Activation-Induced Cytidine Deaminase Expression in Human B Cell Precursors Is Essential for Central B Cell Tolerance

Immunity

Volumn 43, Issue 5, 2015, Pages 884-895

  Cantaert, Tineke ^a   Schickel, Jean Nicolas ^a   Bannock, Jason M ^a   Ng, Yen Shing ^a   Massad, Christopher ^a   Oe, Tyler ^a   Wu, Renee ^a   Lavoie, Aubert ^b   Walter, Jolan E ^c,d   Notarangelo, Luigi D ^d   Al Herz, Waleed ^e   Kilic, Sara Sebnem ^f   Ochs, Hans D ^g   Nonoyama, Shigeaki ^h   Durandy, Anne ⁱ   Meffre, Eric ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Pediatrics   (Canada)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e KUWAIT UNIVERSITY   (Kuwait)

^f ULUDAG UNIVERSITY   (Turkey)

^g UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^h NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

ⁱ INSERM   (France)

Author keywords

Activation induced cytidine deaminase; AID deficient patients; B cell development; B cell tolerance

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; RAG2 PROTEIN; SHORT HAIRPIN RNA; CYTIDINE DEAMINASE; DNA BINDING PROTEIN; NUCLEAR PROTEIN; RAG2 PROTEIN, HUMAN;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE TOLERANCE; BONE MARROW; CELL CLONE; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FETUS; GENE DOSAGE; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MIDDLE AGED; MOUSE; NEWBORN; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADOLESCENT; AGED; ANIMAL; CASE CONTROL STUDY; CHILD; GENETICS; IMMUNOGLOBULIN GENE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; PRESCHOOL CHILD; SOMATIC HYPERMUTATION; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANIMALS; APOPTOSIS; CASE-CONTROL STUDIES; CENTRAL TOLERANCE; CHILD; CHILD, PRESCHOOL; CYTIDINE DEAMINASE; DNA-BINDING PROTEINS; FEMALE; GENES, IMMUNOGLOBULIN; HUMANS; LYMPHOCYTE ACTIVATION; MALE; MICE; MIDDLE AGED; NUCLEAR PROTEINS; PRECURSOR CELLS, B-LYMPHOID; RECOMBINATION, GENETIC; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; YOUNG ADULT;

EID: 84947429257     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.10.002     Document Type: Article

References (57)

