AID dysregulation in lupus-prone MRL/Fas^lpr/lpr mice increases class switch DNA recombination and promotes interchromosomal c-Myc/IgH loci translocations: Modulation by HoxC4

References

• Oates JC. The biology of reactive intermediates in systemic lupus erythematosus. Autoimmunity. 2010; 43:56–63.
   PubMed Web of Science ®Google Scholar
• Peri A. Systems biology of lupus: Mapping the impact of genomic and environmental factors on gene expression signatures, cellular signaling, metabolic pathways, hormonal and cytokine mbalance, and selecting targets for treatment. Autoimmunity. 2010; 43:32–47.
   PubMed Web of Science ®Google Scholar
• Sawalha AH, Harley JB. Antinuclear autoantibodies in systemic lupus erythematosus. Curr Opin Rheumatol. 2004; 16:534–540.
   PubMed Web of Science ®Google Scholar
• Diamond B. Autoimmunity. Immunol Rev. 2005; 204:5–8.
   PubMed Web of Science ®Google Scholar
• Waldman M, Madaio MP. Pathogenic autoantibodies in lupus nephritis. Lupus. 2005; 14:19–24.
   PubMed Web of Science ®Google Scholar
• Deshmukh US, Bagavant H, Fu SM. Role of anti-DNA antibodies in the pathogenesis of lupus nephritis. Autoimmun Rev. 2006; 5:414–418.
   PubMed Web of Science ®Google Scholar
• Elkon K, Casali P. Nature and functions of autoantibodies. Nat Rev Rheumatol. 2008; 4:491–498.
   Web of Science ®Google Scholar
• Jacob N, Stohl W. Autoantibody-dependent and autoantibody-independent roles for B cells in systemic lupus erythematosus: Past, present, and future. Autoimmunity. 2010; 43:84–97.
   PubMed Web of Science ®Google Scholar
• Casali P. Polyclonal B cell activation and antigen-driven antibody response as mechanisms of autoantibody production in SLE. Autoimmunity. 1990; 5:147–150.
   PubMed Web of Science ®Google Scholar
• Atassi MZ, Casali P. Molecular mechanisms of autoimmunity. Autoimmunity. 2008; 41:123–132.
   PubMed Web of Science ®Google Scholar
• Theofilopoulos AN, Dixon FJ. Murine models of systemic lupus erythematosus. Adv Immunol. 1985; 37:269–390.
   PubMed Web of Science ®Google Scholar
• Mevorach D, Zhou JL, Song X, Elkon KB. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J Exp Med. 1998; 188:387–392.
   PubMed Web of Science ®Google Scholar
• Tsubata T. B cell abnormality and autoimmune disorders. Autoimmunity. 2005; 38:331–337.
   PubMed Web of Science ®Google Scholar
• Di Noia JM, Neuberger MS. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem. 2007; 76:1–22.
   PubMed Web of Science ®Google Scholar
• Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol. 2008; 26:261–292.
   PubMed Web of Science ®Google Scholar
• Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature. 2003; 422:726–730.
   PubMed Web of Science ®Google Scholar
• Dickerson SK, Market E, Besmer E, Papavasiliou FN. AID mediates hypermutation by deaminating single stranded DNA. J Exp Med. 2003; 197:1291–1296.
   PubMed Web of Science ®Google Scholar
• Pham P, Bransteitter R, Petruska J, Goodman MF. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature. 2003; 424:103–107.
   PubMed Web of Science ®Google Scholar
• Sohail A, Klapacz J, Samaranayake M, Ullah A, Bhagwat AS. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Res. 2003; 31:2990–2994.
   PubMed Web of Science ®Google Scholar
• Beale RCL, Oetersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: Correlation with mutation spectra in vivo. J Mol Biol. 2004; 337:585–596.
   PubMed Web of Science ®Google Scholar
• Maizels N. Immunoglobulin gene diversification. Annu Rev Genet. 2005; 39:23–46.
   PubMed Web of Science ®Google Scholar
• Teng G, Papavasiliou FN. Immunoglobulin somatic hypermutation. Annu Rev Genet. 2007; 41:107–120.
   PubMed Web of Science ®Google Scholar
• Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, Scharff MD. The biochemistry of somatic hypermutation. Annu Rev Immunol. 2008; 26:481–511.
   PubMed Web of Science ®Google Scholar
• Diaz M, Casali P. Somatic immunoglobulin hypermutation. Curr Opin Immunol. 2002; 14:235–240.
