Circulating human B lymphocytes are deficient in nucleotide excision repair and accumulate mutations upon proliferation

Blood

Volumn 117, Issue 23, 2011, Pages 6277-6286

  Hyka Nouspikel, Nevila ^a   Lemonidis, Kimon ^a   Lu, Wei Ting ^a   Nouspikel, Thierry ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D2; PROTEIN BCL 6; UBIQUITIN ACTIVATING ENZYME UBE1; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EXCISION REPAIR; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 79959450884     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-12-326637     Document Type: Article

References (50)

1. Burger JA, Ghia P, Rosenwald A, Caligaris-Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood. 2009;114(16):3367-3375.
2. Küppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer. 2005;5(4):251-262. (Pubitemid 40488631)
3. Phan RT, Dalla-Favera R. The BCL6 protooncogene suppresses p53 expression in germinalcentre B cells. Nature. 2004;432(7017):635-639. (Pubitemid 39626271)
4. Maul RW, Gearhart PJ. AID and somatic hypermutation. Adv Immunol. 2010;105:159-191.
5. Pasqualucci L, Bhagat G, Jankovic M, et al. AID is required for germinal center-derived lymphomagenesis. Nat Genet. 2008;40(1):108-112.
6. Hanawalt PC. Subpathways of nucleotide excision repair and their regulation. Oncogene. 2002; 21(58):8949-8956. (Pubitemid 36110824)
7. Kraemer KH, Lee MM, Scotto J. Xeroderma pigmentosum. Cutaneous, ocular, and neurological abnormalities in 830 published cases. Arch Dermatol. 1987;123:241-250. (Pubitemid 17002499)
8. Nouspikel T, Hanawalt PC. DNA repair in terminally differentiated cells. DNA Repair. 2002;1:59-75. (Pubitemid 34475693)
9. Nouspikel T, Hanawalt PC. Impaired nucleotide excision repair upon macrophage differentiation is corrected by E1 ubiquitin-activating enzyme. Proc Natl Acad Sci U S A. 2006;103(44):16188-16193. (Pubitemid 44715172)
10. Nouspikel T, Hanawalt PC. Terminally differentiated human neurons repair transcribed genes but display attenuated global DNA repair and modulation of repair gene expression. Mol Cell Biol. 2000;20:1562-1570. (Pubitemid 30100176)
11. Nouspikel TP, Hyka-Nouspikel N, Hanawalt PC. Transcription domain-associated repair in human cells. Mol Cell Biol. 2006;26(23):8722-8730. (Pubitemid 44851933)
12. Pleasance ED, Cheetham RK, Stephens PJ, et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature. 2010; 463(7278):191-196.
13. Spivak G, Hanawalt P. Determination of damage and repair in specific DNA sequences. Methods: Companion Methods Enzymol. 1995;7:147-161.
14. Kaur M, Zhang Y, Liu WH, Tetradis S, Price BD, Makrigiorgos GM. Ligation of a primer at a mutation: a method to detect low level mutations in DNA. Mutagenesis. 2002;17(5):365-374.
15. Bekeredjian-Ding I, Inamura S, Giese T, et al. Staphylococcus aureus protein A triggers T cellindependent B cell proliferation by sensitizing B cells for TLR2 ligands. J Immunol. 2007;178(5): 2803-2812. (Pubitemid 46333158)
16. Hwang BJ, Ford JM, Hanawalt PC, Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc Natl Acad Sci U S A. 1999; 96(2):424-428. (Pubitemid 29061224)
17. Tornaletti S. Transcription arrest at DNA damage sites. Mutat Res. 2005;577(1-2):131-145. (Pubitemid 41225493)
18. Yang Y, Kitagaki J, Dai RM, et al. Inhibitors of ubiquitin-activating enzyme (E1), a new class of potential cancer therapeutics. Cancer Res. 2007; 67(19):9472-9481. (Pubitemid 47535937)
19. Gocke E, Eckhardt K, King MT, Wild D. Autoradiographic detection of 6-thioguanine-resistant lymphocytes of mice. A novel system in somatic mutagenesis testing. Mutat Res. 1983;113(5):455-465. (Pubitemid 13033206)
20. Parry JM, Shamsher M, Skibinski DO. Restriction site mutation analysis, a proposed methodology for the detection and study of DNA base changes following mutagen exposure. Mutagenesis. 1990; 5(3):209-212. (Pubitemid 20329936)
21. Solvason N, Wu WW, Kabra N, Wu X, Lees E, Howard MC. Induction of cell cycle regulatory proteins in anti-immunoglobulin-stimulated mature B lymphocytes. J Exp Med. 1996;184(2):407-417. (Pubitemid 26324094)
22. Capello D, Vitolo U, Pasqualucci L, et al. Distribution and pattern of BCL6 mutations throughout the spectrum of B-cell neoplasia. Blood. 2000; 95(2):651-659. (Pubitemid 30041683)
23. Adami J, Gridley G, Nyren O, et al. Sunlight and non-Hodgkin's lymphoma: a population-based cohort study in Sweden. Int J Cancer. 1999;80(5): 641-645. (Pubitemid 29066270)
