RNF20 Links Histone H2B Ubiquitylation with Inflammation and Inflammation-Associated Cancer

Cell Reports

Volumn 14, Issue 6, 2016, Pages 1462-1476

  Tarcic, Ohad ^a   Pateras, Ioannis S ^b   Cooks, Tomer ^a   Shema, Efrat ^a   Kanterman, Julia ^c   Ashkenazi, Hadas ^c   Boocholez, Hana ^c   Hubert, Ayala ^d   Rotkopf, Ron ^a   Baniyash, Michal ^c   Pikarsky, Eli ^e,f   Gorgoulis, Vassilis G ^b,g,h   Oren, Moshe ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^e HEBREW UNIVERSITY   (Israel)

^f HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^g BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^h UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; PROTEIN RNF20; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CHROMATIN; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RNF20 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL ACTIVITY; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DISEASE SEVERITY; DNA DAMAGE; DOWN REGULATION; EXON; GENE; GENE TARGETING; HETEROZYGOSITY; HUMAN; HUMAN CELL; IL6 GENE; IL8 GENE; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RNF20 GENE; T LYMPHOCYTE; UBIQUITINATION; ULCERATIVE COLITIS; ANIMAL; BONE MARROW CELL; CHEMISTRY; CHROMATIN; COLON; COLORECTAL NEOPLASMS; COMPLICATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INFLAMMATION; MALE; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CHROMATIN; COLITIS, ULCERATIVE; COLON; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; INFLAMMATION; MALE; MICE; MICE, TRANSGENIC; MYELOID CELLS; NF-KAPPA B; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84958123407     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.020     Document Type: Article

References (64)

