Apurinic/apyrimidinic endonuclease 2 is necessary for normal B cell development and recovery of lymphoid progenitors after chemotherapeutic challenge

Journal of Immunology

Volumn 186, Issue 4, 2011, Pages 1943-1950

  Guikema, Jeroen E J ^a   Gerstein, Rachel M ^a   Linehan, Erin K ^a   Cloherty, Erin K ^a   Evan Browning, Eric ^a   Tsuchimoto, Daisuke ^b   Nakabeppu, Yusaku ^b   Schrader, Carol E ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APURINIC APYRIMIDINIC ENDONUCLEASE 2; DNA; ENDONUCLEASE; FLUOROURACIL; INTERLEUKIN 7; PROTEIN P53; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL EXPANSION; COCULTURE; CONTROLLED STUDY; DNA DAMAGE; EXCISION REPAIR; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC RECOMBINATION; HEMATOPOIESIS; IN VITRO STUDY; LYMPHOID PROGENITOR CELL; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PRO B LYMPHOCYTE; STROMA CELL; TURNOVER TIME; V(D)J RECOMBINATION;

ANIMALS; B-LYMPHOCYTE SUBSETS; CELLS, CULTURED; COCULTURE TECHNIQUES; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; ENDONUCLEASES; FLUOROURACIL; HEMATOPOIETIC STEM CELLS; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBSETS; LYMPHOPOIESIS; MICE; MICE, KNOCKOUT; MYELOPOIESIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79951837402     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002422     Document Type: Article

References (52)

