RIP140 increases APC expression and controls intestinal homeostasis and tumorigenesis

Journal of Clinical Investigation

Volumn 124, Issue 5, 2014, Pages 1899-1913

  Lapierre, Marion ^a   Bonnet, Sandrine ^a   Bascoul Mollevi, Caroline ^b   Ait Arsa, Imade ^a   Jalaguier, Stéphan ^a   Del Rio, Maguy ^a   Plateroti, Michela ^c   Roepman, Paul ^d,e   Ychou, Marc ^b   Pannequin, Julie ^f   Hollande, Frédéric ^f   Parker, Malcolm ^g   Cavailles, Vincent ^a  

^a INSERM   (France)

^b CENTRE VAL D AURELLE   (France)

^c CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^d Agendia NV   (Netherlands)

^e Agendia Inc   (United States)

^f INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; CYCLINE; LYSOZYME; MESSENGER RNA; MUCIN 2; RECEPTOR INTERACTING PROTEIN 140; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; CANCER CELL; CANCER PROGNOSIS; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL POPULATION; CELL PROLIFERATION; CHROMOSOME 5Q; COLON ADENOCARCINOMA; COMPARATIVE STUDY; CONTROLLED STUDY; CRYPT CELL; FLUORESCENCE ANALYSIS; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GOBLET CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTESTINE; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; IONIZING RADIATION; MICROSATELLITE INSTABILITY; MOUSE; NONHUMAN; PANETH CELL; PHENOTYPE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROMOTER REGION; PROTEIN EXPRESSION; REVIEW; TRANSCRIPTION REGULATION; UPREGULATION; WHOLE BODY RADIATION; WNT SIGNALING PATHWAY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HOMEOSTASIS; HUMANS; INTESTINAL MUCOSA; MALE; MICE; MICE, KNOCKOUT; MICE, NUDE; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS;

EID: 84899720980     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI65178     Document Type: Review

References (48)

