Deletion of Irf5 protects hematopoietic stem cells from DNA damage-induced apoptosis and suppresses γ-irradiation-induced thymic lymphomagenesis

Oncogene

Volumn 33, Issue 25, 2014, Pages 3288-3297

  Bi, X ^a   Feng, D ^a   Korczeniewska, J ^a   Alper, N ^a   Hu, G ^a   Barnes, B J ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

apoptosis; IRF5; stem cells; thymic lymphoma; irradiation

Indexed keywords

INTERFERON REGULATORY FACTOR 5; PROTEIN P53; PUMA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; GAMMA IRRADIATION; GENE; GENE DELETION; HEMATOPOIETIC STEM CELL; IRF5 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SPLEEN WEIGHT; THYMOCYTE; THYMUS LYMPHOMA; TUMOR SUPPRESSOR GENE; UPREGULATION;

MUS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARCINOGENESIS; DNA DAMAGE; GAMMA RAYS; HEMATOPOIETIC STEM CELLS; INTERFERON REGULATORY FACTORS; LYMPHOMA; MICE; MICE, INBRED C57BL; NEOPLASMS, RADIATION-INDUCED; SEQUENCE DELETION; T-LYMPHOCYTES; THYMOCYTES; THYMUS NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84903307797     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.295     Document Type: Article

References (40)

