth hormone and insulin-like growth factor signaling and illustrates the critical effects of Hmga2 on growth (Zhou et al. >>1995<<). Hmga2 is the most dramatically up-regulated Let-7 target gene in the crypts of our animal models of Let-7 repression. In our rescue experiments with the iiLet7 transgene, Hmga2 is also the most significantly repressed Let-7 target,
n2:mentions: n3:7651535

Subject Item: _:vb25873409
rdf:type: n2:Context
rdf:value: Igf2bp1 and Igf2bp2 may also be important regulators of mucosal growth in the intestine, as this family of RNA-binding proteins is implicated in regulating proliferation and differentiation, among other processes (Bell et al. >>2013<<; Hamilton et al. 2013).
n2:mentions: n3:23069990

Subject Item: _:vb25873410
rdf:type: n2:Context
rdf:value: While Paneth cells have been reported to provide niche signals for Lgr5+ stem cells (Sato et al. >>2011<<), we did not see any effects on this stem cell population in Vil-Lin28b mice (data not shown).
n2:mentions: n3:21113151

Subject Item: _:vb25873411
rdf:type: n2:Context
rdf:value: This is consistent with an alternative hypothesis showing that Paneth cells are dispensable in vivo (Durand et al. >>2012<<). Conversely, we saw increased proliferation throughout the crypt upon depletion of Let-7 in vivo, indicating that Let-7 may supersede any detrimental effects on cellular proliferation caused by Paneth cell reduction. However, Paneth
n2:mentions: n3:22586121

Subject Item: _:vb25873412
rdf:type: n2:Context
rdf:value: In our previous studies, we showed that LIN28B promoted metastasis of colon cancer in xenograft tumor models (King et al. 2011a). However, we also observed that LIN28B-overexpressing cell lines generated primary tumors that appeared more glandular and differentiated (possessing epithelial morphology) compared with empty vector cell lines (King et al. 2011a).
n2:mentions: n3:21512136

Subject Item: _:vb25873413
rdf:type: n2:Context
rdf:value: However, we also observed that LIN28B-overexpressing cell lines generated primary tumors that appeared more glandular and differentiated (possessing epithelial morphology) compared with empty vector cell lines (King et al. 2011a). This also appears consistent with other studies in which LIN28B-expressing adenocarcinomas appear more glandular, whereas LIN28A-expressing tumors appear poorly differentiated (Piskounova et al. 2011). Thus, although Let-7 repression is
n2:mentions: n3:21512136

Subject Item: _:vb25873414
rdf:type: n2:Context
rdf:value: This also appears consistent with other studies in which LIN28B-expressing adenocarcinomas appear more glandular, whereas LIN28A-expressing tumors appear poorly differentiated (Piskounova et al. >>2011<<). Thus, although Let-7 repression is a common theme, the effects on tissue differentiation are likely divergent for LIN28A and LIN28B. Such a differential role may be reflected in our observation that LIN28A is not expressed in the adult
n2:mentions: n3:22118463

Subject Item: _:vb25873415
rdf:type: n2:Context
rdf:value: role may be reflected in our observation that LIN28A is not expressed in the adult intestine epithelium and is similarly absent from other adult tissues but is highly expressed in primordial germ cells and ES cells (West et al. >>2009<<). Divergent or antagonistic functions of LIN28A and LIN28B could also explain why tumors frequently express either LIN28A or LIN28B but not both (Viswanathan et al. 2009; Piskounova et al. 2011).
n2:mentions: n3:19578360

Subject Item: _:vb25873416
rdf:type: n2:Context
rdf:value: Divergent or antagonistic functions of LIN28A and LIN28B could also explain why tumors frequently express either LIN28A or LIN28B but not both (Viswanathan et al. >>2009<<; Piskounova et al. 2011).
n2:mentions: n3:19483683

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rdf:value: Divergent or antagonistic functions of LIN28A and LIN28B could also explain why tumors frequently express either LIN28A or LIN28B but not both (Viswanathan et al. 2009; Piskounova et al. >>2011<<). We observed that endogenous and exogenous LIN28B becomes localized to the cytoplasm in the differentiated intestinal epithelium and differentiating Caco-2 cells (data not shown), which may reflect contrasting roles in differentiated
n2:mentions: n3:22118463

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rdf:value: A recent study revealed that LIN28A binds mRNAs that encode secreted and transmembrane proteins and specifically represses their translation in the ER (Cho et al. >>2012<<). Conversely, we observed positive effects on protein translation as well as enrichment for the functional category “protein processing in the ER,” which was observed in all cell types. Interestingly, ER-associated chaperone expression
n2:mentions: n3:23102813

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rdf:value: normal epithelial differentiation in the intestine, where the transcription factor XBP1, a mediator of the unfolded protein response, is specifically expressed in transit-amplifying and post-mitotic epithelial cells (Schwitalla et al. >>2013<<).
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