1. Barnes, D. E., and T. Lindahl. 2004. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38: 445-476.
2. David, S. S., V. L. O'Shea, and S. Kundu. 2007. Base-excision repair of oxidative DNA damage. Nature 447: 941-950.
3. Jung, D., C. Giallourakis, R. Mostoslavsky, and F. W. Alt. 2006. Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu. Rev. Immunol. 24: 541-570.
4. Mills, K. D., D. O. Ferguson, and F. W. Alt. 2003. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 194: 77-95.
5. Jolly, C. J., A. J. Cook, and J. P. Manis. 2008. Fixing DNA breaks during class switch recombination. J. Exp. Med. 205: 509-513.
6. de Villartay, J. P. 2009. V(D)J recombination deficiencies. Adv. Exp. Med. Biol. 650: 46-58.
7. Xanthoudakis, S., R. J. Smeyne, J. D. Wallace, and T. Curran. 1996. The redox/ DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl. Acad. Sci. USA 93: 8919-8923.
8. Bentley, D., J. Selfridge, J. K. Millar, K. Samuel, N. Hole, J. D. Ansell, and D. W. Melton. 1996. DNA ligase I is required for fetal liver erythropoiesis but is not essential for mammalian cell viability. Nat. Genet. 13: 489-491.
9. Sugo, N., Y. Aratani, Y. Nagashima, Y. Kubota, and H. Koyama. 2000. Neonatal lethality with abnormal neurogenesis in mice deficient in DNA polymerase beta. EMBO J. 19: 1397-1404. (Pubitemid 30151035)
10. Hadi, M. Z., K. Ginalski, L. H. Nguyen, and D. M. Wilson, III. 2002. Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III. J. Mol. Biol. 316: 853-866.
11. Hadi, M. Z., and D. M. Wilson, III. 2000. Second human protein with homology to the Escherichia coli abasic endonuclease exonuclease III. Environ. Mol. Mutagen. 36: 312-324.
12. Burkovics, P., V. Szukacsov, I. Unk, and L. Haracska. 2006. Human Ape2 protein has a 3′-5′ exonuclease activity that acts preferentially on mismatched base pairs. Nucleic Acids Res. 34: 2508-2515. (Pubitemid 43985615)
13. Burkovics, P., I. Hajdú, V. Szukacsov, I. Unk, and L. Haracska. 2009. Role of PCNA-dependent stimulation of 39-phosphodiesterase and 39-59 exonuclease activities of human Ape2 in repair of oxidative DNA damage. Nucleic Acids Res. 37: 4247-4255.
14. Bertoncini, C. R., and R. Meneghini. 1995. DNA strand breaks produced by oxidative stress in mammalian cells exhibit 3́-phosphoglycolate termini. Nucleic Acids Res. 23: 2995-3002.
15. Castillo-Acosta, V. M., L. M. Ruiz-Pérez, W. Yang, D. González-Pacanowska, and A. E. Vidal. 2009. Identification of a residue critical for the excision of 3′-blocking ends in apurinic/apyrimidinic endonucleases of the Xth family. Nucleic Acids Res. 37: 1829-1842
16. 2/M arrest in APEX2-null mice. Blood 104: 4097-4103.
17. Kujoth, G. C., A. Hiona, T. D. Pugh, S. Someya, K. Panzer, S. E. Wohlgemuth, T. Hofer, A. Y. Seo, R. Sullivan, W. A. Jobling, et al. 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-484. (Pubitemid 40994689)
18. Balaban, R. S., S. Nemoto, and T. Finkel. 2005. Mitochondria, oxidants, and aging. Cell 120: 483-495. (Pubitemid 40269763)
19. Meira, L. B., S. Devaraj, G. E. Kisby, D. K. Burns, R. L. Daniel, R. E. Hammer, S. Grundy, I. Jialal, and E. C. Friedberg. 2001. Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress. Cancer Res. 61: 5552-5557.
20. Ide, Y., D. Tsuchimoto, Y. Tominaga, Y. Iwamoto, and Y. Nakabeppu. 2003. Characterization of the genomic structure and expression of the mouse Apex2 gene. Genomics 81: 47-57. (Pubitemid 36263358)
21. Borghesi, L., and R. M. Gerstein. 2004. Developmental separation of V(D)J recombinase expression and initiation of IgH recombination in B lineage progenitors in vivo. J. Exp. Med. 199: 483-489.
22. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
23. Cancro, M. P., A. P. Sah, S. L. Levy, D. M. Allman, M. R. Schmidt, and R. T. Woodland. 2001. xid mice reveal the interplay of homeostasis and Bruton's tyrosine kinase-mediated selection at multiple stages of B cell development. Int. Immunol. 13: 1501-1514.
24. Borghesi, L., L. Y. Hsu, J. P. Miller, M. Anderson, L. Herzenberg, L. Herzenberg, M. S. Schlissel, D. Allman, and R. M. Gerstein. 2004. B lineage-specific regulation of V(D)J recombinase activity is established in common lymphoid progenitors. J. Exp. Med. 199: 491-502.
25. Dan, Y., Y. Ohta, D. Tsuchimoto, M. Ohno, Y. Ide, M. Sami, T. Kanda, K. Sakumi, and Y. Nakabeppu. 2008. Altered gene expression profiles and higher frequency of spontaneous DNA strand breaks in APEX2-null thymus. DNA Repair (Amst.) 7: 1437-1454.
26. Johnson, K., T. Hashimshony, C. M. Sawai, J. M. Pongubala, J. A. Skok, I. Aifantis, and H. Singh. 2008. Regulation of immunoglobulin light-chain recombination by the transcription factor IRF-4 and the attenuation of interleukin-7 signaling. Immunity 28: 335-345.
27. Núñez, G., R. Merino, D. Grillot, and M. González-García. 1994. Bcl-2 and Bclx: regulatory switches for lymphoid death and survival. Immunol. Today 15: 582-588. (Pubitemid 24353910)
28. Lu, L., and D. G. Osmond. 2000. Apoptosis and its modulation during B lymphopoiesis in mouse bone marrow. Immunol. Rev. 175: 158-174.