1. Becker C., Fantini M.C., Neurath M.F. High resolution colonoscopy in live mice. Nat. Protoc. 2006, 1:2900-2904.
2. Bedi U., Scheel A.H., Hennion M., Begus-Nahrmann Y., Rüschoff J., Johnsen S.A. SUPT6H controls estrogen receptor activity and cellular differentiation by multiple epigenomic mechanisms. Oncogene 2014, 34:465-473.
3. Ben-Neriah Y., Karin M. Inflammation meets cancer, with NF-κB as the matchmaker. Nat. Immunol. 2011, 12:715-723.
4. Brigati C., Noonan D.M., Albini A., Benelli R. Tumors and inflammatory infiltrates: friends or foes?. Clin. Exp. Metastasis 2002, 19:247-258.
5. Buro L.J., Chipumuro E., Henriksen M.A. Menin and RNF20 recruitment is associated with dynamic histone modifications that regulate signal transducer and activator of transcription 1 (STAT1)-activated transcription of the interferon regulatory factor 1 gene (IRF1). Epigenetics Chromatin 2010, 3:16.
6. Campos E.I., Reinberg D. Histones: annotating chromatin. Annu. Rev. Genet. 2009, 43:559-599.
7. Chernikova S.B., Brown J.M. R-loops and genomic instability in Bre1 (RNF20/40)-deficient cells. Cell Cycle 2012, 11:2980-2984.
8. Chernikova S.B., Dorth J.A., Razorenova O.V., Game J.C., Brown J.M. Deficiency in Bre1 impairs homologous recombination repair and cell cycle checkpoint response to radiation damage in mammalian cells. Radiat. Res. 2010, 174:558-565.
9. Chernikova S.B., Razorenova O.V., Higgins J.P., Sishc B.J., Nicolau M., Dorth J.A., Chernikova D.A., Kwok S., Brooks J.D., Bailey S.M., et al. Deficiency in mammalian histone H2B ubiquitin ligase Bre1 (Rnf20/Rnf40) leads to replication stress and chromosomal instability. Cancer Res. 2012, 72:2111-2119.
10. Clapper M.L., Cooper H.S., Chang W.C. Dextran sulfate sodium-induced colitis-associated neoplasia: a promising model for the development of chemopreventive interventions. Acta Pharmacol. Sin. 2007, 28:1450-1459.
11. Cooks T., Pateras I.S., Tarcic O., Solomon H., Schetter A.J., Wilder S., Lozano G., Pikarsky E., Forshew T., Rosenfeld N., et al. Mutant p53 prolongs NF-κB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell 2013, 23:634-646.
12. DiDonato J.A., Mercurio F., Karin M. NF-κB and the link between inflammation and cancer. Immunol. Rev. 2012, 246:379-400.
13. Ea C.K., Hao S., Yeo K.S., Baltimore D. EHMT1 protein binds to nuclear factor-κB p50 and represses gene expression. J. Biol. Chem. 2012, 287:31207-31217.
14. Eaden J.A., Abrams K.R., Mayberry J.F. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001, 48:526-535.
15. Fierz B., Chatterjee C., McGinty R.K., Bar-Dagan M., Raleigh D.P., Muir T.W. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 2011, 7:113-119.
16. Fuchs G., Shema E., Vesterman R., Kotler E., Wolchinsky Z., Wilder S., Golomb L., Pribluda A., Zhang F., Haj-Yahya M., et al. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell 2012, 46:662-673.
17. Fuchs G., Hollander D., Voichek Y., Ast G., Oren M. Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate. Genome Res. 2014, 24:1572-1583.
18. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
19. Hahn M.A., Dickson K.A., Jackson S., Clarkson A., Gill A.J., Marsh D.J. The tumor suppressor CDC73 interacts with the ring finger proteins RNF20 and RNF40 and is required for the maintenance of histone 2B monoubiquitination. Hum. Mol. Genet. 2012, 21:559-568.
20. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
21. Hayden M.S., Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008, 132:344-362.
22. Hayden M.S., Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012, 26:203-234.
23. Heinz S., Romanoski C.E., Benner C., Allison K.A., Kaikkonen M.U., Orozco L.D., Glass C.K. Effect of natural genetic variation on enhancer selection and function. Nature 2013, 503:487-492.
24. Hwang W.W., Venkatasubrahmanyam S., Ianculescu A.G., Tong A., Boone C., Madhani H.D. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell 2003, 11:261-266.
25. Jääskeläinen T., Makkonen H., Visakorpi T., Kim J., Roeder R.G., Palvimo J.J. Histone H2B ubiquitin ligases RNF20 and RNF40 in androgen signaling and prostate cancer cell growth. Mol. Cell. Endocrinol. 2012, 350:87-98.
26. Kari V., Shchebet A., Neumann H., Johnsen S.A. The H2B ubiquitin ligase RNF40 cooperates with SUPT16H to induce dynamic changes in chromatin structure during DNA double-strand break repair. Cell Cycle 2011, 10:3495-3504.
27. Karpiuk O., Najafova Z., Kramer F., Hennion M., Galonska C., König A., Snaidero N., Vogel T., Shchebet A., Begus-Nahrmann Y., et al. The histone H2B monoubiquitination regulatory pathway is required for differentiation of multipotent stem cells. Mol. Cell 2012, 46:705-713.
28. Katoh H., Wang D., Daikoku T., Sun H., Dey S.K., Dubois R.N. CXCR2-expressing myeloid-derived suppressor cells are essential to promote colitis-associated tumorigenesis. Cancer Cell 2013, 24:631-644.
29. Kogure M., Takawa M., Saloura V., Sone K., Piao L., Ueda K., Ibrahim R., Tsunoda T., Sugiyama M., Atomi Y., et al. The oncogenic polycomb histone methyltransferase EZH2 methylates lysine 120 on histone H2B and competes ubiquitination. Neoplasia 2013, 15:1251-1261.
30. Koo B.K., Stange D.E., Sato T., Karthaus W., Farin H.F., Huch M., van Es J.H., Clevers H. Controlled gene expression in primary Lgr5 organoid cultures. Nat. Methods 2012, 9:81-83.
31. Kravtsova-Ivantsiv Y., Shomer I., Cohen-Kaplan V., Snijder B., Superti-Furga G., Gonen H., Sommer T., Ziv T., Admon A., Naroditsky I., et al. KPC1-mediated ubiquitination and proteasomal processing of NF-κB1 p105 to p50 restricts tumor growth. Cell 2015, 161:333-347.
32. Kumar V., Robbins S.L. Robbins Basic Pathology 2007, Saunders/Elsevier.
