Genomic uracil homeostasis during normal B cell maturation and loss of this balance during B cell cancer development

Molecular and Cellular Biology

Volumn 34, Issue 21, 2014, Pages 4019-4032

  Shalhout, Sophia ^a   Haddad, Dania ^b   Sosin, Angela ^c   Holland, Thomas C ^c   Al Katib, Ayad ^c   Martin, Alberto ^b   Bhagwata, Ashok S ^a,c  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; DNA GLYCOSYLTRANSFERASE; GENOMIC DNA; TRANSCRIPTOME; URACIL; URACIL DNA GLYCOSIDASE; AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); CYTIDINE DEAMINASE; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; B LYMPHOCYTE; CARCINOGENESIS; CELL LEVEL; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENOMICS; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LYMPHOMA CELL LINE; MALE; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; SPLEEN CELL; TRANSIENT TRANSFECTION; WILD TYPE; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; GENOME; LIVER; LYMPHOPROLIFERATIVE DISEASE; METABOLISM; PALATINE TONSIL; PATHOLOGY; SPLEEN; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; B-LYMPHOCYTES; CELL LINE, TUMOR; CYTIDINE DEAMINASE; GENOME; HUMANS; LIPOPOLYSACCHARIDES; LIVER; LYMPHOPROLIFERATIVE DISORDERS; MICE, INBRED C57BL; MICE, TRANSGENIC; PALATINE TONSIL; SPLEEN; URACIL; URACIL-DNA GLYCOSIDASE;

EID: 84907810906     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00589-14     Document Type: Article

References (59)

1. Bransteitter R, Pham P, Scharff MD, Goodman MF. 2003. Activationinduced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. U. S. A. 100:4102-4107. http://dx.doi.org/10.1073/pnas.0730835100.
2. Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW. 2003. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422:726-730. http://dx.doi.org/10.1038/nature01574.
3. Dickerson SK, Market E, Besmer E, Papavasiliou FN. 2003. AID mediates hypermutation by deaminating single stranded DNA. J. Exp. Med. 197:1291-1296. http://dx.doi.org/10.1084/jem.20030481.
4. Sohail A, Klapacz J, Samaranayake M, Ullah A, Bhagwat AS. 2003. Human activation-induced cytidine deaminase causes transcriptiondependent, strand-biased C to U deaminations. Nucleic Acids Res. 31: 2990-2994. http://dx.doi.org/10.1093/nar/gkg464.
5. Di Noia JM, Neuberger MS. 2007. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76:1-22. http://dx.doi.org /10.1146/annurev.biochem.76.061705.090740.
6. Samaranayake M, Bujnicki JM, Carpenter M, Bhagwat AS. 2006. Evaluation of molecular models for the affinity maturation of antibodies: roles of cytosine deamination by AID and DNA repair. Chem. Rev. 106:700- 719. http://dx.doi.org/10.1021/cr040496t.
7. Stavnezer J, Guikema JE, Schrader CE. 2008. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26:261-292. http: //dx.doi.org/10.1146/annurev.immunol.26.021607.090248.
8. Yamane A, Resch W, Kuo N, Kuchen S, Li Z, Sun HW, Robbiani DF, McBride K, Nussenzweig MC, Casellas R. 2011. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat. Immunol. 12:62-69. http://dx.doi .org/10.1038/ni.1964.
9. Bemark M, Neuberger MS. 2000. The c-MYC allele that is translocated into the IgH locus undergoes constitutive hypermutation in a Burkitt's lymphoma line. Oncogene 19:3404-3410. http://dx.doi.org/10.1038/sj.onc.1203686.
10. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, Kleinstein SH, Schatz DG. 2008. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451:841-845. http://dx.doi.org/10.1038 /nature06547.
11. Pasqualucci L, Migliazza A, Fracchiolla N, William C, Neri A, Baldini L, Chaganti RS, Klein U, Kuppers R, Rajewsky K, Dalla-Favera R. 1998. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc. Natl. Acad. Sci. U. S. A. 95: 11816-11821. http://dx.doi.org/10.1073/pnas.95.20.11816.
12. Shen HM, Peters A, Baron B, Zhu X, Storb U. 1998. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280:1750 -1752. http://dx.doi.org/10.1126/science.280.5370.1750.
13. Petersen-Mahrt SK, Harris RS, Neuberger MS. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99-103. http://dx.doi.org/10.1038/nature00862.
14. Poltoratsky V, Goodman MF, Scharff MD. 2000. Error-prone candidates vie for somatic mutation. J. Exp. Med. 192:F27-F30. http://dx.doi.org/10.1084/jem.192.10.F27.
