Transcriptional regulation of B cell class-switch recombination: the role in development of noninfectious complications

References

• Durandy A, Kracker S. Immunoglobulin class-switch recombination deficiencies. Arthritis Res Ther. 2012;14(4):218.
   PubMed Web of Science ®Google Scholar
• Vale AM, Kearney JF, Nobrega A, et al. Development and function of B cell subsets. Molecular Biology of B Cells: Elsevier. 2015: 99–119
   Google Scholar
• Victora GD, Nussenzweig MC. Germinal Centers. Annu Rev Immunol. 2022;40(1):413–442.
   PubMedGoogle Scholar
• Martin A, Chahwan R, Parsa JY, et al. Somatic hypermutation: the molecular mechanisms underlying the production of effective high-affinity antibodies. Molecular Biology of B Cells: Elsevier. 2015: 363–388
   Google Scholar
• Palanichamy A, Bauer JW, Yalavarthi S, et al. Neutrophil-mediated IFN activation in the bone marrow alters B cell development in human and murine systemic lupus erythematosus. J Immunol. 2014;192(3):906–918.
   PubMed Web of Science ®Google Scholar
• Sanz I, Wei C, Jenks SA, et al. Challenges and opportunities for consistent classification of human B cell and plasma cell populations. Front Immunol. 2019;10:2458.
   PubMed Web of Science ®Google Scholar
• Pan-Hammarstrom Q, Zhao Y, Hammarstrom L. Class switch recombination: a comparison between mouse and human. Adv Immunol. 2007;93:1–61.
   PubMed Web of Science ®Google Scholar
• Yazdani R, Fekrvand S, Shahkarami S, et al. The hyper IgM syndromes: epidemiology, pathogenesis, clinical manifestations, diagnosis and management. Clin Immunol. 2019;198:19–30.
   PubMed Web of Science ®Google Scholar
• Yazdani R, Abolhassani H, Kiaee F, et al. Comparison of common monogenic defects in a large predominantly antibody deficiency cohort. J Allergy Clin Immunol Pract. 2019;7:864–78 e9.
   PubMed Web of Science ®Google Scholar
• Roco JA, Mesin L, Binder SC, et al., Class-switch recombination occurs infrequently in germinal centers. Immunity. 2019;51(2):337–50 e7.
   PubMed Web of Science ®Google Scholar
• Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol. 2008;26(1):261–292.
   PubMedGoogle Scholar
• Amirifar P, Yazdani R, Azizi G, et al. Known and potential molecules associated with altered B cell development leading to predominantly antibody deficiencies. Pediatr Allergy Immunol. 2021;32(8):1601–1615.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, Hammarstrom L, Cunningham-Rundles C. Current genetic landscape in common variable immune deficiency. Blood. 2020;135(9):656–667.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, Aghamohammadi A, Fang M, et al. Clinical implications of systematic phenotyping and exome sequencing in patients with primary antibody deficiency. Genet Med. 2019;21(1):243–251.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, Parvaneh N, Rezaei N, et al. Genetic defects in B-cell development and their clinical consequences. J Investig Allergol Clin Immunol. 2014;24(1):6–22.
   PubMed Web of Science ®Google Scholar
• Mayer CT, Gazumyan A, Kara EE, et al. The microanatomic segregation of selection by apoptosis in the germinal center. Science. 2017;358(6360):eaao2602.
   PubMed Web of Science ®Google Scholar
• Stewart I, Radtke D, Phillips B, et al. Germinal center B cells replace their antigen receptors in dark zones and fail light zone entry when immunoglobulin gene mutations are damaging. Immunity. 2018;49(3):477–89 e7.
   PubMed Web of Science ®Google Scholar
• Willis SN, Tellier J, Liao Y, et al. Environmental sensing by mature B cells is controlled by the transcription factors PU.1 and SpiB. Nat Commun. 2017;8(1):1426.
   PubMedGoogle Scholar
• Ersching J, Efeyan A, Mesin L, et al. Germinal center selection and affinity maturation require dynamic regulation of mTORC1 kinase. Immunity. 2017;46(6):1045–58 e6.