1. Basso K., Dalla-Favera R. Roles of BCL6 in normal and transformed germinal center B cells. Immunol. Rev. 2012, 247:172-183.
2. Burrows P.D., Stephan R.P., Wang Y.H., Lassoued K., Zhang Z., Cooper M.D. The transient expression of pre-B cell receptors governs B cell development. Semin. Immunol. 2002, 14:343-349.
3. Crouch E.E., Li Z., Takizawa M., Fichtner-Feigl S., Gourzi P., Montaño C., Feigenbaum L., Wilson P., Janz S., Papavasiliou F.N., Casellas R. Regulation of AID expression in the immune response. J. Exp. Med. 2007, 204:1145-1156.
4. Di Noia J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 2007, 76:1-22.
5. Duy C., Yu J.J., Nahar R., Swaminathan S., Kweon S.M., Polo J.M., Valls E., Klemm L., Shojaee S., Cerchietti L., et al. BCL6 is critical for the development of a diverse primary B cell repertoire. J. Exp. Med. 2010, 207:1209-1221.
6. Fang W., Mueller D.L., Pennell C.A., Rivard J.J., Li Y.S., Hardy R.R., Schlissel M.S., Behrens T.W. Frequent aberrant immunoglobulin gene rearrangements in pro-B cells revealed by a bcl-xL transgene. Immunity 1996, 4:291-299.
7. Goodnow C.C. Balancing immunity and tolerance: deleting and tuning lymphocyte repertoires. Proc. Natl. Acad. Sci. USA 1996, 93:2264-2271.
8. Grawunder U., Leu T.M., Schatz D.G., Werner A., Rolink A.G., Melchers F., Winkler T.H. Down-regulation of RAG1 and RAG2 gene expression in preB cells after functional immunoglobulin heavy chain rearrangement. Immunity 1995, 3:601-608.
9. Green D.R., Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009, 458:1127-1130.
10. Han J.H., Akira S., Calame K., Beutler B., Selsing E., Imanishi-Kari T. Class switch recombination and somatic hypermutation in early mouse B cells are mediated by B cell and Toll-like receptors. Immunity 2007, 27:64-75.
11. Imai K., Slupphaug G., Lee W.I., Revy P., Nonoyama S., Catalan N., Yel L., Forveille M., Kavli B., Krokan H.E., et al. Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat. Immunol. 2003, 4:1023-1028.
12. Imai K., Zhu Y., Revy P., Morio T., Mizutani S., Fischer A., Nonoyama S., Durandy A. Analysis of class switch recombination and somatic hypermutation in patients affected with autosomal dominant hyper-IgM syndrome type 2. Clin. Immunol. 2005, 115:277-285.
13. Isnardi I., Ng Y.S., Srdanovic I., Motaghedi R., Rudchenko S., von Bernuth H., Zhang S.Y., Puel A., Jouanguy E., Picard C., et al. IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans. Immunity 2008, 29:746-757.
14. Ito S., Nagaoka H., Shinkura R., Begum N., Muramatsu M., Nakata M., Honjo T. Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc. Natl. Acad. Sci. USA 2004, 101:1975-1980.
15. Juszczynski P., Chen L., O'Donnell E., Polo J.M., Ranuncolo S.M., Dalla-Favera R., Melnick A., Shipp M.A. BCL6 modulates tonic BCR signaling in diffuse large B-cell lymphomas by repressing the SYK phosphatase, PTPROt. Blood 2009, 114:5315-5321.
16. Kinnunen T., Chamberlain N., Morbach H., Cantaert T., Lynch M., Preston-Hurlburt P., Herold K.C., Hafler D.A., O'Connor K.C., Meffre E. Specific peripheral B cell tolerance defects in patients with multiple sclerosis. J. Clin. Invest. 2013, 123:2737-2741.
17. Komarov P.G., Komarova E.A., Kondratov R.V., Christov-Tselkov K., Coon J.S., Chernov M.V., Gudkov A.V. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999, 285:1733-1737.
18. Kruse J.P., Gu W. Modes of p53 regulation. Cell 2009, 137:609-622.
19. Kuraoka M., Liao D., Yang K., Allgood S.D., Levesque M.C., Kelsoe G., Ueda Y. Activation-induced cytidine deaminase expression and activity in the absence of germinal centers: insights into hyper-IgM syndrome. J. Immunol. 2009, 183:3237-3248.
20. Kuraoka M., Holl T.M., Liao D., Womble M., Cain D.W., Reynolds A.E., Kelsoe G. Activation-induced cytidine deaminase mediates central tolerance in B cells. Proc. Natl. Acad. Sci. USA 2011, 108:11560-11565.
21. Li Z., Dordai D.I., Lee J., Desiderio S. A conserved degradation signal regulates RAG-2 accumulation during cell division and links V(D)J recombination to the cell cycle. Immunity 1996, 5:575-589.
22. Mao C., Jiang L., Melo-Jorge M., Puthenveetil M., Zhang X., Carroll M.C., Imanishi-Kari T. T cell-independent somatic hypermutation in murine B cells with an immature phenotype. Immunity 2004, 20:133-144.
23. Mårtensson I.L., Rolink A., Melchers F., Mundt C., Licence S., Shimizu T. The pre-B cell receptor and its role in proliferation and Ig heavy chain allelic exclusion. Semin. Immunol. 2002, 14:335-342.
24. McBride K.M., Gazumyan A., Woo E.M., Schwickert T.A., Chait B.T., Nussenzweig M.C. Regulation of class switch recombination and somatic mutation by AID phosphorylation. J. Exp. Med. 2008, 205:2585-2594.
25. Meffre E. The establishment of early B cell tolerance in humans: lessons from primary immunodeficiency diseases. Ann. N Y Acad. Sci. 2011, 1246:1-10.
26. Meffre E., Casellas R., Nussenzweig M.C. Antibody regulation of B cell development. Nat. Immunol. 2000, 1:379-385.
27. Menard L., Saadoun D., Isnardi I., Ng Y.S., Meyers G., Massad C., Price C., Abraham C., Motaghedi R., Buckner J.H., et al. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J. Clin. Invest. 2011, 121:3635-3644.
28. Menard L., Cantaert T., Chamberlain N., Tangye S.G., Riminton S., Church J.A., Klion A., Cunningham-Rundles C., Nichols K.E., Meffre E. Signaling lymphocytic activation molecule (SLAM)/SLAM-associated protein pathway regulates human B-cell tolerance. J. Allergy Clin. Immunol. 2014, 133:1149-1161.