15. Nilsen H, Rosewell I, Robins P, Skjelbred CF, Andersen S, Slupphaug G, Daly G, Krokan HE, Lindahl T, Barnes DE. 2000. Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol. Cell 5:1059-1065. http://dx.doi.org/10.1016/S1097-2765(00)80271-3.
16. Di Noia JM, Williams GT, Chan DT, Buerstedde JM, Baldwin GS, Neuberger MS. 2007. Dependence of antibody gene diversification on uracil excision. J. Exp. Med. 204:3209-3219. http://dx.doi.org/10.1084 /jem.20071768.
17. Winter DB, Phung QH, Umar A, Baker SM, Tarone RE, Tanaka K, Liskay RM, Kunkel TA, Bohr VA, Gearhart PJ. 1998. Altered spectra of hypermutation in antibodies from mice deficient for the DNA mismatch repair protein PMS2. Proc. Natl. Acad. Sci. U. S. A. 95:6953-6958. http: //dx.doi.org/10.1073/pnas.95.12.6953.
18. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, Honjo T. 2003. Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197:1173-1181. http://dx.doi.org/10.1084/jem.20030275.
19. Lossos IS, Levy R, Alizadeh AA. 2004. AID is expressed in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity. Leukemia 18:1775- 1779. http://dx.doi.org/10.1038/sj.leu.2403488.
20. Pasqualucci L, Guglielmino R, Houldsworth J, Mohr J, Aoufouchi S, Polakiewicz R, Chaganti RS, Dalla-Favera R. 2004. Expression of the AID protein in normal and neoplastic B cells. Blood 104:3318-3325. http: //dx.doi.org/10.1182/blood-2004-04-1558.
21. Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, Muramatsu M, Honjo T, Nussenzweig A, Nussenzweig MC. 2004. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118: 431-438. http://dx.doi.org/10.1016/j.cell.2004.08.006.
22. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, Bolland DJ, Chen HT, Corcoran AE, Nussenzweig A, Nussenzweig MC. 2008. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135:1028-1038. http: //dx.doi.org/10.1016/j.cell.2008.09.062.
23. Andersen S, Ericsson M, Dai HY, Pena-Diaz J, Slupphaug G, Nilsen H, Aarset H, Krokan HE. 2005. Monoclonal B-cell hyperplasia and leukocyte imbalance precede development of B-cell malignancies in uracil-DNA glycosylase deficient mice. DNA Repair 4:1432-1441. http://dx.doi.org/10.1016/j.dnarep.2005.08.004.
24. Robbiani DF, Nussenzweig MC. 2013. Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu. Rev. Pathol. 8:79-103. http://dx.doi.org/10.1146/annurev-pathol-020712-164004.
25. Maul RW, Saribasak H, Martomo SA, McClure RL, Yang W, Vaisman A, Gramlich HS, Schatz DG, Woodgate R, Wilson DM, III, Gearhart PJ. 2011. Uracil residues dependent on the deaminase AID in immunoglobulin gene variable and switch regions. Nat. Immunol. 12:70-76. http://dx.doi.org/10.1038/ni.1970.
26. Roche B, Claes A, Rougeon F. 2010. Deoxyuridine triphosphate incorporation during somatic hypermutation of mouse VkOx genes after immunization with phenyloxazolone. J. Immunol. 185:4777-4782. http://dx.doi.org/10.4049/jimmunol.1001459.
27. Chiarle R, Zhang Y, Frock RL, Lewis SM, Molinie B, Ho YJ, Myers DR, Choi VW, Compagno M, Malkin DJ, Neuberg D, Monti S, Giallourakis CC, Gostissa M, Alt FW. 2011. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147:107-119. http://dx.doi.org/10.1016/j.cell.2011.07.049.
28. Klein IA, Resch W, Jankovic M, Oliveira T, Yamane A, Nakahashi H, Di Virgilio M, Bothmer A, Nussenzweig A, Robbiani DF, Casellas R, Nussenzweig MC. 2011. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147:95-106. http://dx.doi.org/10.1016/j.cell.2011.07.048.
29. Zhang W, Bardwell PD, Woo CJ, Poltoratsky V, Scharff MD, Martin A. 2001. Clonal instability of V region hypermutation in the Ramos Burkitt's lymphoma cell line. Int. Immunol. 13:1175-1184. http://dx.doi.org/10.1093/intimm/13.9.1175.
30. Kubo K, Ide H, Wallace SS, Kow YW. 1992. A novel, sensitive, and specific assay for abasic sites, the most commonly produced DNA lesion. Biochemistry 31:3703-3708. http://dx.doi.org/10.1021/bi00129a020.
31. Ide H, Akamatsu K, Kimura Y, Michiue K, Makino K, Asaeda A, Takamori Y, Kubo K. 1993. Synthesis and damage specificity of a novel probe for the detection of abasic sites in DNA. Biochemistry 32:8276- 8283. http://dx.doi.org/10.1021/bi00083a031.