   PubMed Web of Science ®Google Scholar
• Kometani K, Nakagawa R, Shinnakasu R, et al. Repression of the transcription factor Bach2 contributes to predisposition of IgG1 memory B cells toward plasma cell differentiation. Immunity. 2013;39(1):136–147.
   PubMed Web of Science ®Google Scholar
• Tamahara T, Ochiai K, Muto A, et al. The mTOR-Bach2 cascade controls cell cycle and class switch recombination during B cell differentiation. Mol Cell Biol. 2017;37(24):e00418–17.
   PubMed Web of Science ®Google Scholar
• Fischer SF, Bouillet P, O’Donnell K, et al. Proapoptotic BH3-only protein Bim is essential for developmentally programmed death of germinal center-derived memory B cells and antibody-forming cells. Blood. 2007;110(12):3978–3984.
   PubMed Web of Science ®Google Scholar
• Luo W, Weisel F, Shlomchik MJ. B Cell Receptor and CD40 signaling are rewired for synergistic induction of the c-Myc transcription factor in germinal center B cells. Immunity. 2018;48(2):313–26 e5.
   PubMed Web of Science ®Google Scholar
• Zhu Z, Shukla A, Ramezani-Rad P, et al. The AKT isoforms 1 and 2 drive B cell fate decisions during the germinal center response. Life Sci Alliance. 2019;2(6):e201900506.
   PubMed Web of Science ®Google Scholar
• Zhang TT, Gonzalez DG, Cote CM, et al. Germinal center B cell development has distinctly regulated stages completed by disengagement from T cell help. Elife. 2017;6:e19552.
   PubMed Web of Science ®Google Scholar
• Ise W, Fujii K, Shiroguchi K, et al. T follicular helper cell-germinal center B cell interaction strength regulates entry into plasma cell or recycling germinal center cell fate. Immunity. 2018;48(4):702–15 e4.
   PubMed Web of Science ®Google Scholar
• Saito M, Gao J, Basso K, et al. A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell. 2007;12(3):280–292.
   PubMed Web of Science ®Google Scholar
• Moens L, Tangye SG. Cytokine-mediated regulation of plasma cell generation: IL-21 takes center stage. Front Immunol. 2014;5:65.
   PubMed Web of Science ®Google Scholar
• Bryant VL, Ma CS, Avery DT, et al. Cytokine-mediated regulation of human b cell differentiation into Ig-secreting cells: predominant role of IL-21 Produced by CXCR5 + T follicular helper cells. J Immunol. 2007;179(12):8180–8190.
   PubMed Web of Science ®Google Scholar
• Parrish-Novak J, Dillon SR, Nelson A, et al. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature. 2000;408(6808):57–63.
   PubMed Web of Science ®Google Scholar
• Good KL, Bryant VL, Tangye SG. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J Immunol. 2006;177(8):5236–5247.
   PubMed Web of Science ®Google Scholar
• Avery DT, Deenick EK, Ma CS, et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J Exp Med. 2010;207(1):155–171.
   PubMed Web of Science ®Google Scholar
• Diehl SA, Schmidlin H, Nagasawa M, et al. STAT3-mediated up-regulation of BLIMP1 Is coordinated with BCL6 down-regulation to control human plasma cell differentiation. J Immunol. 2008;180(7):4805–4815.
   PubMed Web of Science ®Google Scholar
• Pene J, Gauchat JF, Lecart S, et al. Cutting edge: IL-21 is a switch factor for the production ofIgG 1 and IgG 3 by human B cells. J Immunol. 2004;172(9):5154–5157.
   PubMed Web of Science ®Google Scholar
• Avery DT, Bryant VL, Ma CS, et al. IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J Immunol. 2008;181(3):1767–1779.
   PubMed Web of Science ®Google Scholar
• Ettinger R, Sims GP, Fairhurst AM, et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol. 2005;175(12):7867–7879.
   PubMed Web of Science ®Google Scholar
• Avery DT, Ma CS, Bryant VL, et al. STAT3 is required for IL-21-induced secretion of IgE from human naive B cells. Blood. 2008;112(5):1784–1793.
   PubMed Web of Science ®Google Scholar
• Pene J, Guglielmi L, Gauchat JF, et al. IFN-γ-Mediated inhibition of human IgE synthesis by IL-21 Is associated with a polymorphism in the IL-21R Gene. J Immunol. 2006;177(8):5006–5013.