   PubMed Web of Science ®Google Scholar
• Papavasiliou FN, Schatz DG. Somatic hypermutation of immunoglobulin genes: Merging mechanisms for genetic diversity. Cell. 2002; 109 Suppl:S35–S44.
   PubMed Web of Science ®Google Scholar
• Wu X, Feng J, Komori A, Kim EC, Zan H, Casali P. Immunoglobulin somatic hypermutation: Double-strand DNA breaks, AID and error-prone DNA repair. J Clin Immunol. 2003; 23:235–246.
   PubMed Web of Science ®Google Scholar
• Xu Z, Fulop Z, Zhong Y, Evinger AJ, Zan H, Casali P. DNA lesions and repair in immunoglobulin class switch recombination and somatic hypermutation. Ann NY Acad Sci. 2005; 1050:146–162.
   PubMed Web of Science ®Google Scholar
• Xu Z, Pone EJ, Al-Qahtani A, Park SR, Zan H, Casali P. Regulation of aicda expression and AID activity: Relevance to somatic hypermutation and class switch DNA recombination. Crit Rev Immunol. 2007; 27:367–397.
   PubMed Web of Science ®Google Scholar
• Xu Z, Zan H, Pal Z, Casali P. DNA replication to aid somatic hypermutation. Adv Exp Med Biol. 2007; 596:111–127.
   PubMed Web of Science ®Google Scholar
• Robbiani DF, Bunting S, Feldhahn N, Bothmer A, Camps J, Deroubaix S, McBride KM, Klein IA, Stone G, Eisenreich TR, Ried T, Nussenzweig A, Nussenzweig MC. AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol Cell. 2009; 36:631–641.
   PubMed Web of Science ®Google Scholar
• Zan H, Zhang J, Ardeshna S, Xu Z, Park SR, Casali P. Lupus-prone MRL/faslpr/lpr mice display increased AID expression and extensive DNA lesions, comprising deletions and insertions, in the immunoglobulin locus: Concurrent upregulation of somatic hypermutation and class switch DNA recombination. Autoimmunity. 2009; 42:89–103.
   PubMed Web of Science ®Google Scholar
• Liu S, Cerutti A, Casali P, Crow MK. Ongoing immunoglobulin class switch DNA recombination in lupus B cells: Analysis of switch regulatory regions. Autoimmunity. 2004; 37:431–443.
   PubMed Web of Science ®Google Scholar
• Kasaian MT, Ikematsu H, Casali P. Identification and analysis of a novel human surface CD5 − B lymphocyte subset producing natural antibodies. J Immunol. 1992; 148:2690–2702.
   PubMed Web of Science ®Google Scholar
• Hirose S, Wakiya M, Kawano-Nishi Y, Yi J, Sanokawa R, Taki S, Shimamura T, Kishimoto T, Tsurui H, Nishimura H, Shirai T. Somatic diversification and affinity maturation of IgM and IgG anti-DNA antibodies in murine lupus. Eur J Immunol. 1993; 23:2813–2820.
   PubMed Web of Science ®Google Scholar
• Kasaian MT, Casali P. Autoimmunity-prone B-1 (CD5 B) cells, natural antibodies and self recognition. Autoimmunity. 1993; 15:315–329.
   PubMed Web of Science ®Google Scholar
• Kasaian MT, Ikematsu H, Balow JE, Casali P. Structure of the VH and VL segments of monoreactive and polyreactive IgA autoantibodies to DNA in patients with systemic lupus erythematosus. J Immunol. 1994; 152:3137–3151.
   PubMed Web of Science ®Google Scholar
• Dorner T, Kaschner S, Hansen A, Pruss A, Lipsky PE. Perturbations in the impact of mutational activity on Vlambda genes in systemic lupus erythematosus. Arthritis Res. 2001; 3:368–374.
   PubMedGoogle Scholar
• Sekine H, Watanabe H, Gilkeson GS. Enrichment of anti-glomerular antigen antibody-producing cells in the kidneys of MRL/MpJ-Fas(lpr) mice. J Immunol. 2004; 172:3913–3921.
   PubMed Web of Science ®Google Scholar
• Guo W, Smith D, Aviszus K, Detanico T, Heiser RA, Wysocki LJ. Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity. J Exp Med. 2010; 207:2225–2237.