24. Bentham G. Association between incidence of non-Hodgkin's lymphoma and solar ultraviolet radiation in England and Wales. Br Med J. 1996; 312(7039):1128-1131. (Pubitemid 26131291)
25. Kripke ML. Ultraviolet radiation and immunology: something new under the sun-presidential address. Cancer Res. 1994;54(23):6102-6105.
26. Clydesdale GJ, Dandie GW, Muller HK. Ultraviolet light induced injury: immunological and inflammatory effects. Immunol Cell Biol. 2001;79(6): 547-568. (Pubitemid 33070443)
27. Kripke ML, Cox PA, Alas LG, Yarosh DB. Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc Natl Acad Sci U S A. 1992;89(16):7516-7520.
28. Brown EL, Rivas JM, Ullrich SE, Young CR, Norris SJ, Kripke ML. Modulation of immunity to Borrelia burgdorferi by ultraviolet irradiation: differential effect on Th1 and Th2 immune responses. Eur J Immunol. 1995;25(11):3017-3022.
29. Scudiero D, Norin A, Karran P, Strauss B. DNA excision-repair deficiency of human peripheral blood lymphocytes treated with chemical carcinogens. Cancer Res. 1976;36(4):1397-1403.
30. Freeman SE, Ryan SL. Excision repair of pyrimidine dimers in human peripheral blood lymphocytes: comparison between mitogen stimulated and unstimulated cells. Mutat Res. 1988;194(2): 143-150.
31. Barret JM, Calsou P, Laurent G, Salles B. DNA repair activity in protein extracts of fresh human malignant lymphoid cells. Mol Pharmacol. 1996; 49(5):766-771. (Pubitemid 26146137)
32. Stary A, Kannouche P, Lehmann AR, Sarasin A. Role of DNA polymerase eta in the UV mutation spectrum in human cells. J Biol Chem. 2003; 278(21):18767-18775. (Pubitemid 36799258)
33. McCulloch SD, Kokoska RJ, Masutani C, Iwai S, Hanaoka F, Kunkel TA. Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature. 2004;428(6978): 97-100. (Pubitemid 38332365)
34. Li Z, Xiao W, McCormick JJ, Maher VM. Identification of a protein essential for a major pathway used by human cells to avoid UV- induced DNA damage. Proc Natl Acad Sci U S A. 2002;99(7): 4459-4464. (Pubitemid 34286007)
35. Küppers R. The biology of Hodgkin's lymphoma. Nat Rev Cancer. 2009;9(1):15-27.
36. Chen L, Apgar J, Huynh L, et al. ZAP-70 directly enhances IgM signaling in chronic lymphocytic leukemia. Blood. 2005;105(5):2036-2041. (Pubitemid 40731789)
37. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000; 403(6769):503-511. (Pubitemid 30082188)
38. Clark HM, Yano T, Otsuki T, Jaffe ES, Shibata D, Raffeld M. Mutations in the coding region of c-MYC in AIDS-associated and other aggressive lymphomas. Cancer Res. 1994;54(13):3383-3386. (Pubitemid 24225954)
39. Ichikawa A, Hotta T, Takagi N, et al. Mutations of p53 gene and their relation to disease progression in B-cell lymphoma. Blood. 1992;79(10): 2701-2707.
40. Lee JW, Yoo NJ, Soung YH, et al. BRAF mutations in non-Hodgkin's lymphoma. Br J Cancer. 2003;89(10):1958-1960.
41. Tanaka S, Louie DC, Kant JA, Reed JC. Frequent incidence of somatic mutations in translocated BCL2 oncogenes of non-Hodgkin's lymphomas. Blood. 1992;79(1):229-237.
42. Yamaguchi H, Inokuchi K, Tarusawa M, Dan K. Mutation of bcl-x gene in non-Hodgkin's lymphoma. Am J Hematol. 2002;69(1):74-76.
43. Migliazza A, Martinotti S, Chen W, et al. Frequent somatic hypermutation of the 5′ noncoding region of the BCL6 gene in B-cell lymphoma. Proc Natl Acad Sci U S A. 1995;92(26):12520-12524.
44. Fearon DT, Manders P, Wagner SD. Arrested differentiation, the self-renewing memory lymphocyte, and vaccination. Science. 2001;293(5528): 248-250. (Pubitemid 32694731)
45. Klein U, Dalla-Favera R. Germinal centres: role in B-cell physiology and malignancy. Nat Rev Immunol. 2008;8(1):22-33.
46. Pasqualucci L, Migliazza A, Fracchiolla N, et al. BCL6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc Natl Acad Sci U S A. 1998; 95(20):11816-11821. (Pubitemid 28460497)
47. Shaffer AL, Yu X, He Y, Boldrick J, Chan EP, Staudt LM. BCL6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity. 2000;13(2):199-212.
48. Wagner SD, Elvin JG, Norris P, McGregor JM, Neuberger MS. Somatic hypermutation of Ig genes in patients with xeroderma pigmentosum (XP-D). Int Immunol. 1996;8(5):701-705. (Pubitemid 26148291)
49. Kim N, Kage K, Matsuda F, Lefranc MP, Storb U. B lymphocytes of xeroderma pigmentosum or Cockayne syndrome patients with inherited defects in nucleotide excision repair are fully capable of somatic hypermutation of immunoglobulin genes. J Exp Med. 1997;186(3):413-419. (Pubitemid 27332899)
50. Küppers R, Klein U, Hansmann ML, Rajewsky K. Cellular origin of human B-cell lymphomas. N Engl J Med. 1999;341(20):1520-1529. (Pubitemid 29526356)