   PubMed Web of Science ®Google Scholar
• Brenne AT, Ro TB, Waage A, et al. Interleukin-21 is a growth and survival factor for human myeloma cells. Blood. 2002;99(10):3756–3762.
   PubMed Web of Science ®Google Scholar
• Kuchen S, Robbins R, Sims GP, et al. Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J Immunol. 2007;179(9):5886–5896.
   PubMed Web of Science ®Google Scholar
• Deenick EK, Avery DT, Chan A, et al. Naive and memory human B cells have distinct requirements for STAT3 activation to differentiate into antibody-secreting plasma cells. J Exp Med. 2013;210(12):2739–2753.
   PubMed Web of Science ®Google Scholar
• Recher M, Berglund LJ, Avery DT, et al. IL-21 is the primary common gamma chain-binding cytokine required for human B-cell differentiation in vivo. Blood. 2011;118(26):6824–6835.
   PubMed Web of Science ®Google Scholar
• Kotlarz D, Zietara N, Uzel G, et al. Loss-of-function mutations in the IL-21 receptor gene cause a primary immunodeficiency syndrome. J Exp Med. 2013;210(3):433–443.
   PubMed Web of Science ®Google Scholar
• Crotty S. Follicular Helper CD4 T Cells (TFH). Annu Rev Immunol. 2011;29(1):621–663.
   PubMed Web of Science ®Google Scholar
• Ma CS, Deenick EK, Batten M, et al. The origins, function, and regulation of T follicular helper cells. J Exp Med. 2012;209(7):1241–1253.
   PubMed Web of Science ®Google Scholar
• Tangye SG, Ma CS, Brink R, et al. The good, the bad and the ugly - TFH cells in human health and disease. Nat Rev Immunol. 2013;13(6):412–426.
   PubMed Web of Science ®Google Scholar
• Holland SM, DeLeo FR, Elloumi HZ, et al. STAT3 mutations in the hyper-Ige syndrome. N Engl J Med. 2007;357(16):1608–1619.
   PubMed Web of Science ®Google Scholar
• Minegishi Y, Saito M, Tsuchiya S, et al., Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature. 2007;448(7157):1058–1062.
   PubMed Web of Science ®Google Scholar
• Tavassoli M, Abolhassani H, Yazdani R, et al. The first cohort of Iranian patients with hyper immunoglobulin E syndrome: a long-term follow-up and genetic analysis. Pediatr Allergy Immunol. 2019;30(4):469–478.
   PubMed Web of Science ®Google Scholar
• Aghamohammadi A, Moghaddam ZG, Abolhassani H, et al. Investigation of underlying primary immunodeficiencies in patients with severe atopic dermatitis. Allergol Immunopathol (Madr). 2014;42(4):336–341.
   PubMed Web of Science ®Google Scholar
• Berglund LJ, Avery DT, Ma CS, et al. IL-21 signalling via STAT3 primes human naive B cells to respond to IL-2 to enhance their differentiation into plasmablasts. Blood. 2013;122(24):3940–3950.
   PubMed Web of Science ®Google Scholar
• Tangye SG, Al-Herz W, Bousfiha A, et al. Human inborn errors of immunity: 2019 update on the classification from the International Union of Immunological Societies Expert Committee. J Clin Immunol. 2020;40(1):24–64.
   PubMed Web of Science ®Google Scholar
• Rousset F, Garcia E, Defrance T, et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A. 1992;89(5):1890–1893.
   PubMed Web of Science ®Google Scholar
• Briere F, Servet-Delprat C, Bridon JM, et al. Human interleukin 10 induces naive surface immunoglobulin D+ (sIgD+) B cells to secrete IgG1 and IgG3. J Exp Med. 1994;179(2):757–762.
   PubMed Web of Science ®Google Scholar
• Arpin C, Dechanet J, Van Kooten C, et al. Generation of memory B cells and plasma cells in vitro. Science. 1995;268(5211):720–722.
   PubMed Web of Science ®Google Scholar
• Defrance T, Vanbervliet B, Briere F, et al. Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med. 1992;175(3):671–682.
