DOI QR코드

DOI QR Code

Immune modulation and possible pathological implications mediated by naturally produced immunoglobulin G idiotypes: from historical to recent experimental and clinical studies focused on atopic dermatitis

  • Lucas Santander (Medical School, Santo Amaro University) ;
  • Nicolle Rakanidis Machado (Laboratory of Medical Investigation LIM-56, Division of Dermatology, University of Sao Paulo, Medical School) ;
  • Beatriz Oliveira Fagundes (Laboratory of Medical Investigation LIM-56, Division of Dermatology, University of Sao Paulo, Medical School) ;
  • Jefferson Russo Victor (Laboratory of Medical Investigation LIM-56, Division of Dermatology, University of Sao Paulo, Medical School)
  • 투고 : 2023.06.17
  • 심사 : 2023.10.17
  • 발행 : 2024.01.31

초록

Since the 1950s decade, it has been suggested that a naturally produced or induced repertoire of immunoglobulin G (IgG) idiotypes may exert some immunoregulatory functions. In the last decades, some more advanced theories have suggested that the repertoire of IgG idiotypes may influence the development or control of some atopic diseases. In atopic dermatitis (AD), some evidence indicated that the IgG repertoire obtained from these patients could effectively mediate regulatory functions on thymic and peripheral CD4+ and CD8+ T cells. Furthermore, some recent clinical trials have corroborated the hypothesis that IgG from AD patients can exert regulatory functions in vivo. Here, we revised some historical aspects that yield current approaches developed in vitro and in vivo to elucidate a recently proposed theory termed "hooks without bait" that can strengthen the broad spectrum of research about evaluating different sets of IgG idiotypes and determine their immunological effects.