   PubMed Web of Science ®Google Scholar
• Hsu HC, Zhou T, Kim H, Barnes S, Yang P, Wu Q, Zhou J, Freeman BA, Luo M, Mountz JD. Production of a novel class of polyreactive pathogenic autoantibodies in BXD2 mice causes glomerulonephritis and arthritis. Arthritis Rheum. 2006; 54:343–355.
   PubMed Web of Science ®Google Scholar
• Hsu HC, Wu Y, Yang P, Wu Q, Job G, Chen J, Wang J, Accavitti-Loper MA, Grizzle WE, Carter RH, Mountz JD. Overexpression of activation-induced cytidine deaminase in B cells is associated with production of highly pathogenic autoantibodies. J Immunol. 2007; 178:5357–5365.
   PubMed Web of Science ®Google Scholar
• Jiang C, Foley J, Clayton N, Kissling G, Jokinen M, Herbert R, Diaz M. Abrogation of lupus nephritis in activation-induced deaminase-deficient MRL/lpr mice. J Immunol. 2007; 178:7422–7431.
   PubMed Web of Science ®Google Scholar
• Jiang C, Zhao ML, Diaz M. Activation-induced deaminase heterozygous MRL/lpr mice are delayed in the production of high-affinity pathogenic antibodies and in the development of lupus nephritis. Immunology. 2009; 126:102–113.
   PubMed Web of Science ®Google Scholar
• Jiang C, Zhao M-L, Scearce RM, Diaz M. Activation-induced deaminase-deficient MRL/lpr mice secrete high levels of protective antibodies against lupus nephritis. Arthritis Rheum. 2011; 63:1086–1096.
   PubMed Web of Science ®Google Scholar
• Sultan SM, Ioannou Y, Isenberg DA. Is there an association of malignancy with systemic lupus erythematosus? An analysis of 276 patients under long-term review. Rheumatology. 2000; 39:1147–1152.
   PubMed Web of Science ®Google Scholar
• Cibere J, Sibley J, Haga M. Systemic lupus erythematosus and the risk of malignancy. Lupus. 2001; 10:394–400.
   PubMed Web of Science ®Google Scholar
• Nived O, Bengtsson A, Jonsen A, Sturfelt G, Olsson H. Malignancies during follow-up in an epidemiologically defined systemic lupus erythematosus inception cohort in southern Sweden. Lupus. 2001; 10:500–504.
   PubMed Web of Science ®Google Scholar
• Bernatsky S, Clarke A, Ramsey-Goldman R. Malignancy and systemic lupus erythematosus. Curr Rheumatol Rep. 2002; 4:351–358.
   PubMedGoogle Scholar
• Bjornadal L, Lofstrom B, Yin L, Lundberg IE, Ekbom A. Increased cancer incidence in a Swedish cohort of patients with systemic lupus erythematosus. Scand J Rheumatol. 2002; 31:66–71.
   PubMed Web of Science ®Google Scholar
• Moss KE, Ioannou Y, Sultan SM, Haq I, Isenberg DA. Outcome of a cohort of 300 patients with systemic lupus erythematosus attending a dedicated clinic for over two decades. Ann Rheum Dis. 2002; 61:409–413.
   PubMed Web of Science ®Google Scholar
• Bernatsky S, Boivin JF, Joseph L, Rajan R, Zoma A, Manzi S. An international cohort study of cancer in systemic lupus erythematosus. Arthritis Rheum. 2005; 52:1481–1490.
   PubMed Web of Science ®Google Scholar
• Parikh-Patel A, White RH, Allen M, Cress R. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control. 2008; 19:887–894.
   PubMed Web of Science ®Google Scholar
• Gayed M, Bernatsky S, Ramsey-Goldman R, Clarke A, Gordon C. Lupus and cancer. Lupus. 2009; 18:479–485.
   PubMed Web of Science ®Google Scholar
• Bernatsky S, Ramsey-Goldman R, Isenberg D, Rahman A, Dooley MA, Sibley J, Boivin JF, Joseph L, Armitage J, Zoma A, Clarke A. Hodgkin's lymphoma in systemic lupus erythematosus. Rheumatology. 2007; 46:830–832.
   PubMed Web of Science ®Google Scholar
• Kuppers R, Dalla-Favera R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene. 2001; 20:5580–5594.
   PubMed Web of Science ®Google Scholar
• Kuppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer. 2005; 5:251–262.