   PubMed Web of Science ®Google Scholar
• Dubois B, Massacrier C, Vanbervliet B, et al. Critical role of IL-12 in dendritic cell-induced differentiation of naive B lymphocytes. J Immunol. 1998;161(5):2223–2231.
   PubMed Web of Science ®Google Scholar
• Gauchat JF, Aversa G, Gascan H, et al. Modulation of IL-4 induced germline epsilon RNA synthesis in human B cells by tumor necrosis factor-alpha, anti-CD40 monoclonal antibodies or transforming growth factor-beta correlates with levels of IgE production. Int Immunol. 1992;4(3):397–406.
   PubMed Web of Science ®Google Scholar
• Itoh K, Hirohata S. The role of IL-10 in human B cell activation, proliferation, and differentiation. J Immunol. 1995;154(9):4341–4350.
   PubMed Web of Science ®Google Scholar
• Ruprecht CR, Lanzavecchia A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur J Immunol. 2006;36(4):810–816.
   PubMed Web of Science ®Google Scholar
• He B, Qiao X, Cerutti A. CpG DNA induces IgG class switch DNA recombination by activating human B cells through an innate pathway that requires TLR9 and cooperates with IL-10. J Immunol. 2004;173(7):4479–4491.
   PubMed Web of Science ®Google Scholar
• Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007;87(3):905–931.
   PubMed Web of Science ®Google Scholar
• Pauklin S, Sernandez IV, Bachmann G, et al. Estrogen directly activates AID transcription and function. J Exp Med. 2009;206(1):99–111.
   PubMed Web of Science ®Google Scholar
• Mai T, Zan H, Zhang J, et al. 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(48):37797–37810.
   PubMed Web of Science ®Google Scholar
• Park SR, Zan H, Pal Z, et al. 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(5):540–550.
   PubMed Web of Science ®Google Scholar
• White CA, Seth Hawkins J, Pone EJ, et al. AID dysregulation in lupus-prone MRL/ Faslpr/ lpr mice increases class switch DNA recombination and promotes interchromosomal c-Myc/IgH loci translocations: modulation by HoxC4. Autoimmunity. 2011;44(8):585–598.
   PubMed Web of Science ®Google Scholar
• Perez-Duran P, de Yebenes VG, Ramiro AR. Oncogenic events triggered by AID, the adverse effect of antibody diversification. Carcinogenesis. 2007;28(12):2427–2433.
   PubMed Web of Science ®Google Scholar
• Casellas R, Basu U, Yewdell WT, et al., Mutations, kataegis and translocations in B cells: understanding AID promiscuous activity. Nat Rev Immunol. 2016;16(3):164–176.
   PubMed Web of Science ®Google Scholar
• Robbiani DF, Nussenzweig MC. Chromosome translocation, B cell lymphoma, and activation-induced cytidine deaminase. Annu Rev Pathol. 2013;8(1):79–103.
   PubMedGoogle Scholar
• Sayegh CE, Quong MW, Agata Y, et al. E-proteins directly regulate expression of activation-induced deaminase in mature B cells. Nat Immunol. 2003;4(6):586–593.
   PubMed Web of Science ®Google Scholar
• Ise W, Kohyama M, Schraml BU, et al. The transcription factor BATF controls the global regulators of class-switch recombination in both B cells and T cells. Nat Immunol. 2011;12(6):536–543.
   PubMed Web of Science ®Google Scholar
• Inoue T, Shinnakasu R, Ise W, et al. The transcription factor Foxo1 controls germinal center B cell proliferation in response to T cell help. J Exp Med. 2017;214(4):1181–1198.
   PubMed Web of Science ®Google Scholar
• Sun L, Zhao X, Liu X, et al. Transcription factor Ascl2 promotes germinal center B cell responses by directly regulating AID transcription. Cell Rep. 2021;35(9):109188.
   PubMed Web of Science ®Google Scholar
• Daniel JA, Santos MA, Wang Z, et al. PTIP promotes chromatin changes critical for immunoglobulin class switch recombination. Science. 2010;329(5994):917–923.
   PubMed Web of Science ®Google Scholar
• Pavri R, Gazumyan A, Jankovic M, et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell. 2010;143(1):122–133.