32. Cabelof DC, Nakamura J, Heydari AR. 2006. A sensitive biochemical assay for the detection of uracil. Environ. Mol. Mutagen. 47:31-37. http: //dx.doi.org/10.1002/em.20165.
33. Lari SU, Chen CY, Vertessy BG, Morre J, Bennett SE. 2006. Quantitative determination of uracil residues in Escherichia coli DNA: contribution of ung, dug, and dut genes to uracil avoidance. DNA Repair 5:1407-1420. http://dx.doi.org/10.1016/j.dnarep.2006.06.009.
34. Parisien R, Bhagwat AS. 2009.Studying antibody maturation using techniques for detecting uracils in DNA, p 127-143. In Grosjean H (ed), DNA and RNA modification enzymes: comparative structure, mechanism, functions, cellular interactions and evolution. Landes Bioscience, Austin, TX.
35. Unniraman S, Schatz DG. 2007. Strand-biased spreading of mutations during somatic hypermutation. Science 317:1227-1230. http://dx.doi.org /10.1126/science.1145065.
36. Doseth B, Visnes T, Wallenius A, Ericsson I, Sarno A, Pettersen HS, Flatberg A, Catterall T, Slupphaug G, Krokan HE, Kavli B. 2011. Uracil-DNA glycosylase in base excision repair and adaptive immunity: species differences between man and mouse. J. Biol. Chem. 286:16669- 16680. http://dx.doi.org/10.1074/jbc.M111.230052.
37. Fritz EL, Rosenberg BR, Lay K, Mihailovic A, Tuschl T, Papavasiliou FN. 2013.Acomprehensive analysis of the effects of the deaminase AID on the transcriptome and methylome of activated B cells. Nat. Immunol. 14:749-755. http://dx.doi.org/10.1038/ni.2616.
38. Dingler FA, Kemmerich K, Neuberger MS, Rada C. 27 May 2014. Uracil excision by endogenous SMUG1 glycosylase promotes efficient Ig class switching and impacts on A:T substitutions during somatic mutation. Eur. J. Immunol. http://dx.doi.org/10.1002/eji.201444482.
39. Nakamura M, Kondo S, Sugai M, Nazarea M, Imamura S, Honjo T. 1996. High frequency class switching of an IgM_ B lymphoma clone CH12F3 to IgA_ cells. Int. Immunol. 8:193-201. http://dx.doi.org/10.1093/intimm/8.2.193.
40. Seitz V, Hummel M, Walter J, Stein H. 2003. Evolution of classic Hodgkin lymphoma in correlation to changes in the lymphoid organ structure of vertebrates. Dev. Comp. Immunol. 27:43-53. http://dx.doi.org/10.1016/S0145-305X(02)00042-3.
41. Greiner A, Tobollik S, Buettner M, Jungnickel B, Herrmann K, Kremmer E, Niedobitek G. 2005. Differential expression of activation-induced cytidine deaminase (AID) in nodular lymphocyte-predominant and classical Hodgkin lymphoma. J. Pathol. 205:541-547. http://dx.doi.org/10.1002/path.1746.
42. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646-674. http://dx.doi.org/10.1016/j.cell.2011.02.013.
43. Martin A, Bardwell PD, Woo CJ, Fan M, Shulman MJ, Scharff MD. 2002. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature 415:802-806. http://dx.doi.org/10.1038 /nature714.
44. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW. 2008.WHO classification of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon, France.
45. Heintel D, Kroemer E, Kienle D, Schwarzinger I, Gleiss A, Schwarzmeier J, Marculescu R, Le T, Mannhalter C, Gaiger A, Stilgenbauer S, Döhner H, Fonatsch C, Jäger U, German CLL Study Group. 2004. High expression of activation-induced cytidine deaminase (AID) mRNA is associated with unmutated IGVH gene status and unfavourable cytogenetic aberrations in patients with chronic lymphocytic leukaemia. Leukemia 18:756-762. http://dx.doi.org/10.1038/sj.leu.2403294.
46. Oppezzo P, Vuillier F, Vasconcelos Y, Dumas G, Magnac C, Payelle-Brogard B, Pritsch O, Dighiero G. 2003. Chronic lymphocytic leukemia B cells expressing AID display dissociation between class switch recombination and somatic hypermutation. Blood 101:4029-4032. http://dx.doi.org/10.1182/blood-2002-10-3175.
47. Kim N, Jinks-Robertson S. 2009. dUTP incorporation into genomicDNA is linked to transcription in yeast. Nature 459:1150-1153. http://dx.doi.org/10.1038/nature08033.
