Msh2-dependent DNA repair mitigates a unique susceptibility of B cell progenitors to c-Myc-induced lymphomas

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 44, 2009, Pages 18698-18703

  Nepal, Rajeev M ^a   Tong, Li ^a   Kolaj, Blerta ^a   Edelmann, Winfried ^b   Martin, Alberto ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Mismatch repair; Oncogenesis; p53

Indexed keywords

MYC PROTEIN; PROTEIN MSH2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CARCINOGENESIS; CELL MATURATION; CONTROLLED STUDY; DNA REPAIR; MISSENSE MUTATION; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; DISEASE SUSCEPTIBILITY; DNA REPAIR; LYMPHOMA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTS HOMOLOG 2 PROTEIN; PRECURSOR CELLS, B-LYMPHOID; PROTO-ONCOGENE PROTEINS C-MYC; TUMOR SUPPRESSOR PROTEIN P53;

MUS; MUS MUSCULUS;

EID: 73249119147     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905965106     Document Type: Article

References (46)

1. Harris NL, et al. (2001) New approaches to lymphoma diagnosis. Hematol Am Soc Hematol Educ Program 1:194-220.
2. Facchini LM, Penn LZ (1998) The molecular role of Myc in growth and transformation: Recent discoveries lead to new insights. FASEB J 12:633-651.
3. Amati B, et al. (1992) Transcriptional activation by the human c-Myc oncoprotein in yeast requires interaction with Max. Nature 359:423-426.
4. Amati B, Littlewood TD, Evan GI, Land H (1993) The c-Myc protein induces cell cycle progression and apoptosis through dimerization with Max. EMBO J 12:5083-5087.
5. Adams JM, et al. (1985) The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318:533-538.
6. Harris AW, et al. (1988) The E mu-myc transgenic mouse. A model for high-incidence spontaneous lymphoma and leukemia of early B cells. J Exp Med 167:353-371.
7. van Lohuizen M, et al. (1991) Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65:737-752.
8. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL (1999) Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13:2658-2669.
9. Kotani A, et al. (2007) Activation-induced cytidine deaminase (AID) promotes B cell lymphomagenesis in Emu-cmyc transgenic mice. Proc Natl Acad Sci USA 104:1616-1620.
10. Kunkel TA, Erie DA (2005) DNA mismatch repair. Annu Rev Biochem 74:681-710.
11. Wei K, Kucherlapati R, Edelmann W (2002) Mouse models for human DNA mismatchrepair gene defects. Trends Mol Med 8:346-353.
12. Reitmair AH, et al. (1995) MSH2-deficient mice are viable and susceptible to lymphoid tumors. Nat Genet 11:64-70.
13. Fishel R, et al. (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75:1027-1038.
14. Nepal RM, et al. (2008) AID and RAG1 do not contribute to lymphomagenesis in Emu c-myc transgenic mice. Oncogene 27:4752-4756.
15. Liu Z, et al. (2008) Protective immunosurveillance and therapeutic antitumor activity of gammadelta T cells demonstrated in a mouse model of prostate cancer. J Immunol 180:6044-6053.
16. Mombaerts P, et al. (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869-877.
17. Kitamura D, Roes J, Kuhn R, Rajewsky K (1991) A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423-426.
18. Lu L, Lejtenyi D, Osmond DG (1999) Regulation of cell survival during B lymphopoiesis: Suppressed apoptosis of pro-B cells in P53-deficient mouse bone marrow. Eur J Immunol 29:2484-2490.
19. Schmidt NW,Mayo LD, Donner DB, Kaplan MH (2006) p53 regulates Btk-dependent B cell proliferation but not differentiation. J Leukocyte Biol 79:852-859.
20. Young LC, Hays JB, Tron VA, Andrew SE (2003)DNAmismatch repair proteins: Potential guardians against genomic instability and tumorigenesis induced by ultraviolet photoproducts. J Invest Dermatol 121:435-440.
21. Lin DP, et al. (2004) An Msh2 point mutation uncouples DNA mismatch repair and apoptosis. Cancer Res 64:517-522.