   PubMed Web of Science ®Google Scholar
• Wang L, Wuerffel R, Feldman S, et al. S region sequence, RNA polymerase II, and histone modifications create chromatin accessibility during class switch recombination. J Exp Med. 2009;206(8):1817–1830.
   PubMed Web of Science ®Google Scholar
• Yamane A, Resch W, Kuo N, et al. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat Immunol. 2011;12(1):62–69.
   PubMed Web of Science ®Google Scholar
• Wang L, Whang N, Wuerffel R, et al. AID-dependent histone acetylation is detected in immunoglobulin S regions. J Exp Med. 2006;203(1):215–226.
   PubMed Web of Science ®Google Scholar
• Chowdhury M, Forouhi O, Dayal S, et al. Analysis of intergenic transcription and histone modification across the human immunoglobulin heavy-chain locus. Proc Natl Acad Sci U S A. 2008;105(41):15872–15877.
   PubMed Web of Science ®Google Scholar
• Kuang FL, Luo Z, Scharff MD. H3 trimethyl K9 and H3 acetyl K9 chromatin modifications are associated with class switch recombination. Proc Natl Acad Sci U S A. 2009;106(13):5288–5293.
   PubMed Web of Science ®Google Scholar
• Stanlie A, Aida M, Muramatsu M, et al. Histone3 lysine4 trimethylation regulated by the facilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination. Proc Natl Acad Sci U S A. 2010;107(51):22190–22195.
   PubMed Web of Science ®Google Scholar
• Jeevan-Raj BP, Robert I, Heyer V, et al. Epigenetic tethering of AID to the donor switch region during immunoglobulin class switch recombination. J Exp Med. 2011;208(8):1649–1660.
   PubMed Web of Science ®Google Scholar
• Bradley SP, Kaminski DA, Peters AH, et al. The histone methyltransferase Suv39h1 increases class switch recombination specifically to IgA. J Immunol. 2006;177(2):1179–1188.
   PubMed Web of Science ®Google Scholar
• Crouch EE, Li Z, Takizawa M, et al. Regulation of AID expression in the immune response. J Exp Med. 2007;204(5):1145–1156.
   PubMed Web of Science ®Google Scholar
• Begum NA, Stanlie A, Nakata M, et al. The histone chaperone Spt6 is required for activation-induced cytidine deaminase target determination through H3K4me3 regulation. J Biol Chem. 2012;287(39):32415–32429.
   PubMed Web of Science ®Google Scholar
• Li G, White CA, Lam T, et al. Combinatorial H3K9acS10ph histone modification in IgH locus S regions targets 14-3-3 adaptors and AID to specify antibody class-switch DNA recombination. Cell Rep. 2013;5(3):702–714.
   PubMed Web of Science ®Google Scholar
• Xu Z, Fulop Z, Wu G, et al., 14-3-3 adaptor proteins recruit AID to 5’-AGCT-3’-rich switch regions for class switch recombination. Nat Struct Mol Biol. 2010;17(9):1124–1135.
   PubMed Web of Science ®Google Scholar
• Zan H, White CA, Thomas LM, et al. Rev1 recruits ung to switch regions and enhances du glycosylation for immunoglobulin class switch DNA recombination. Cell Rep. 2012;2(5):1220–1232.
   PubMed Web of Science ®Google Scholar
• Pei H, Wu X, Liu T, et al. The histone methyltransferase MMSET regulates class switch recombination. J Immunol. 2013;190(2):756–763.
   PubMed Web of Science ®Google Scholar
• Lio CJ, Shukla V, Samaniego-Castruita D, et al. TET enzymes augment activation-induced deaminase (AID) expression via 5-hydroxymethylcytosine modifications at the Aicda superenhancer. Sci Immunol. 2019;4(34):eaau7523.
   PubMed Web of Science ®Google Scholar
• Rosikiewicz W, Chen X, Dominguez PM, et al. TET2 deficiency reprograms the germinal center B cell epigenome and silences genes linked to lymphomagenesis. Sci Adv. 2020;6(25):eaay5872.