33. Lawrence T., Gilroy D.W., Colville-Nash P.R., Willoughby D.A. Possible new role for NF-kappaB in the resolution of inflammation. Nat. Med. 2001, 7:1291-1297.
34. Majno G., Joris I. Cells, Tissues, and Disease: Principles of General Pathology 2004, Oxford University Press.
35. Mantovani A., Romero P., Palucka A.K., Marincola F.M. Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 2008, 371:771-783.
36. Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell 2010, 140:771-776.
37. Minsky N., Shema E., Field Y., Schuster M., Segal E., Oren M. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 2008, 10:483-488.
38. Moyal L., Lerenthal Y., Gana-Weisz M., Mass G., So S., Wang S.Y., Eppink B., Chung Y.M., Shalev G., Shema E., et al. Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol. Cell 2011, 41:529-542.
39. Myant K.B., Cammareri P., McGhee E.J., Ridgway R.A., Huels D.J., Cordero J.B., Schwitalla S., Kalna G., Ogg E.L., Athineos D., et al. ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 2013, 12:761-773.
40. Nakachi I., Rice J.L., Coldren C.D., Edwards M.G., Stearman R.S., Glidewell S.C., Varella-Garcia M., Franklin W.A., Keith R.L., Lewis M.T., et al. Application of SNP microarrays to the genome-wide analysis of chromosomal instability in premalignant airway lesions. Cancer Prev. Res. (Phila) 2013, 7:255-265.
41. Nakamura K., Kato A., Kobayashi J., Yanagihara H., Sakamoto S., Oliveira D.V., Shimada M., Tauchi H., Suzuki H., Tashiro S., et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell 2011, 41:515-528.
42. O'Dea E., Hoffmann A. The regulatory logic of the NF-kappaB signaling system. Cold Spring Harb. Perspect. Biol. 2010, 2:a000216.
43. Pavri R., Zhu B., Li G., Trojer P., Mandal S., Shilatifard A., Reinberg D. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 2006, 125:703-717.
44. Perkins N.D. The diverse and complex roles of NF-κB subunits in cancer. Nat. Rev. Cancer 2012, 12:121-132.
45. Pikarsky E., Porat R.M., Stein I., Abramovitch R., Amit S., Kasem S., Gutkovich-Pyest E., Urieli-Shoval S., Galun E., Ben-Neriah Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431:461-466.
46. Prenzel T., Begus-Nahrmann Y., Kramer F., Hennion M., Hsu C., Gorsler T., Hintermair C., Eick D., Kremmer E., Simons M., et al. Estrogen-dependent gene transcription in human breast cancer cells relies upon proteasome-dependent monoubiquitination of histone H2B. Cancer Res. 2011, 71:5739-5753.
47. Sato T., Stange D.E., Ferrante M., Vries R.G., Van Es J.H., Van den Brink S., Van Houdt W.J., Pronk A., Van Gorp J., Siersema P.D., Clevers H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 2011, 141:1762-1772.
48. Schetter A.J., Heegaard N.H., Harris C.C. Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 2010, 31:37-49.
49. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., Canli O., Heijmans J., Huels D.J., Moreaux G., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152:25-38.
50. Sen R., Bhaumik S.R. Transcriptional stimulatory and repressive functions of histone H2B ubiquitin ligase. Transcription 2013, 4:221-226.
51. Shema E., Tirosh I., Aylon Y., Huang J., Ye C., Moskovits N., Raver-Shapira N., Minsky N., Pirngruber J., Tarcic G., et al. The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev. 2008, 22:2664-2676.
52. Shema E., Kim J., Roeder R.G., Oren M. RNF20 inhibits TFIIS-facilitated transcriptional elongation to suppress pro-oncogenic gene expression. Mol. Cell 2011, 42:477-488.
53. Shema-Yaacoby E., Nikolov M., Haj-Yahya M., Siman P., Allemand E., Yamaguchi Y., Muchardt C., Urlaub H., Brik A., Oren M., Fischle W. Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription. Cell Rep. 2013, 4:601-608.
54. Shiloh Y., Shema E., Moyal L., Oren M. RNF20-RNF40: A ubiquitin-driven link between gene expression and the DNA damage response. FEBS Lett. 2011, 585:2795-2802.
55. Tanaka T., Kohno H., Suzuki R., Yamada Y., Sugie S., Mori H. A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci. 2003, 94:965-973.
56. Terzić J., Grivennikov S., Karin E., Karin M. Inflammation and colon cancer. Gastroenterology 2010, 138:2101-2114.e5.
57. Thompson L.L., Guppy B.J., Sawchuk L., Davie J.R., McManus K.J. Regulation of chromatin structure via histone post-translational modification and the link to carcinogenesis. Cancer Metastasis Rev. 2013, 32:363-376.
58. Ullman T.A., Itzkowitz S.H. Intestinal inflammation and cancer. Gastroenterology 2011, 140:1807-1816.
59. Urasaki Y., Heath L., Xu C.W. Coupling of glucose deprivation with impaired histone H2B monoubiquitination in tumors. PLoS ONE 2012, 7:e36775.
60. Wang Z.J., Yang J.L., Wang Y.P., Lou J.Y., Chen J., Liu C., Guo L.D. Decreased histone H2B monoubiquitination in malignant gastric carcinoma. World J. Gastroenterol. 2013, 19:8099-8107.
61. Ward J.M., Yamamoto R.S., Brown C.A. Pathology of intestinal neoplasms and other lesions in rats exposed to azoxymethane. J. Natl. Cancer Inst. 1973, 51:1029-1039.
62. Whitehead R.H., VanEeden P.E., Noble M.D., Ataliotis P., Jat P.S. Establishment of conditionally immortalized epithelial cell lines from both colon and small intestine of adult H-2Kb-tsA58 transgenic mice. Proc. Natl. Acad. Sci. USA 1993, 90:587-591.
63. Zhang X.Y., Pfeiffer H.K., Thorne A.W., McMahon S.B. USP22, an hSAGA subunit and potential cancer stem cell marker, reverses the polycomb-catalyzed ubiquitylation of histone H2A. Cell Cycle 2008, 7:1522-1524.
64. Zhu B., Zheng Y., Pham A.D., Mandal S.S., Erdjument-Bromage H., Tempst P., Reinberg D. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol. Cell 2005, 20:601-611.