1. Schneikert J, Behrens J. The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut. 2007;56(3):417-425.
2. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer. 2008;8(5):387-398.
3. Zeng X, et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature. 2005;438(7069):873-877.
4. Kwong LN, Dove WF. APC and its modifiers in colon cancer. Adv Exp Med Biol. 2009;656:85-106.
5. Colnot S, et al. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab Invest. 2004;84(12):1619-1630.
6. Cavailles V, et al. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 1995;14(15):3741-3751.
7. Augereau P, et al. The nuclear receptor transcriptional coregulator RIP140. Nucl Recept Signal. 2006;4:e024.
8. Docquier A, et al. The transcriptional coregulator RIP140 represses E2F1 activity and discriminates breast cancer subtypes. Clin Cancer Res. 2010; 16(11):2959-2970.
9. Christian M, Tullet JM, Parker MG. Characterization of four autonomous repression domains in the corepressor receptor interacting protein 140. J Biol Chem. 2004;279(15):15645-15651.
10. Yang X-J, Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell. 2008;31(4):449-461.
11. Docquier A, et al. The RIP140 gene is a transcriptional target of E2F1. PLoS One. 2012;7(5):e35839.
12. White R, et al. The nuclear receptor co-repressor nrip1 (RIP140) is essential for female fertility. Nat Med. 2000;6(12):1368-1374.
13. Leonardsson G, et al. Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc Natl Acad Sci U S A. 2004;101(22):8437-8442.
14. Duclot F, et al. Cognitive impairments in adult mice with constitutive inactivation of RIP140 gene expression. Genes Brain Behav. 2012;11(1):69-78.
15. Nautiyal J, et al. The transcriptional co-factor RIP140 regulates mammary gland development by promoting the generation of key mitogenic signals. Development. 2013;140(5):1079-1089.
16. Fritah A, Christian M, Parker MG. The metabolic coregulator RIP140: an update. Am J Physiol Endocrinol Metab. 2010;299(3):E335-E340.
17. Van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009;71:241-260.
18. MacDonald BT, Tamai K, He X. Wnt/-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17(1):9-26.
19. Tan CW, et al. Wnt signalling pathway parameters for mammalian cells. PLoS One. 2012;7(2):e31882.
20. Hlubek F, et al. Heterogeneous expression of Wnt/-catenin target genes within colorectal cancer. Int J Cancer. 2007;121(9):1941-1948.
21. Kim TH, Xiong H, Zhang Z, Ren B. Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene. 2005;24(4):597-604.
22. Rodilla V, et al. Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci U S A. 2009;106(15):6315-6320.
23. Mann B, et al. Target genes of catenin-T cell-factor/ lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci U S A. 1999;96(4):1603-1608.
24. Van Es JH, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol. 2005;7(4):381-386.
25. Zilliacus J, et al. Regulation of glucocorticoid receptor activity by 14-3-3-dependent intracellular relocalization of the corepressor RIP140. Mol Endocrinol. 2001;15(4):501-511.
26. Jaiswal AS, Balusu R, Narayan S. 7,12-Dimethylbenzanthracene- dependent transcriptional regulation of adenomatous polyposis coli (APC) gene expression in normal breast epithelial cells is mediated by GC-box binding protein Sp3. Carcinogenesis. 2006;27(2):252-261.
27. Jaiswal AS, Narayan S. Upstream stimulating factor-1 (USF1) and USF2 bind to and activate the promoter of the adenomatous polyposis coli (APC) tumor suppressor gene. J Cell Biochem. 2001; 81(2):262-277.
28. Castet A, et al. Receptor-interacting protein 140 differentially regulates estrogen receptor-related receptor transactivation depending on target genes. Mol Endocrinol. 2006;20(5):1035-1047.
29. Nishisho I, et al. Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science. 1991;253(5020):665-669.
30. Del Rio M, et al. Gene expression signature in advanced colorectal cancer patients select drugs and response for the use of leucovorin, fluorouracil, and irinotecan. J Clin Oncol. 2007;25(7):773-780.
31. Salazar R, et al. Gene expression signature to improve prognosis prediction of stage II and III colorectal cancer. J Clin Oncol. 2011;29(1):17-24.
32. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology. 2007;50(1):113-130.
33. Sansom OJ, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 2004;18(12):1385-1390.
34. Modica S, et al. The intestinal nuclear receptor signature with epithelial localization patterns and expression modulation in tumors. Gastroenterology. 2010;138(2):636-648.
35. D'Errico I, Moschetta A. Nuclear receptors, intestinal architecture and colon cancer: an intriguing link. Cell Mol Life Sci. 2008;65(10):1523-1543.
36. Mulholland DJ, Dedhar S, Coetzee GA, Nelson CC. Interaction of nuclear receptors with the Wnt/- catenin/Tcf signaling axis: Wnt you like to know? Endocr Rev. 2005;26(7):898-915.
37. Garneau H, Paquin M-C, Carrier JC, Rivard N. E2F4 expression is required for cell cycle progression of normal intestinal crypt cells and colorectal cancer cells. J Cell Physiol. 2009;221(2):350-358.
38. Guo J, Longshore S, Nair R, Warner BW. Retinoblastoma protein (pRb), but not p107 or p130, is required for maintenance of enterocyte quiescence and differentiation in small intestine. J Biol Chem. 2009;284(1):134-140.
39. Chandra SHV, Wacker I, Appelt UK, Behrens J, Schneikert J. A common role for various human truncated adenomatous polyposis coli isoforms in the control of catenin activity and cell proliferation. PLoS One. 2012;7(4):e34479.
40. Andreu P, et al. Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development. 2005; 132(6):1443-1451.
41. Hoverter NP, Waterman ML. A Wnt-fall for gene regulation: repression. Sci Signal. 2008;1(39):pe43.
42. Blauwkamp TA, Chang MV, Cadigan KM. Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 2008;27(10):1436-1446.
43. Nannini M, et al. Gene expression profiling in colorectal cancer using microarray technologies: results and perspectives. Cancer Treat Rev. 2009;35(3):201-209.
44. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487(7407):330-337.
45. Mori Y, et al. Identification of genes uniquely involved in frequent microsatellite instability colon carcinogenesis by expression profiling combined with epigenetic scanning. Cancer Res. 2004; 64(7):2434-2438.
46. Weiser MM. Intestinal epithelial cell surface membrane glycoprotein synthesis. II. Glycosyltransferases and endogenous acceptors of the undifferentiated cell surface membrane. J Biol Chem. 1973;248(7):2542-2548.
47. Shibamoto S, et al. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells. 1998;3(10):659-670.
48. Castet A, et al. Multiple domains of the receptor-interacting protein 140 contribute to transcription inhibition. Nucleic Acids Res. 2004;32(6):1957- 1966.