29. Merino, R., L. Ding, D. J. Veis, S. J. Korsmeyer, and G. Nuñez. 1994. Developmental regulation of the Bcl-2 protein and susceptibility to cell death in B lymphocytes. EMBO J. 13: 683-691. (Pubitemid 24050683)
30. Li, Y. S., K. Hayakawa, and R. R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178: 951-960.
31. Cancro, M. P., and S. H. Smith. 2003. Peripheral B cell selection and homeostasis. Immunol. Res. 27: 141-148.
32. Tsuboi, I., Y. Hirabayashi, T. Harada, M. Koshinaga, T. Kawamata, J. Kanno, T. Inoue, and S. Aizawa. 2008. Role of hematopoietic microenvironment in prolonged impairment of B cell regeneration in age-related stromal-cellimpaired SAMP1 mouse: effects of a single dose of 5-fluorouracil. J. Appl. Toxicol. 28: 797-805.
33. Guikema, J. E., E. K. Linehan, D. Tsuchimoto, Y. Nakabeppu, P. R. Strauss, J. Stavnezer, and C. E. Schrader. 2007. APE1- and APE2-dependent DNA breaks in immunoglobulin class switch recombination. J. Exp. Med. 204: 3017-3026.
34. Rossi, D. J., D. Bryder, J. Seita, A. Nussenzweig, J. Hoeijmakers, and I. L. Weissman. 2007. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447: 725-729.
35. Navarro, S., N. W. Meza, O. Quintana-Bustamante, J. A. Casado, A. Jacome, K. McAllister, S. Puerto, J. Surrallés, J. C. Segovia, and J. A. Bueren. 2006. Hematopoietic dysfunction in a mouse model for Fanconi anemia group D1. Mol. Ther. 14: 525-535.
36. Reese, J. S., L. Liu, and S. L. Gerson. 2003. Repopulating defect of mismatch repair-deficient hematopoietic stem cells. Blood 102: 1626-1633.
37. Domen, J., S. H. Cheshier, and I. L.Weissman. 2000. The role of apoptosis in the regulation of hematopoietic stem cells: overexpression of Bcl-2 increases both their number and repopulation potential. J. Exp. Med. 191: 253-264.
38. Milyavsky, M., O. I. Gan, M. Trottier, M. Komosa, O. Tabach, F. Notta, E. Lechman, K. G. Hermans, K. Eppert, Z. Konovalova, et al. 2010. A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosisin-dependent role for p53 in self-renewal. Cell Stem Cell 7: 186-197.
39. Bondar, T., and R. Medzhitov. 2010. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6: 309-322.
40. Mohrin, M., E. Bourke, D. Alexander, M. R. Warr, K. Barry-Holson, M. M. Le Beau, C. G. Morrison, and E. Passegué. 2010. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell 7: 174-185.
41. McNeill, D. R., and D. M. Wilson, III. 2007. A dominant-negative form of the major human abasic endonuclease enhances cellular sensitivity to laboratory and clinical DNA-damaging agents. Mol. Cancer Res. 5: 61-70.
42. Matuo, R., F. G. Sousa, A. E. Escargueil, D. G. Soares, I. Grivicich, J. Saffi, A. K. Larsen, and J. A. Henriques. 2010. DNA repair pathways involved in repair of lesions induced by 5-fluorouracil and its active metabolite FdUMP. Biochem. Pharmacol. 79: 147-153.
43. Li, L. S., J. C. Morales, M. Veigl, D. Sedwick, S. Greer, M. Meyers, M. Wagner, R. Fishel, and D. A. Boothman. 2009. DNA mismatch repair (MMR)-dependent 5-fluorouracil cytotoxicity and the potential for new therapeutic targets. Br. J. Pharmacol. 158: 679-692.
44. Grunda, J. M., J. Fiveash, C. A. Palmer, A. Cantor, H. M. Fathallah-Shaykh, L. B. Nabors, and M. R. Johnson. 2010. Rationally designed pharmacogenomic treatment using concurrent capecitabine and radiotherapy for glioblastoma; gene expression profiles associated with outcome. Clin. Cancer Res. 16: 2890-2898.
45. Berardi, A. C., A. Wang, J. D. Levine, P. Lopez, and D. T. Scadden. 1995. Functional isolation and characterization of human hematopoietic stem cells. Science 267: 104-108.
46. Bocci, G., R. Danesi, A. D. Di Paolo, F. Innocenti, G. Allegrini, A. Falcone, A. Melosi, M. Battistoni, G. Barsanti, P. F. Conte, and M. Del Tacca. 2000. Comparative pharmacokinetic analysis of 5-fluorouracil and its major metabolite 5-fluoro-5,6-dihydrouracil after conventional and reduced test dose in cancer patients. Clin. Cancer Res. 6: 3032-3037.
47. Dykstra, B., and G. de Haan. 2008. Hematopoietic stem cell aging and self-renewal. Cell Tissue Res. 331: 91-101. (Pubitemid 50003499)
48. Rossi, D. J., D. Bryder, J. M. Zahn, H. Ahlenius, R. Sonu, A. J. Wagers, and I. L. Weissman. 2005. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc. Natl. Acad. Sci. USA 102: 9194-9199.
49. Stephan, R. P., C. R. Reilly, and P. L. Witte. 1998. Impaired ability of bone marrow stromal cells to support B-lymphopoiesis with age. Blood 91: 75-88.
50. Lamberts, S. W., A. W. van den Beld, and A. J. van der Lely. 1997. The endocrinology of aging. Science 278: 419-424. (Pubitemid 27454418)
51. Labrie, J. E., III, A. P. Sah, D. M. Allman, M. P. Cancro, and R. M. Gerstein. 2004. Bone marrow microenvironmental changes underlie reduced RAG-mediated recombination and B cell generation in aged mice. J. Exp. Med. 200: 411-423.
52. Mayack, S. R., J. L. Shadrach, F. S. Kim, and A. J. Wagers. 2010. Systemic signals regulate ageing and rejuvenation of blood stem cell niches. Nature 463: 495-500.