Cohesin Rad21 Mediates Loss of Heterozygosity and Is Upregulated via Wnt Promoting Transcriptional Dysregulation in Gastrointestinal Tumors

Cell Reports

Volumn 9, Issue 5, 2014, Pages 1781-1797

  Xu, Huiling ^a,b   Yan, Yuqian ^a   Deb, Siddhartha ^c,d   Rangasamy, Danny ^e   Germann, Markus ^a,b   Malaterre, Jordane ^a,b   Eder, Noreen C ^a   Ward, Robyn L ^f   Hawkins, Nicholas J ^g   Tothill, Richard W ^c   Chen, Long ^e   Mortensen, Neil J ^h   Fox, Stephen B ^b,c   McKay, Michael J ⁱ   Ramsay, Robert G ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PMCC   (Australia)

^d Victorian Cancer Agency   (Australia)

^e Australian National University   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g UNIVERSITY OF NEW SOUTH WALES   (Australia)

^h CHURCHILL HOSPITAL   (United Kingdom)

ⁱ UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; COHESIN; RAD21 PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; RAD21 PROTEIN, HUMAN; RETROPOSON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON CARCINOGENESIS; COLORECTAL ADENOMA; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; EX VIVO STUDY; GENE EXPRESSION; GENOME ANALYSIS; GENOMIC INSTABILITY; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; LONG INTERSPERSED REPEAT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; RAD21 GENE; RETROPOSON; TRANSCRIPTION REGULATION; UPREGULATION; ADULT STEM CELL; ANIMAL; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; COLON; COLON POLYPOSIS; DNA DAMAGE; GENE EXPRESSION REGULATION; GENETICS; HAPLOINSUFFICIENCY; HCT116 CELL LINE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ADENOMATOUS POLYPOSIS COLI; ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; COLON; DNA DAMAGE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HAPLOINSUFFICIENCY; HCT116 CELLS; HUMANS; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; PHOSPHOPROTEINS; RETROELEMENTS; UP-REGULATION;

EID: 84915821343     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.10.059     Document Type: Article

References (47)