키워드

참고문헌

  1. Jerne NK. The natural-selection theory of antibody formation. Proc Natl Acad Sci USA 1955;41:849-57.
  2. Jerne NK. Towards a network theory of the immune system. Ann Immunol (Paris) 1974;125C:373-89.
  3. Jerne NK. Idiotypic networks and other preconceived ideas. Immunol Rev 1984;79:5-24.
  4. Jerne NK. The generative grammar of the immune system. EMBO J 1985;4:847-52.
  5. Binz H, Wigzell H. Shared idiotypic determinants on B and T lymphocytes reactive against the same antigenic determinants. I. Demonstration of similar or identical idiotypes on IgG molecules and T-cell receptors with specificity for the same alloantigens. J Exp Med 1975;142:197-211.
  6. Binz H, Wigzell H, Bazin H. T-cell idiotypes are linked to immunoglobulin heavy chain genes. Nature 1976;264:639-42.
  7. Martinez C, Bragado R, de la Hera A, et al. Functional and biochemical evidence for the recognition of T cell receptors by monoclonal antibodies to an immunoglobulin idiotype. J Mol Cell Immunol 1986;2:307-13.
  8. Eichmann K, Rajewsky K. Induction of T and B cell immunity by anti-idiotypic antibody. Eur J Immunol 1975;5:661-6.
  9. Vakil M, Sauter H, Paige C, Kearney JF. In vivo suppression of perinatal multispecific B cells results in a distortion of the adult B cell repertoire. Eur J Immunol 1986;16:1159-65.
  10. Marchalonis JJ, Kaymaz H, Schluter SF, Yocum DE. Naturally occurring human autoantibodies to defined T-cell receptor and light chain peptides. Adv Exp Med Biol 1994;347:135-45.
  11. Borghesi C, Nicoletti C. Autologous anti-idiotypic antibody response is regulated by the level of circulating complementary idiotype. Immunology 1996;89:172-7.
  12. Schluter SF, Adelman MK, Taneja V, David C, Yocum DE, Marchalonis JJ. Natural autoantibodies to TCR public idiotopes: potential roles in immunomodulation. Cell Mol Biol (Noisy-le-grand) 2003;49:193-207.
  13. Adelman MK, Schluter SF, Robey IF, Marchalonis JJ. Natural and autoantibodies to human T-cell receptor Vbeta segments: potential roles in immunomodulation. Crit Rev Immunol 2007;27:221-32.
  14. Proulx DP, Aubin E, Lemieux R, Bazin R. Spontaneous internalization of IVIg in activated B cells. Immunol Lett 2009;124:18-26.
  15. Paquin Proulx D, Aubin E, Lemieux R, Bazin R. Inhibition of B cell-mediated antigen presentation by intravenous immunoglobulins (IVIg). Clin Immunol 2010;135:422-9.
  16. Jacobsen JT, Sundvold-Gjerstad V, Skjeldal FM, et al. B-cell tolerance to the B-cell receptor variable regions. Eur J Immunol 2013;43:2577-87.
  17. Jacobsen J, Haabeth OA, Tveita AA, Schjetne KW, Munthe LA, Bogen B. Naive idiotope-specific B and T cells collaborate efficiently in the absence of dendritic cells. J Immunol 2014;192:4174-83.
  18. Seite JF, Goutsmedt C, Youinou P, Pers JO, Hillion S. Intravenous immunoglobulin induces a functional silencing program similar to anergy in human B cells. J Allergy Clin Immunol 2014;133:181-8.
  19. Victor JR. Do different IgG repertoires play a role in B- and T-cell functional modulation during ontogeny?: the "hooks without bait" theory. Immunol Cell Biol 2020;98:540-8.
  20. Nomura T, Kabashima K. Advances in atopic dermatitis in 2019-2020: endotypes from skin barrier, ethnicity, properties of antigen, cytokine profiles, microbiome, and engagement of immune cells. J Allergy Clin Immunol 2021;148:1451-62.
  21. Thijs JL, Strickland I, Bruijnzeel-Koomen CA, et al. Moving toward endotypes in atopic dermatitis: identification of patient clusters based on serum biomarker analysis. J Allergy Clin Immunol 2017;140:730-7.
  22. Bakker DS, Nierkens S, Knol EF, et al. Confirmation of multiple endotypes in atopic dermatitis based on serum biomarkers. J Allergy Clin Immunol 2021;147:189-98.
  23. Victor JR, Muniz BP, Fusaro AE, et al. Maternal immunization with ovalbumin prevents neonatal allergy development and up-regulates inhibitory receptor Fc gamma RIIB expression on B cells. BMC Immunol 2010;11:11.
  24. Gorczynski RM, Maqbool T, Hoffmann G. Mechanism(s) of prolonged attenuation of allergic responses after modulation of idiotypic regulatory network. Allergy Asthma Clin Immunol 2019;15:79.
  25. Tawfik DS, Cowan KR, Walsh AM, Hamilton WS, Goldman FD. Exogenous immunoglobulin downregulates T-cell receptor signaling and cytokine production. Pediatr Allergy Immunol 2012;23:88-95.
  26. Sgnotto FD, de Oliveira MG, Lira AA, et al. IgG from atopic dermatitis patients induces IL-17 and IL-10 production in infant intrathymic TCD4 and TCD8 cells. Int J Dermatol 2018;57:434-40.
  27. Santos LS, Sgnotto FD, Sousa TR, et al. IgG from atopic dermatitis patients induces non-atopic infant thymic invariant natural killer T (iNKT) cells to produce IL-4, IL-17, and IL-10. Int J Dermatol 2020;59:359-64.
  28. de Sousa TR, Fagundes BO, Nascimento A, et al. IgG from adult atopic dermatitis (AD) patients induces thymic IL-22 production and CLA expression on CD4+ T cells: possible epigenetic implications mediated by miRNA. Int J Mol Sci 2022;23:6867.