   PubMed Web of Science ®Google Scholar
• Schaffer A, Kim EC, Wu X, Zan H, Testoni L, Salamon S, Cerutti A, Casali P. Selective inhibition of class switching to IgG and IgE by recruitment of the HoxC4 and Oct-1 homeodomain proteins and Ku70/Ku86 to newly identified ATTT cis-elements. J Biol Chem. 2003; 278:23141–23150.
   PubMed Web of Science ®Google Scholar
• Kim EC, Edmonston CR, Wu X, Schaffer A, Casali P. The HoxC4 homeodomain protein mediates activation of the immunoglobulin heavy chain 3′ hs1,2 enhancer in human B cells. Relevance to class switch DNA recombination. J Biol Chem. 2004; 279:42258–42269.
   PubMed Web of Science ®Google Scholar
• Park SR, Zan H, Pal Z, Zhang J, Al-Qahtani A, Pone EJ, Xu Z, Mai T, Casali P. HoxC4 binds to the promoter of the cytidine deaminase AID gene to induce AID expression, class-switch DNA recombination and somatic hypermutation. Nat Immunol. 2009; 10:540–550.
   PubMed Web of Science ®Google Scholar
• Delker RK, Fugmann SD, Papavasiliou FN. A coming-of-age story: Activation-induced cytidine deaminase turns 10. Nat Immunol. 2009; 10:1147–1153.
   Google Scholar
• Mai T, Zan H, Zhang J, Hawkins JS, Xu Z, Casali P. Estrogen receptors bind to and activate the HOXC4/HoxC4 promoter to potentiate HoxC4-mediated activation-induced cytosine deaminase induction, immunoglobulin class switch DNA recombination, and somatic hypermutation. J Biol Chem. 2010; 285:37797–37810.
   PubMed Web of Science ®Google Scholar
• Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkin Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000; 102:553–563.
   PubMed Web of Science ®Google Scholar
• Xu Z, Fulop Z, Wu G, Pone EJ, Zhang J, Mai T, Thomas LM, Al-Qahtani A, White CA, Park SR, Steinacker P, Li Z, Yates J, Herron B, Otto M, Zan H, Fu H, Casali P. 14-3-3 adaptor proteins recruit AID to 5′-AGCT-3′-rich switch regions for class switch recombination. Nat Struct Mol Biol. 2010; 17:1124–1135.
   PubMed Web of Science ®Google Scholar
• Hughes GC, Martin D, Zhang K, Hudkins KL, Alpers CE, Clark EA, Elkon KB. Decrease in glomerulonephritis and Th1-associated autoantibody production after progesterone treatment in NZB/NZW mice. Arthritis Rheum. 2009; 60:1775–1784.
   PubMed Web of Science ®Google Scholar
• Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, Muramatsu M, Honjo T, Nussenzweig A, Nussenzweig MC. AID is required for c-myc/IgH chromosome translocations in vivo. Cell. 2004; 118:431–438.
   PubMed Web of Science ®Google Scholar
• Ramiro AR, Jankovic M, Callen E, Difilippantonio S, Chen HT, McBride KM, Eisenreich TR, Chen J, Dickins RA, Lowe SW, Nussenzweig A, Nussenzweig MC. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature. 2006; 440:105–109.
   PubMedGoogle Scholar
• Ogden CA, Kowalewski R, Peng Y, Montenegro V, Elkon KB. IgM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity. 2005; 38:259–264.
   PubMed Web of Science ®Google Scholar
• Binder CJ, Silverman GJ. Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin Immunopathol. 2005; 26:385–404.
   PubMed Web of Science ®Google Scholar
• Peng Y, Kowalewski R, Kim S, Elkon KB. The role of IgM antibodies in the recognition and clearance of apoptotic cells. Mol Immunol. 2005; 42:781–787.
   PubMed Web of Science ®Google Scholar
• Ait-Azzouzene D, Kono DH, Gonzalez-Quintial R, McHeyzer-Williams LJ, Lim M, Wickramarachchi D, Gerdes T, Gavin AL, Skog P, McHeyzer-Williams MG, Nemazee D, Theofilopoulos AN. Deletion of IgG-switched autoreactive B cells and defects in Fas(lpr) lupus mice. J Immunol. 2010; 185:1015–1027.
   PubMed Web of Science ®Google Scholar
• Cohen-Solal JF, Jeganathan V, Hill L, Kawabata D, Rodriguez-Pinto D, Grimaldi C, Diamond B. Hormonal regulation of B-cell function and systemic lupus erythematosus. Lupus. 2008; 17:528–532.