   PubMed Web of Science ®Google Scholar
• Dhordain P, Lin RJ, Quief S, et al. The LAZ3(BCL-6) oncoprotein recruits a SMRT/mSIN3A/histone deacetylase containing complex to mediate transcriptional repression. Nucleic Acids Res. 1998;26(20):4645–4651.
   PubMed Web of Science ®Google Scholar
• Lemercier C, Brocard MP, Puvion-Dutilleul F, et al. Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor. J Biol Chem. 2002;277(24):22045–22052.
   PubMed Web of Science ®Google Scholar
• de Yebenes VG, Belver L, Pisano DG, et al. miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J Exp Med. 2008;205(10):2199–2206.
   PubMed Web of Science ®Google Scholar
• Borchert GM, Holton NW, Larson ED. Repression of human activation induced cytidine deaminase by miR-93 and miR-155. BMC Cancer. 2011;11(1):347.
   PubMedGoogle Scholar
• Basso K, Schneider C, Shen Q, et al. BCL6 positively regulates AID and germinal center gene expression via repression of miR-155. J Exp Med. 2012;209(13):2455–2465.
   PubMed Web of Science ®Google Scholar
• Kluiver J, van den Berg A, de Jong D, et al. Regulation of pri-microRNA BIC transcription and processing in Burkitt lymphoma. Oncogene. 2007;26(26):3769–3776.
   PubMed Web of Science ®Google Scholar
• Zaprazna K, Atchison ML. YY1 controls immunoglobulin class switch recombination and nuclear activation-induced deaminase levels. Mol Cell Biol. 2012;32(8):1542–1554.
   PubMed Web of Science ®Google Scholar
• Kuhny M, Forbes LR, Cakan E, et al. Disease-associated CTNNBL1 mutation impairs somatic hypermutation by decreasing nuclear AID. J Clin Invest. 2020;130(8):4411–4422.
   PubMed Web of Science ®Google Scholar
• Heltemes-Harris LM, Gearhart PJ, Ghosh P, et al. Activation-induced deaminase-mediated class switch recombination is blocked by anti-IgM signaling in a phosphatidylinositol 3-kinase-dependent fashion. Mol Immunol. 2008;45(6):1799–1806.
   PubMed Web of Science ®Google Scholar
• Pone EJ, Zhang J, Mai T, et al. BCR-signalling synergizes with TLR-signalling for induction of AID and immunoglobulin class-switching through the non-canonical NF-kappaB pathway. Nat Commun. 2012;3(1):767.
   PubMedGoogle Scholar
• Chen Z, Krinsky A, Woolaver RA, et al. TRAF3 acts as a checkpoint of B cell receptor signaling to control antibody class switch recombination and anergy. J Immunol. 2020;205(3):830–841.
   PubMed Web of Science ®Google Scholar
• Azizi G, Bagheri Y, Tavakol M, et al. The clinical and immunological features of patients with primary antibody deficiencies. Endocr Metab Immune Disord Drug Targets. 2018;18(5):537–545.
   PubMed Web of Science ®Google Scholar
• Bazregari S, Azizi G, Tavakol M, et al. Evaluation of infectious and non-infectious complications in patients with primary immunodeficiency. Cent Eur J Immunol. 2017;42(4):336–341.
   PubMed Web of Science ®Google Scholar
• Aghamohammadi A, Abolhassani H, Latif A, et al. Long-term evaluation of a historical cohort of Iranian common variable immunodeficiency patients. Expert Rev Clin Immunol. 2014;10(10):1405–1417.
   PubMed Web of Science ®Google Scholar
• Rizvi FS, Zainaldain H, Rafiemanesh H, et al. Autoimmunity in common variable immunodeficiency: a systematic review and meta-analysis. Expert Rev Clin Immunol. 2020;16(12):1227–1235.
   PubMed Web of Science ®Google Scholar
• Asgardoon MH, Azizi G, Yazdani R, et al. Monogenic primary immunodeficiency disorder associated with common variable immunodeficiency and autoimmunity. Int Arch Allergy Immunol. 2020;181(9):706–714.
   PubMed Web of Science ®Google Scholar
• Cunningham-Rundles C. Autoimmunity in primary immune deficiency: taking lessons from our patients. Clin Exp Immunol. 2011;164(Suppl 2):6–11.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, Amirkashani D, Parvaneh N, et al. Autoimmune phenotype in patients with common variable immunodeficiency. J Investig Allergol Clin Immunol. 2013;23(5):323–329.