  29. Czarnowicki T, Santamaria-Babi LF, Guttman-Yassky E. Circulating CLA+ T cells in atopic dermatitis and their possible role as peripheral biomarkers. Allergy 2017;72:366-72.
  30. Rodrigues de Sousa T, da Ressureicao Sgnotto F, Oliveira Fagundes B, Souza Santos L, da Silva Duarte AJ, Victor JR. IgG from atopic individuals can mediate non-atopic infant thymic and adult peripheral CD8+ TC2 skewing without influence on TC17 or TC22 cells. Eur Ann Allergy Clin Immunol 2021;53:161-7.
  31. Sali AD, Karakasiliotis I, Evangelidou M, Avrameas S, Lymberi P. Immunological evidence and regulatory potential for cell-penetrating antibodies in intravenous immunoglobulin. Clin Transl Immunology 2015;4:e42.
  32. Fagundes BO, de Sousa TR, Nascimento A, et al. IgG from adult atopic dermatitis (AD) patients induces nonatopic neonatal thymic gamma-delta T cells (γδT) to acquire IL-22/IL-17 secretion profile with skin-homing properties and epigenetic implications mediated by miRNA. Int J Mol Sci 2022;23:6872.
  33. Sgnotto FD, Oliveira MG, Lira AA, Bento-de-Souza L, Duarte AJ, Victor JR. Low doses of IgG from atopic individuals can modulate in vitro IFN-γ production by human intrathymic TCD4 and TCD8 cells: an IVIg comparative approach. Hum Vaccin Immunother 2017;13:1563-72.
  34. de-Oliveira MG, Lira AA, Sgnotto FR, et al. Maternal IgG impairs the maturation of offspring intrathymic IL-17-producing γδT cells: implications for murine and human allergies. Clin Exp Allergy 2019;49:1000-12.
  35. Santos LS, Sgnotto FD, Inoue AH, et al. IgG from non-atopic individuals induces in vitro IFN-γ and IL-10 production by human intra-thymic γδT cells: a comparison with atopic IgG and IVIg. Arch Immunol Ther Exp (Warsz) 2019;67:263-70.
  36. da Ressureicao Sgnotto F, Souza Santos L, Rodrigues de Sousa T, et al. IgG from HIV-1-exposed seronegative and HIV-1-infected subjects differently modulates IFN-γ production by thymic T and B cells. J Acquir Immune Defic Syndr 2019;82:e56-60.
  37. Kimata H. High dose gammaglobulin treatment for atopic dermatitis. Arch Dis Child 1994;70:335-6.
  38. Jolles S, Hughes J, Rustin M. The treatment of atopic dermatitis with adjunctive high-dose intravenous immunoglobulin: a report of three patients and review of the literature. Br J Dermatol 2000;142:551-4.
  39. Bemanian MH, Movahedi M, Farhoudi A, et al. High doses intravenous immunoglobulin versus oral cyclosporine in the treatment of severe atopic dermatitis. Iran J Allergy Asthma Immunol 2005;4:139-43.
  40. Nahm DH, Ahn A, Kim ME, Cho SM, Park MJ. Autologous immunoglobulin therapy in patients with severe recalcitrant atopic dermatitis: long-term changes of clinical severity and laboratory parameters. Allergy Asthma Immunol Res 2016;8:375-82.
  41. Cho SM, Kim ME, Kwon B, Nahm DH. Immunomodulatory effects induced by intramuscular administration of autologous total immunoglobulin G in patients with atopic dermatitis. Int Immunopharmacol 2017;52:1-6.
  42. Nahm DH, Ye YM, Shin YS, et al. Efficacy, safety, and immunomodulatory effect of the intramuscular administration of autologous total immunoglobulin G for atopic dermatitis: a randomized clinical trial. Allergy Asthma Immunol Res 2020;12:949-63.
  43. Kwon B, Yang SJ, Cho SM, Kim ME, Nahm DH. Intramuscular administration of autologous total immunoglobulin G induces immunomodulatory effects on T cells in healthy human subjects: an open-labeled prospective single-arm trial. Medicine (Baltimore) 2022;101:e29486.
  44. Nawata Y, Koike T, Hosokawa H, Tomioka H, Yoshida S. Anti-IgE autoantibody in patients with atopic dermatitis. J Immunol 1985;135:478-82.
  45. Marone G, Casolaro V, Paganelli R, Quinti I. IgG anti-IgE from atopic dermatitis induces mediator release from basophils and mast cells. J Invest Dermatol 1989;93:246-52.
  46. Poto R, Patella V, Criscuolo G, Marone G, Coscioni E, Varricchi G. Autoantibodies to IgE can induce the release of proinflammatory and vasoactive mediators from human cardiac mast cells. Clin Exp Med 2023;23:1265-76.
  47. Poto R, Quinti I, Marone G, et al. IgG autoantibodies against IgE from atopic dermatitis can induce the release of cytokines and proinflammatory mediators from basophils and mast cells. Front Immunol 2022;13:880412.
  48. Mikus M, Johansson C, Acevedo N, Nilsson P, Scheynius A. The antimicrobial protein S100A12 identified as a potential autoantigen in a subgroup of atopic dermatitis patients. Clin Transl Allergy 2019;9:6.
  49. Luo L, Luo Y, Xu J, et al. Heterogeneous origin of IgE in atopic dermatitis and psoriasis revealed by B cell receptor repertoire analysis. Allergy 2022;77:559-68.
  50. Holmes J, Fairclough LC, Todd I. Correction to: atopic dermatitis and autoimmunity: the occurrence of autoantibodies and their association with disease severity. Arch Dermatol Res 2020;312:393.
  51. Chen K, Magri G, Grasset EK, Cerutti A. Rethinking mucosal antibody responses: IgM, IgG and IgD join IgA. Nat Rev Immunol 2020;20:427-41.
  52. Totte JE, Pardo LM, Fieten KB, et al. IgG response against staphylococcus aureus is associated with severe atopic dermatitis in children. Br J Dermatol 2018;179:118-26.