1. Akcora D., Huynh D., Lightowler S., Germann M., Robine S., de May J.R., Pollard J.W., Stanley E.R., Malaterre J., Ramsay R.G. The CSF-1 receptor fashions the intestinal stem cell niche. Stem Cell Res. (Amst.) 2013, 10:203-212.
2. Baba Y., Murata A., Watanabe M., Baba H. Clinical implications of the LINE-1 methylation levels in patients with gastrointestinal cancer. Surg. Today 2014, 44:1807-1816.
3. Barber T.D., McManus K., Yuen K.W., Reis M., Parmigiani G., Shen D., Barrett I., Nouhi Y., Spencer F., Markowitz S., et al. Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers. Proc. Natl. Acad. Sci. USA 2008, 105:3443-3448.
4. Barker N., Ridgway R.A., van Es J.H., van de Wetering M., Begthel H., van den Born M., Danenberg E., Clarke A.R., Sansom O.J., Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
5. Caldwell C.M., Green R.A., Kaplan K.B. APC mutations lead to cytokinetic failures invitro and tetraploid genotypes in Min mice. J.Cell Biol. 2007, 178:1109-1120.
6. Clevers H., Nusse R. Wnt/β-catenin signaling and disease. Cell 2012, 149:1192-1205.
7. Cottrell S., Bicknell D., Kaklamanis L., Bodmer W.F. Molecular analysis of APC mutations in familial adenomatous polyposis and sporadic colon carcinomas. Lancet 1992, 340:626-630.
8. Deardorff M.A., Wilde J.J., Albrecht M., Dickinson E., Tennstedt S., Braunholz D., Mönnich M., Yan Y., Xu W., Gil-Rodríguez M.C., et al. RAD21 mutations cause a human cohesinopathy. Am. J. Hum. Genet. 2012, 90:1014-1027.
9. Deb S., Xu H., Tuynman J., George J., Yan Y., Li J., Ward R.L., Mortensen N., Hawkins N.J., McKay M.J., et al. RAD21 cohesin overexpression is a prognostic and predictive marker exacerbating poor prognosis in KRAS mutant colorectal carcinomas. Br. J. Cancer 2014, 110:1606-1613.
10. Dikovskaya D., Schiffmann D., Newton I.P., Oakley A., Kroboth K., Sansom O., Jamieson T.J., Meniel V., Clarke A., Näthke I.S. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J.Cell Biol. 2007, 176:183-195.
11. Dorsett D. Cohesin: genomic insights into controlling gene transcription and development. Curr. Opin. Genet. Dev. 2011, 21:199-206.
12. Faux M.C., Ross J.L., Meeker C., Johns T., Ji H., Simpson R.J., Layton M.J., Burgess A.W. Restoration of full-length adenomatous polyposis coli (APC) protein in a colon cancer cell line enhances cell adhesion. J.Cell Sci. 2004, 117:427-439.
13. Fleming E.S., Temchin M., Wu Q., Maggio-Price L., Tirnauer J.S. Spindle misorientation in tumors from APC(min/+) mice. Mol. Carcinog. 2009, 48:592-598.
14. Guillou E., Ibarra A., Coulon V., Casado-Vela J., Rico D., Casal I., Schwob E., Losada A., Méndez J. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 2010, 24:2812-2822.
15. Haering C.H., Farcas A.M., Arumugam P., Metson J., Nasmyth K. The cohesin ring concatenates sister DNA molecules. Nature 2008, 454:297-301.
16. Haigis K.M., Dove W.F. A Robertsonian translocation suppresses a somatic recombination pathway to loss of heterozygosity. Nat. Genet. 2003, 33:33-39.
17. Iskow R.C., McCabe M.T., Mills R.E., Torene S., Pittard W.S., Neuwald A.F., Van Meir E.G., Vertino P.M., Devine S.E. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 2010, 141:1253-1261.
18. Jessberger R. Cohesin's dual role in the DNA damage response: repair and checkpoint activation. EMBO J. 2009, 28:2491-2493.
19. Johnson D.S., Mortazavi A., Myers R.M., Wold B. Genome-wide mapping of invivo protein-DNA interactions. Science 2007, 316:1497-1502.
20. Kagey M.H., Newman J.J., Bilodeau S., Zhan Y., Orlando D.A., van Berkum N.L., Ebmeier C.C., Goossens J., Rahl P.B., Levine S.S., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
21. Kong X., Ball A.R., Sonoda E., Feng J., Takeda S., Fukagawa T., Yen T.J., Yokomori K. Cohesin associates with spindle poles in a mitosis-specific manner and functions in spindle assembly in vertebrate cells. Mol. Biol. Cell 2009, 20:1289-1301.
22. Lee E., Iskow R., Yang L., Gokcumen O., Haseley P., Luquette L.J., Lohr J.G., Harris C.C., Ding L., Wilson R.K., et al. Landscape of somatic retrotransposition in human cancers. Science 2012, 337:967-971. Cancer Genome Atlas Research Network.
23. Mazoyer S. Genomic rearrangements in the BRCA1 and BRCA2 genes. Hum. Mutat. 2005, 25:415-422.
24. McKay M.J., Troelstra C., van der Spek P., Kanaar R., Smit B., Hagemeijer A., Bootsma D., Hoeijmakers J.H. Sequence conservation of the rad21 Schizosaccharomyces pombe DNA double-strand break repair gene in human and mouse. Genomics 1996, 36:305-315.