   PubMed Web of Science ®Google Scholar
• Azizi G, Kiaee F, Hedayat E, et al. Rheumatologic complications in a cohort of 227 patients with common variable immunodeficiency. Scand J Immunol. 2018;87(5):e12663.
   PubMed Web of Science ®Google Scholar
• Azizi G, Abolhassani H, Kiaee F, et al. Autoimmunity and its association with regulatory T cells and B cell subsets in patients with common variable immunodeficiency. Allergol Immunopathol (Madr). 2018;46(2):127–135.
   PubMed Web of Science ®Google Scholar
• Yu L, Robles DT, Abiru N, et al. Early expression of antiinsulin autoantibodies of humans and the NOD mouse: evidence for early determination of subsequent diabetes. Proc Natl Acad Sci U S A. 2000;97(4):1701–1706.
   PubMed Web of Science ®Google Scholar
• Guo W, Smith D, Aviszus K, et al. Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity. J Exp Med. 2010;207(10):2225–2237.
   PubMed Web of Science ®Google Scholar
• Azizi G, Ahmadi M, Abolhassani H, et al. Autoimmunity in primary antibody deficiencies. Int Arch Allergy Immunol. 2016;171(3–4):180–193.
   PubMed Web of Science ®Google Scholar
• Fairweather D, Kaya Z, Shellam GR, et al. From infection to autoimmunity. J Autoimmun. 2001;16(3):175–186.
   PubMed Web of Science ®Google Scholar
• Azizi G, Abolhassani H, Asgardoon MH, et al. Autoimmunity in common variable immunodeficiency: epidemiology, pathophysiology and management. Expert Rev Clin Immunol. 2017;13(2):101–115.
   PubMed Web of Science ®Google Scholar
• Gupta S, Demirdag Y, Gupta AA. Members of the regulatory lymphocyte club in common variable immunodeficiency. Front Immunol. 2022;13:864307.
   PubMed Web of Science ®Google Scholar
• Abolhassani H. Specific immune response and cytokine production in CD70 deficiency. Front Pediatr. 2021;9:615724.
   PubMed Web of Science ®Google Scholar
• Ghosh S, Kostel Bal S, Edwards ESJ, et al. Extended clinical and immunological phenotype and transplant outcome in CD27 and CD70 deficiency. Blood. 2020;136(23):2638–2655.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, Edwards ES, Ikinciogullari A, et al. Combined immunodeficiency and Epstein-Barr virus-induced B cell malignancy in humans with inherited CD70 deficiency. J Exp Med. 2017;214(1):91–106.
   PubMed Web of Science ®Google Scholar
• Alkhairy OK, Perez-Becker R, Driessen GJ, et al. Novel mutations in TNFRSF7/CD27: clinical, immunologic, and genetic characterization of human CD27 deficiency. J Allergy Clin Immunol. 2015;136(3):703–12 e10.
   PubMed Web of Science ®Google Scholar
• Dimitrova D, Nademi Z, Maccari ME, et al. International retrospective study of allogeneic hematopoietic cell transplantation for activated PI3K-delta syndrome. J Allergy Clin Immunol. 2022;149(1):410–21 e7.
   PubMed Web of Science ®Google Scholar
• Jamee M, Moniri S, Zaki-Dizaji M, et al. Clinical, immunological, and genetic features in patients with activated PI3Kdelta syndrome (APDS): a systematic review. Clin Rev Allergy Immunol. 2020;59(3):323–333.
   PubMed Web of Science ®Google Scholar
• Maccari ME, Abolhassani H, Aghamohammadi A, et al. Disease evolution and response to rapamycin in activated phosphoinositide 3-kinase delta syndrome: the European Society for Immunodeficiencies-activated Phosphoinositide 3-kinase Delta Syndrome Registry. Front Immunol. 2018;9:543.
   PubMed Web of Science ®Google Scholar
• Ye X, Maglione PJ, Wehr C, et al. Genomic characterization of lymphomas in patients with inborn errors of immunity. Blood Adv. 2022. DOI:10.1182/bloodadvances.2021006654.