29. Meyers G., Ng Y.S., Bannock J.M., Lavoie A., Walter J.E., Notarangelo L.D., Kilic S.S., Aksu G., Debré M., Rieux-Laucat F., et al. Activation-induced cytidine deaminase (AID) is required for B-cell tolerance in humans. Proc. Natl. Acad. Sci. USA 2011, 108:11554-11559.
30. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
31. Nemazee D. Receptor editing in lymphocyte development and central tolerance. Nat. Rev. Immunol. 2006, 6:728-740.
32. Ng Y.S., Wardemann H., Chelnis J., Cunningham-Rundles C., Meffre E. Bruton's tyrosine kinase is essential for human B cell tolerance. J. Exp. Med. 2004, 200:927-934.
33. Opferman J.T., Letai A., Beard C., Sorcinelli M.D., Ong C.C., Korsmeyer S.J. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003, 426:671-676.
34. Perez M.A., Gordon A., Sanchez F., Narvaez F., Gutierrez G., Ortega O., Nuñez A., Harris E., Balmaseda A. Severe coinfections of dengue and pandemic influenza A H1N1 viruses. Pediatr. Infect. Dis. J. 2010, 29:1052-1055.
35. Porter A.G., Jänicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
36. Qin H., Suzuki K., Nakata M., Chikuma S., Izumi N., Huong T., Maruya M., Fagarasan S., Busslinger M., Honjo T., Nagaoka H. Activation-induced cytidine deaminase expression in CD4+ T cells is associated with a unique IL-10-producing subset that increases with age. PLoS ONE 2011, 6:e29141.
37. Rada C., Jarvis J.M., Milstein C. AID-GFP chimeric protein increases hypermutation of Ig genes with no evidence of nuclear localization. Proc. Natl. Acad. Sci. USA 2002, 99:7003-7008.
38. Radic M.Z., Weigert M. Origins of anti-DNA antibodies and their implications for B-cell tolerance. Ann. N Y Acad. Sci. 1995, 764:384-396.
39. Revy P., Muto T., Levy Y., Geissmann F., Plebani A., Sanal O., Catalan N., Forveille M., Dufourcq-Labelouse R., Gennery A., et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 2000, 102:565-575.
40. Rolink A., Melchers F., Andersson J. The SCID but not the RAG-2 gene product is required for S mu-S epsilon heavy chain class switching. Immunity 1996, 5:319-330.
41. Romberg N., Chamberlain N., Saadoun D., Gentile M., Kinnunen T., Ng Y.S., Virdee M., Menard L., Cantaert T., Morbach H., et al. CVID-associated TACI mutations affect autoreactive B cell selection and activation. J. Clin. Invest. 2013, 123:4283-4293.
42. Saito M., Novak U., Piovan E., Basso K., Sumazin P., Schneider C., Crespo M., Shen Q., Bhagat G., Califano A., et al. BCL6 suppression of BCL2 via Miz1 and its disruption in diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. USA 2009, 106:11294-11299.
43. Sauer A.V., Morbach H., Brigida I., Ng Y.S., Aiuti A., Meffre E. Defective B cell tolerance in adenosine deaminase deficiency is corrected by gene therapy. J. Clin. Invest. 2012, 122:2141-2152.
44. Schatz D.G., Swanson P.C. V(D)J recombination: mechanisms of initiation. Annu. Rev. Genet. 2011, 45:167-202.
45. Schickel J.N., Pasquali J.L., Soley A., Knapp A.M., Decossas M., Kern A., Fauny J.D., Marcellin L., Korganow A.S., Martin T., Soulas-Sprauel P. Carabin deficiency in B cells increases BCR-TLR9 costimulation-induced autoimmunity. EMBO Mol. Med. 2012, 4:1261-1275.
46. Shultz L.D., Lyons B.L., Burzenski L.M., Gott B., Chen X., Chaleff S., Kotb M., Gillies S.D., King M., Mangada J., et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 2005, 174:6477-6489.
47. Smith K.G., Weiss U., Rajewsky K., Nossal G.J., Tarlinton D.M. Bcl-2 increases memory B cell recruitment but does not perturb selection in germinal centers. Immunity 1994, 1:803-813.
48. Swaminathan S., Klemm L., Park E., Papaemmanuil E., Ford A., Kweon S.M., Trageser D., Hasselfeld B., Henke N., Mooster J., et al. Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia. Nat. Immunol. 2015, 16:766-774.
49. Takizawa M., Tolarová H., Li Z., Dubois W., Lim S., Callen E., Franco S., Mosaico M., Feigenbaum L., Alt F.W., et al. AID expression levels determine the extent of cMyc oncogenic translocations and the incidence of B cell tumor development. J. Exp. Med. 2008, 205:1949-1957.
50. Tsai A.G., Lu H., Raghavan S.C., Muschen M., Hsieh C.L., Lieber M.R. Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Cell 2008, 135:1130-1142.
51. Ueda Y., Liao D., Yang K., Patel A., Kelsoe G. T-independent activation-induced cytidine deaminase expression, class-switch recombination, and antibody production by immature/transitional 1 B cells. J. Immunol. 2007, 178:3593-3601.
52. Umiker B.R., McDonald G., Larbi A., Medina C.O., Hobeika E., Reth M., Imanishi-Kari T. Production of IgG autoantibody requires expression of activation-induced deaminase in early-developing B cells in a mouse model of SLE. Eur. J. Immunol. 2014, 44:3093-3108.
53. Victora G.D., Dominguez-Sola D., Holmes A.B., Deroubaix S., Dalla-Favera R., Nussenzweig M.C. Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Blood 2012, 120:2240-2248.
54. Vikstrom I., Carotta S., Lüthje K., Peperzak V., Jost P.J., Glaser S., Busslinger M., Bouillet P., Strasser A., Nutt S.L., Tarlinton D.M. Mcl-1 is essential for germinal center formation and B cell memory. Science 2010, 330:1095-1099.
55. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
56. Zaheen A., Boulianne B., Parsa J.Y., Ramachandran S., Gommerman J.L., Martin A. AID constrains germinal center size by rendering B cells susceptible to apoptosis. Blood 2009, 114:547-554.
57. Zahn A., Eranki A.K., Patenaude A.M., Methot S.P., Fifield H., Cortizas E.M., Foster P., Imai K., Durandy A., Larijani M., et al. Activation induced deaminase C-terminal domain links DNA breaks to end protection and repair during class switch recombination. Proc. Natl. Acad. Sci. USA 2014, 111:E988-E997.