22. Campbell MR,Wang Y, Andrew SE, Liu Y (2006) Msh2 deficiency leads to chromosomal abnormalities, centrosome amplification, and telomere capping defect. Oncogene 25:2531-2536.
23. Prasad VS, Temple MJ, Davisson MT, Akeson EC, Sidman CL (1996) Heterogeneity of B-lymphoid tumors in E mu-myc transgenic mice. Cytometry 23:131-139.
24. Larijani M, et al. (2005) Lack of MSH2 involvement differentiates V(D)J recombination from other nonhomologous end joining events. Nucleic Acids Res 33:6733-6742.
25. Gay D, Saunders T, Camper S, Weigert M (1993) Receptor editing: An approach by autoreactive B cells to escape tolerance. J Exp Med 177:999-1008.
26. Dalla-Favera R, et al. (1982) Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci USA 79:7824-7827.
27. Fagarasan S, et al. (2002) Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 298:1424-1427.
28. Wen R, et al. (2006) Essential role of phospholipase C gamma 2 in early B-cell development and Myc-mediated lymphomagenesis. Mol Cell Biol 26:9364-9376.
29. Wang D, et al. (2000) Phospholipase C gamma2 is essential in the functions of B cell and several Fc receptors. Immunity 13:25-35.
30. Ball JK, Sinclair NR, McCarter JA (1966) Prolonged immunosuppression and tumor induction by a chemical carcinogen injected at birth. Science 152:650-651.
31. Harfe BD, Jinks-Robertson S (2000) DNA mismatch repair and genetic instability. Annu Rev Genet 34:359-399.
32. Kolodner R (1996) Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev 10:1433-1442.
33. Fishel R (2001) The selection for mismatch repair defects in hereditary nonpolyposis colorectal cancer: Revising the mutator hypothesis. Cancer Res 61:7369-7374. 34. Iyer RR, Pluciennik A, Burdett V, Modrich PL (2006)DNAmismatch repair: Functions and mechanisms. Chem Rev 106:302-323.
34. Duckett DR, Bronstein SM, Taya Y, Modrich P (1999) hMutSα- and hMutLα-dependent phosphorylation of p53 in response to DNA methylator damage. Proc Natl Acad Sci USA 96:12384-12388.
35. Flores ER, et al. (2002) p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416:560-564.
36. Jost CA, Marin MC, Kaelin WG, Jr (1997) p73 is a simian [correction of human] p53-related protein that can induce apoptosis. Nature 389:191-194.
37. Pusapati RV, et al. (2006) ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc Natl Acad Sci USA 103:1446-1451.
38. Andrew SE, et al. (1997) Base transitions dominate the mutational spectrum of a transgenic reporter gene in MSH2-deficient mice. Oncogene 15:123-129.
39. Gladdy RA, et al. (2003) The RAG-1/2 endonuclease causes genomic instability and controls CNS complications of lymphoblastic leukemia in p53/Prkdc-deficient mice. Cancer Cell 3:37-50.
40. Drynan LF, Hamilton TL, Rabbitts TH (2001) T cell tumorigenesis in Lmo2 transgenic mice is independent of V-D-J recombinase activity. Oncogene 20:4412-4415.
41. Vafa O, et al. (2002) c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: A mechanism for oncogene-induced genetic instability. Mol Cell 9:1031-1044.
42. Russo MT, De Luca G, Degan P, Bignami M (2007) Different DNA repair strategies to combat the threat from 8-oxoguanine. Mutat Res 614:69-76.
43. Colussi C, et al. (2002) The mammalian mismatch repair pathway removes DNA 8-oxodGMP incorporated from the oxidized dNTP pool. Curr Biol 12:912-918.
44. Klein U, Dalla-Favera R (2008) Germinal centers: Role in B-cell physiology and malignancy. Nat Rev Immunol 8:22-33.
45. Mombaerts P, et al. (1992) Mutations in T cell antigen receptor genes α and β block thymocyte development at different stages. Nature 360:225-231.
46. Itohara S, et al. (1993) T cell receptor delta gene mutant mice: Independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell 72:337-348.