25. Møllersen L., Paulsen J.E., Alexander J. Loss of heterozygosity and nonsense mutation in Apc in azoxymethane-induced colonic tumours in min mice. Anticancer Res. 2004, 24(5A):2595-2599.
26. Moreb J.S. Aldehyde dehydrogenase as a marker for stem cells. Curr. Stem Cell Res. Ther. 2008, 3:237-246.
27. Moser A.R., Dove W.F., Roth K.A., Gordon J.I. The Min (multiple intestinal neoplasia) mutation: its effect on gut epithelial cell differentiation and interaction with a modifier system. J.Cell Biol. 1992, 116:1517-1526.
28. Moynahan M.E., Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 2010, 11:196-207.
29. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 2001, 35:673-745.
30. Nigumann P., Redik K., Mätlik K., Speek M. Many human genes are transcribed from the antisense promoter of L1 retrotransposon. Genomics 2002, 79:628-634.
31. Patnala R., Lee S.H., Dahlstrom J.E., Ohms S., Chen L., Dheen S.T., Rangasamy D. Inhibition of LINE-1 retrotransposon-encoded reverse transcriptase modulates the expression of cell differentiation genes in breast cancer cells. Breast Cancer Res. Treat. 2014, 143:239-253.
32. Pierce A.J., Johnson R.D., Thompson L.H., Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999, 13:2633-2638.
33. Rhodes J.M., Bentley F.K., Print C.G., Dorsett D., Misulovin Z., Dickinson E.J., Crosier K.E., Crosier P.S., Horsfield J.A. Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. Dev. Biol. 2010, 344:637-649.
34. Sato T., Vries R.G., Snippert H.J., van de Wetering M., Barker N., Stange D.E., van Es J.H., Abo A., Kujala P., Peters P.J., Clevers H. Single Lgr5 stem cells build crypt-villus structures invitro without a mesenchymal niche. Nature 2009, 459:262-265.
35. Sato T., van Es J.H., Snippert H.J., Stange D.E., Vries R.G., van den Born M., Barker N., Shroyer N.F., van de Wetering M., Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469:415-418.
36. Schaaf C.A., Misulovin Z., Gause M., Koenig A., Gohara D.W., Watson A., Dorsett D. Cohesin and polycomb proteins functionally interact to control transcription at silenced and active genes. PLoS Genet. 2013, 9:e1003560.
37. Sonoda E., Sasaki M.S., Morrison C., Yamaguchi-Iwai Y., Takata M., Takeda S. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 1999, 19:5166-5169.
38. Spirio L.N., Samowitz W., Robertson J., Robertson M., Burt R.W., Leppert M., White R. Alleles of APC modulate the frequency and classes of mutations that lead to colon polyps. Nat. Genet. 1998, 20:385-388.
39. van Es J.H., Jay P., Gregorieff A., van Gijn M.E., Jonkheer S., Hatzis P., Thiele A., van den Born M., Begthel H., Brabletz T., et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat. Cell Biol. 2005, 7:381-386.
40. Wong R.W., Blobel G. Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc. Natl. Acad. Sci. USA 2008, 105:15441-15445.
41. Xu H., Beasley M., Verschoor S., Inselman A., Handel M.A., McKay M.J. A new role for the mitotic RAD21/SCC1 cohesin in meiotic chromosome cohesion and segregation in the mouse. EMBO Rep. 2004, 5:378-384.
42. Xu H., Balakrishnan K., Malaterre J., Beasley M., Yan Y., Essers J., Appeldoorn E., Tomaszewski J.M., Vazquez M., Verschoor S., et al. Rad21-cohesin haploinsufficiency impedes DNA repair and enhances gastrointestinal radiosensitivity in mice. PLoS ONE 2010, 5:e12112.
43. Xu H., Tomaszewski J.M., McKay M.J. Can corruption of chromosome cohesion create a conduit to cancer?. Nat. Rev. Cancer 2011, 11:199-210.
44. Xu H., Yan M., Patra J., Natrajan R., Yan Y., Swagemakers S., Tomaszewski J.M., Verschoor S., Millar E.K., van der Spek P., et al. Enhanced RAD21 cohesin expression confers poor prognosis and resistance to chemotherapy in high grade luminal, basal and HER2 breast cancers. Breast Cancer Res. 2011, 13:R9.
45. Yan M., Xu H., Waddell N., Shield-Artin K., Haviv I., McKay M.J., Fox S.B. Enhanced RAD21 cohesin expression confers poor prognosis in BRCA2 and BRCAX, but not BRCA1 familial breast cancers. Breast Cancer Res. 2012, 14:R69. kConFab authors.
46. Zhang J., Neisa R., Mao Y. Oncogenic Adenomatous polyposis coli mutants impair the mitotic checkpoint through direct interaction with Mad2. Mol. Biol. Cell 2009, 20:2381-2388.
47. Zuin J., Dixon J.R., van der Reijden M.I., Ye Z., Kolovos P., Brouwer R.W., van de Corput M.P., van de Werken H.J., Knoch T.A., van IJcken W.F., et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. USA 2014, 111:996-1001.