   PubMed Web of Science ®Google Scholar
• Greenstein B, Roa R, Dhaher Y, Nunn E, Greenstein A, Khamashta M, Hughes GR. Estrogen and progesterone receptors in murine models of systemic lupus erythematosus. Int Immunopharmacol. 2001; 1:1025–1035.
   PubMed Web of Science ®Google Scholar
• Vinuesa CG, Sanz I, Cook MC. Dysregulation of germinal centres in autoimmune disease. Nat Rev Immunol. 2009; 9:845–857.
   PubMed Web of Science ®Google Scholar
• Ehrenfeld M, Abu-Shakra M, Buskila D, Shoenfeld Y. The dual association between lymphoma and autoimmunity. Blood Cells Mol Dis. 2001; 27:750–756.
   PubMed Web of Science ®Google Scholar
• Kiss E, Kovacs L, Szodoray P. Malignancies in systemic lupus erythematosus. Autoimmun Rev. 2010; 9:195–199.
   PubMed Web of Science ®Google Scholar
• Armitage JO. 2001. Malignancies of lymphoid cells. New York: McGraw-Hill.
   Google Scholar
• Bijl J, van Oostveen JW, Kreike M, Rieger E, van der Raaij-Helmer LM, Walboomers JM, Corte G, Boncinelli E, van den Brule AJ, Meijer CJ. Expression of HOXC4, HOXC5, and HOXC6 in human lymphoid cell lines, leukemias, and benign and malignant lymphoid tissue. Blood. 1996; 87:1737–1745.
   PubMed Web of Science ®Google Scholar
• Bijl JJ, van Oostveen JW, Walboomers JM, Horstman A, van den Brule AJ, Willemze R, Meijer CJ. HOXC4, HOXC5, and HOXC6 expression in non-Hodgkin's lymphoma: Preferential expression of the HOXC5 gene in primary cutaneous anaplastic T-cell and oro-gastrointestinal tract mucosa-associated B-cell lymphomas. Blood. 1997; 90:4116–4125.
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Guglielmino R, Houldsworth J, Mohr J, Aoufouchi S, Polakiewicz R, Chaganti RS, Dalla-Favera R. Expression of the AID protein in normal and neoplastic B cells. Blood. 2004; 104:3318–3325.
   PubMed Web of Science ®Google Scholar
• Guikema JE, Rosati S, Akkermans K, Bende RJ, van Noesel CJ, van Krieken JH, Hansmann ML, Schuuring E, Kluin PM. Quantitative RT-PCR analysis of activation-induced cytidine deaminase expression in tissue samples from mantle cell lymphoma and B-cell chronic lymphocytic leukemia patients. Blood. 2005; 105:2997–2999.
   PubMed Web of Science ®Google Scholar
• Zan H, Wu X, Komori A, Holloman WK, Casali P. AID-dependent generation of resected double-strand DNA breaks and recruitment of Rad52/Rad51 in somatic hypermutation. Immunity. 2003; 18:727–738.
   PubMed Web of Science ®Google Scholar
• Zan H, Casali P. AID- and Ung-dependent generation of staggered double-strand DNA breaks in immunoglobulin class switch DNA recombination: A post-cleavage role for AID. Mol Immunol. 2008; 46:45–61.
   PubMed Web of Science ®Google Scholar
• Zan H, Zhang J, Al-Qahtani A, Pone EJ, White CA, Lee D, Yel L, Mai T, Casali P. Endonuclease G plays a role in immunoglobulin class switch DNA recombination by introducing double-strand breaks in switch regions. Mol Immunol. 2011; 48:610–622.
   PubMed Web of Science ®Google Scholar
• Dorsett Y, McBride KM, Jankovic M, Gazumyan A, Thai TH, Robbiani DF, Di Virgilio M, Reina San-Martin B, Heidkamp G, Schwickert TA, Eisenreich T, Rajewsky K, Nussenzweig MC. MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity. 2008; 28:630–638.
   PubMed Web of Science ®Google Scholar
• Takizawa M, Tolarova H, Li Z, Dubois W, Lim S, Callen E, Franco S, Mosaico M, Feigenbaum L, Alt FW, Nussenzweig A, Potter M, Casellas R. AID expression levels determine the extent of c-Myc oncogenic translocations and the incidence of B cell tumor development. J Exp Med. 2008; 205:1949–1957.
   PubMed Web of Science ®Google Scholar