48. Galashevskaya A, Sarno A, Vagbo CB, Aas PA, Hagen L, Slupphaug G, Krokan HE. 2013. A robust, sensitive assay for genomic uracil determination by LC/MS/MS reveals lower levels than previously reported. DNA Repair 12:699-706. http://dx.doi.org/10.1016/j.dnarep.2013.05.002.
49. Mashiyama ST, Hansen CM, Roitman E, Sarmiento S, Leklem JE, Shultz TD, Ames BN. 2008. An assay for uracil in human DNA at baseline: effect of marginal vitamin B6 deficiency. Anal. Biochem. 372:21-31. http://dx.doi.org/10.1016/j.ab.2007.08.034.
50. Li G, Zan H, Xu Z, Casali P. 2 May 2013. Epigenetics of the antibody response. Trends Immunol. http://dx.doi.org/10.1016/j.it.2013.03.006.
51. Storb U. 2014. Why does somatic hypermutation by AID require transcription of its target genes? Adv. Immunol. 122:253-277. http://dx.doi.org/10.1016/B978-0-12-800267-4.00007-9.
52. Zan H, White CA, Thomas LM, Mai T, Li G, Xu Z, Zhang J, Casali P. 2012. Rev1 recruits ung to switch regions and enhances du glycosylation for immunoglobulin class switch DNA recombination. Cell Rep. 2:1220- 1232. http://dx.doi.org/10.1016/j.celrep.2012.09.029.
53. An Q, Robins P, Lindahl T, Barnes DE. 2005. C -_ T mutagenesis and gamma-radiation sensitivity due to deficiency in the Smug1 and UngDNA glycosylases. EMBO J. 24:2205-2213. http://dx.doi.org/10.1038/sj.emboj.7600689.
54. Nilsen H, Stamp G, Andersen S, Hrivnak G, Krokan HE, Lindahl T, Barnes DE. 2003. Gene-targeted mice lacking the Ung uracil-DNA glycosylase develop B-cell lymphomas. Oncogene 22:5381-5386. http://dx.doi.org/10.1038/sj.onc.1206860.
55. Loeffler M, Kreuz M, Haake A, Hasenclever D, Trautmann H, Arnold C, Winter K, Koch K, Klapper W, Scholtysik R, Rosolowski M, Hoffmann S, Ammerpohl O, Szczepanowski M, Herrmann D, Küppers R, Pott C, Siebert R. 16 July 2014. Genomic and epigenomic co-evolution in follicular lymphomas. Leukemia http://dx.doi.org/10.1038/leu.2014.209.
56. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, Boyault S, Burkhardt B, Butler AP, Caldas C, Davies HR, Desmedt C, Eils R, Eyfjord JE, Foekens JA, Greaves M, Hosoda F, Hutter B, Ilicic T, Imbeaud S, Imielinsk M, Jager N, Jones DT, Jones D, Knappskog S, Kool M, Lakhani SR, Lopez-Otin C, Martin S, Munshi NC, Nakamura H, Northcott PA, Pajic M, Papaemmanuil E, Paradiso A, Pearson JV, Puente XS, Raine K, Ramakrishna M, Richardson AL, Richter J, Rosenstiel P, Schlesner M, Schumacher TN, Span PN, Teague JW, et al. 2013. Signatures of mutational processes in human cancer. Nature 500:415- 421. http://dx.doi.org/10.1038/nature12477.
57. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, Jones D, Hinton J, Marshall J, Stebbings LA, Menzies A, Martin S, Leung K, Chen L, Leroy C, Ramakrishna M, Rance R, Lau KW, Mudie LJ, Varela I, McBride DJ, Bignell GR, Cooke SL, Shlien A, Gamble J, Whitmore I, Maddison M, Tarpey PS, Davies HR, Papaemmanuil E, Stephens PJ, McLaren S, Butler AP, Teague JW, Jonsson G, Garber JE, Silver D, Miron P, Fatima A, Boyault S, Langerod A, Tutt A, Martens JW, Aparicio SA, Borg A, Salomon AV, Thomas G, Borresen-Dale AL, Richardson AL, Neuberger MS, et al. 2012. Mutational processes molding the genomes of 21 breast cancers. Cell 149:979-993. http://dx.doi.org/10.1016/j.cell.2012.04.024.
58. Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P, Kiezun A, Kryukov GV, Carter SL, Saksena G, Harris S, Shah RR, Resnick MA, Getz G, Gordenin DA. 2013. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat. Genet. 45:970-976. http://dx.doi.org/10.1038/ng.2702.
59. Burns MB, Lackey L, Carpenter MA, Rathore A, Land AM, Leonard B, Refsland EW, Kotandeniya D, Tretyakova N, Nikas JB, Yee D, Temiz NA, Donohue DE, McDougle RM, Brown WL, Law EK, Harris RS. 2013. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494:366-370. http://dx.doi.org/10.1038/nature11881.