1. Rossi DJ, Jamieson CH, Weissman IL. Stem cells and the pathways to aging and cancer. Cell 2008; 132: 681-696.
2. Elledge SJ. Cell cycle checkpoints: preventing an identity crisis. Science 1996; 274: 1664-1672.
3. Vousden KH, Lane DP. P53 in health and disease. Nat Rev Mol Cell Biol 2007; 8: 275-283.
4. Erlacher M, Labi V, Manzl C, Bock G, Tzankov A, Hacker G et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J Exp Med 2006; 203: 2939-2951.
5. Michalak EM, Villunger A, Adam JM, Strasser A. In several cell types the tumour suppressor p53 induces apoptosis largely via Puma but Noxa can contribute. Cell Death Differ 2008; 15: 1019-1029.
6. Kemp CJ, Wheldon T, Balmain A. P53-deficient mice are extremely susceptible to radiation-induced tumorigenesis. Nat Genet 1994; 8: 66-69.
7. Kelly PN, White MJ, Goschnick MW, Fairfax KA, Tarlinton DM, Kinkel SA et al. Individual and overlapping roles of BH3-only proteins Bim and Bad in apoptosis of lymphocytes and platelets and in suppression of thymic lymphoma development. Cell Death Differ 2010; 17: 1655-1664.
8. Michalak EM, Vandenberg CJ, Delbridge ARD, Wu L, Scott CL, Adams JM et al. Apoptosis-promoted tumorigenesis: g-irradiation-induced thymic lymphomagenesis requires Puma-driven leukocyte death. Genes Dev 2010; 24: 1608-1613.
9. Labi V, Erlacher M, Krumschnabel G, Manzl C, Tzankov A, Pinon J et al. Apoptosis of leukocytes triggered by acute DNA damage promotes lymphoma formation. Genes Dev 2010; 24: 1602-1607.
10. Mori T, Anazawa Y, Iiizumi M, Fukuda S, Nakamura Y, Arakawa H. Identification of the interferon regulatory factor 5 gene (IRF-5) as a direct target for p53. Oncogene 2002; 21: 2914-2918.
11. Barnes BJ, Kellum MJ, Pinder KE, Frisancho JA, Pitha PM. Interferon regulatory factor 5, a novel mediator of cell cycle arrest and cell death. Cancer Res 2003; 63: 6424-6431.
12. Hu G, Mancl ME, Barnes BJ. Signaling through IFN regulatory factor-5 sensitizes p53-deficient tumors to DNA damage-induced apoptosis and cell death. Cancer Res 2005; 65: 7403-7412.
13. Yanai H, Chen HM, Inuzuka T, Kondo S, Mak TW, Takaoka A et al. Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression. Proc Natl Acad Sci USA 2007; 104: 3402-3407.
14. Stankovic T, Hubank M, Cronin D, Stewart GS, Fletcher D, Bignell CR et al. Microarray analysis reveals that TP53-and ATM-mutant B-CLLs share a defect in activating proapoptotic responses after DNA damage but are distinguished by major differences in activating prosurvival responses. Blood 2004; 103: 291-300.
15. Yang L, Zhao T, Shi X, Nakhaei P, Wang Y, Sun Q et al. Functional analysis of a dominant negative mutation of interferon regulatory factor 5. PLoS One 2009; 4: e5500.
16. Barnes BJ, Moore PA, Pitha PM. Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon alpha genes. J Biol Chem 2001; 276: 23382-23390.
17. Watkins AJ, Hamoudi RA, Zeng N, Yan Q, Huang Y, Liu H et al. An integrated genomic and expression analysis of 7q deletion in splenic marginal zone lymphoma. PLoS One 2012; 7: e44997.
18. Fresquet V, Robles EF, Parker A, Martinez-Useros J, Mena M, Malumbres R et al. High-throughput sequencing analysis of the chromosome 7q32 deletion reveals IRF5 as a potential tumor supressor in splenic marginal-zone lymphoma. Br J Haematol 2012; 158: 712-726.
19. Kaplan HS, Brown MB. A quantitative dose-response study of lymphoid-tumor development in irradiated C57 black mice. J Natl Cancer Inst 1952; 13: 185-208.
20. Kaplan HS. The role of irradiation on experimental leukemogenesis. Natl Cancer Inst Monogr 1964; 14: 207-220.
21. Yang L, Feng D, Bi X, Stone RC, Barnes BJ. Monocytes from Irf5-/-mice have an intrinsic defect in their response to pristane-induced lupus. J Immunol 2012; 189: 3741-3750.
22. Kim HJ, Alonzo ES, Dorothee G, Pollard JW, Snat-Angelo DB. Selective depletion of eosinophils or neutrophils in mice impacts the efficiency of apoptotic cell clearance in the thymus. PLoS One 2010; 5: e11439.
23. Kominami R, Niwa O. Radiation carcinogenesis in mouse thymic lymphomas. Cancer Sci 2006; 97: 575-581.
24. Bi X, Hameed M, Mirani N, Pimenta EM, Anari J, Barnes BJ. Loss of interferon regulatory factor 5 (IRF5) expression in human ductal carcinoma correlates with disease stage and contributes to metastasis. Breast Cancer Res 2011; 13: R111.
25. Xu D, Meyer F, Ehlers E, Balsnitz L, Zhang L. Interferon regulatory factor 4 (IRF-4) targets IRF-5 to regulate Epstein-Barr virus transformation. J Biol Chem 2011; 286: 18261-18267.
26. Hu G, Barnes BJ. IRF-5 is a mediator of the death receptor-induced apoptotic signaling pathway. J Biol Chem 2009; 284: 2767-2777.
27. Botcheva K, McCorkle SR, McCombie WR, Dunn JJ, Anderson CW. Distinct p53 genomic binding patterns in normal and cancer-derived cell lines. Cell Cycle 2011; 10: 4237-4249.
28. Nikulenkov F, Spinnler C, Li H, Tonnelli C, Shi Y, Turunen M et al. Insights into p53 transcriptional function via genome-wide chromatin occupancy and gene expression analysis. Cell Death Differ 2012; 19: 1992-2002.
29. Wu WS, Heinrichs S, Xu D, Garrison SP, Zambetti GP, Adams JM et al. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 2005; 123: 641-653.
30. Yu H, Shen H, Yuan Y, XuFeng R, Hu X, Garrison SP et al. Deletion of Puma protects hematopoietic stem cells and confers long-term survival in response to high-dose g-irradiation. Blood 2010; 115: 3472-3480.
31. Mauch P, Constine L, Greenberger J, Knospe W, Sullivan J, Liesveld JL et al. Hematopoietic stem cell compartment: acute and late effects of radiation therapy and chemotherapy. Int J Radiat Oncol Biol Phys 1995; 31: 1319-1339.
32. Wang Y, Schulte BA, LaRue AC, Ogawa M, Zhou D. Total body irradiation selectively induces murine hematopoietic stem cell senescence. Blood 2006; 107: 358-366.
33. Takaoka A, Yanai H, Kondo S, Duncan G, Negishi H, Mitzutani T et al. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 2005; 434: 243-249.
34. Schoenemeyer A, Barnes BJ, Mancl ME, Latz E, Goutagny N, Pitha PM et al. The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor signaling. J Biol Chem 2005; 280: 17005-17012.
35. Feng D, Sangster-Guity N, Stone R, Korczeniewska J, Mancl ME, Fitzgerald-Bocarsly P et al. Differential requirement of histone acetylase and deacetylase activities for IRF5-mediated proinflammatory cytokine expression. J Immunol 2010; 185: 6003-6012.
36. Feng D, Yang L, Bi X, Stone RC, Patel P, Barnes BJ. Irf5-deficient mice are protected from pristane-induced lupus via increased Th2 cytokines and altered IgG class switching. Europ J Immunol 2012; 42: 1477-1487.
37. Liu C, Gao F, Li B, Mitchel REJ, Liu X, Lin J et al. TLR4 knockout protects mice from radiation-induced thymic lymphoma by downregulation of IL6 and miR-21. Leukemia 2011; 25: 1516-1519.
38. Garrison SP, Jeffers JR, Yang C, Nilsson JA, Hall MA, Rehg JE et al. Selection against PUMA gene expression in Myc-driven B-cell lymphomagenesis. Mol Cell Biol 2008; 28: 5391-5402.
39. Michalak EM, Jansen ES, Happo L, Cragg MS, Tai L, Smyth GK et al. Puma and to a lesser extent Noxa are suppressors of Myc-induced lymphomagenesis. Cell Death Differ 2009; 16: 684-696.
40. Purtha WE, Swiecki M, Colonna M, Diamond MS, Bhattacharya D. Spontaneous mutation of the Dock2 gene in Irf5-/-mice complicates interpretation of type I interferon production and antibody responses. Proc Natl Acad Sci USA 2012; 109: E898-E904.