   Google Scholar
• Abolhassani H, Wang Y, Hammarstrom L, et al. Hallmarks of cancers: primary antibody deficiency versus other inborn errors of immunity. Front Immunol. 2021;12:720025.
   PubMed Web of Science ®Google Scholar
• Kiaee F, Azizi G, Rafiemanesh H, et al. Malignancy in common variable immunodeficiency: a systematic review and meta-analysis. Expert Rev Clin Immunol. 2019;15(10):1105–1113.
   PubMed Web of Science ®Google Scholar
• Tak Manesh A, Azizi G, Heydari A, et al. Epidemiology and pathophysiology of malignancy in common variable immunodeficiency? Allergol Immunopathol (Madr). 2017;45(6):602–615.
   PubMed Web of Science ®Google Scholar
• Kiaee F, Zaki-Dizaji M, Hafezi N, et al. Clinical, immunologic and molecular spectrum of patients with immunodeficiency, centromeric Instability, and Facial Anomalies (ICF) syndrome: a systematic review. Endocr Metab Immune Disord Drug Targets. 2021;21(4):664–672.
   PubMed Web of Science ®Google Scholar
• Dehkordy SF, Aghamohammadi A, Ochs HD, et al. Primary immunodeficiency diseases associated with neurologic manifestations. J Clin Immunol. 2012;32(1):1–24.
   PubMed Web of Science ®Google Scholar
• Chavoshzadeh Z, Hashemitari A, Darougar S. Neurological manifestations of primary immunodeficiencies. Iran J Child Neurol. 2018;12(3):7–23.
   PubMed Web of Science ®Google Scholar
• Yildirim M, Ayvaz DC, Konuskan B, et al. Neurologic involvement in primary immunodeficiency disorders. J Child Neurol. 2018;33(5):320–328.
   PubMed Web of Science ®Google Scholar
• Abolhassani H, El-Sherbiny YM, Arumugakani G, et al. Expanding clinical phenotype and novel insights into the pathogenesis of ICOS deficiency. J Clin Immunol. 2020;40(2):277–288.
   PubMed Web of Science ®Google Scholar
• Alkhairy OK, Abolhassani H, Rezaei N, et al. Spectrum of phenotypes associated with mutations in LRBA. J Clin Immunol. 2016;36(1):33–45.
   PubMed Web of Science ®Google Scholar
• Tesch VK, Abolhassani H, Shadur B, et al. Long-term outcome of LRBA deficiency in 76 patients after various treatment modalities as evaluated by the immune deficiency and dysregulation activity (IDDA) score. J Allergy Clin Immunol. 2020;145(5):1452–1463.
   PubMed Web of Science ®Google Scholar
• Lorenzini T, Fliegauf M, Klammer N, et al. Characterization of the clinical and immunologic phenotype and management of 157 individuals with 56 distinct heterozygous NFKB1 mutations. J Allergy Clin Immunol. 2020;146(4):901–911.
   PubMed Web of Science ®Google Scholar
• Tsilifis C, Freeman AF, Gennery AR. STAT3 Hyper-IgE syndrome-an update and unanswered questions. J Clin Immunol. 2021;41(5):864–880.
   PubMed Web of Science ®Google Scholar
• Andersen IM, Jorgensen SF. Gut inflammation in CVID: causes and consequences. Expert Rev Clin Immunol. 2022;18(1):31–45.
   PubMed Web of Science ®Google Scholar
• Yazdani R, Azizi G, Abolhassani H, et al. Selective IgA deficiency: epidemiology, pathogenesis, clinical phenotype, diagnosis, prognosis and management. Scand J Immunol. 2017;85(1):3–12.
   PubMed Web of Science ®Google Scholar
• Al-Nesf MA, Morgan D, Mohamed-Ali V. Primary immunodeficiency and the microbiome. Curr Opin Pediatr. 2021;33(6):633–638.
   PubMed Web of Science ®Google Scholar
• Tangye SG, Al-Herz W, Bousfiha A, et al. The ever-increasing array of novel inborn errors of immunity: an interim update by the IUIS committee. J Clin Immunol. 2021;41(3):666–679.
   PubMed Web of Science ®Google Scholar