Immunopathological events initiated and maintained by pathogenic IgG autoantibodies in an experimental autoimmune kidney disease

Autoimmunity

Volumn 45, Issue 7, 2012, Pages 495-509

  Barabas, Arpad Zsigmond ^a   Cole, Chad Douglas ^b   Lafreniere, Rene ^a   Weir, Donald MacKay ^c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Autoimmune disease; Membranous glomerulonephritis; Modified vaccination technique; Non pathogenic autoantibody; Pathogenic autoantibody

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; IMMUNOSUPPRESSIVE AGENT; NEPHRITOGENIC ANTIGEN;

ANTIGEN ANTIBODY COMPLEX; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BRUSH BORDER; ELECTRON MICROSCOPY; GLOMERULONEPHRITIS; GLOMERULUS BASEMENT MEMBRANE; HEYMANN NEPHRITIS; HUMAN; IMMUNOPATHOLOGY; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY DISEASE; NONHUMAN; PATHOGENESIS; PROTEINURIA; REVIEW; SLOWLY PROGRESSIVE HEYMANN NEPHRITIS; VACCINATION;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; GLOMERULONEPHRITIS, MEMBRANOUS; HUMANS; IMMUNOGLOBULIN G; IMMUNOTHERAPY, ACTIVE; KIDNEY DISEASES;

EID: 84867069310     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2012.702812     Document Type: Review

References (118)

1. Agmon-Levin N, Paz Z, Israeli E, Shoenfeld Y. Vaccines and autoimmunity. Nat Rev Rheumatol 2009;5:648-652.
2. Alballa S, Fritzler M, Davis P. A case of drug induced lupus due to carbamazepine. J Rheumatol 1987;14:599-600.
3. Barabas AZ, ColeCD, Barabas AD, Lafreniere R. Production of Heymann nephritis by a chemically modified renal antigen. Int J Exp Pathol 2004;85:277-285.
4. Bielekova B, Goodwin B, Richert N, Cortese I, Kondo T, Afshar G, Gran B, Eaton J, Antel J, Frank JA, McFarland HF, Martin R. Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand. Nat Med 2000;6:1167-1175.
5. Biesecker G, Noble B, Andres GA, Koffler D. Immunopathogenesis of Heymann's nephritis. Clin Immunol Immunopathol 1984;33:333-338.
6. Heymann W, Hackel DB, Harwood S, Wilson SG, Hunter JLP. Production of nephritic syndrome in rats by Freund's adjuvant and rat kidney suspensions. Proc Soc Exp Biol Med 1959;100:660-664.
7. Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y. Adjuvants and autoimmunity. Lupus 2009;18:1217-1225.
8. Kivity S, Agmon-Levin N, Blank M, Shoenfeld Y. Infections and autoimmunity-friends or foes? Trends Immunol 2009; 30:409-414.
9. Molina V, Shoenfeld Y. Infection, vaccines and other environmental triggers of autoimmunity. Autoimmunity 2005;38:235-245.
10. Naito T, Kawamura T, Bannai M, Kosaka T, Kameyama H, Shimamura K, Hoshi O, Ushiki T, Hatakeyama K, Abo T. Simultaneous activation of natural killer T cells and autoantibody production in mice injected with denatured syngeneic liver tissue. Clin Exp Immunol 2002;129: 397-404.
11. Weir DM, Pinckard RN. Failure to induce tolerance to rat tissue antigens. Immunology 1967;13:373-380.
12. Weir DM, Elson CJ. Antitissue antibodies and immunological tolerance to self. Arthritis Rheum 1969;12:254-260.
13. Rich MW. Drug-induced lupus. The list of culprits grows. Postgrad Med 1996;100, 299-8.
14. Chen M, von Mikecz A. Proteasomal processing of nuclear autoantigens in systemic autoimmunity. Autoimmun Rev 2005;4:117-122.
15. Lleo A, Battezzati PM, Selmi C, Gershwin ME, Podda M. Is autoimmunity a matter of sex? Autoimmun Rev 2008;7: 626-630.
16. Orbach H, Shoenfeld Y. Vaccination infection and autoimmunity: myth and reality VIAMR 2005-10-26-28, Beau-Rivage Palace Hotel, Lausanne, Switzerland. Autoimmun Rev 2007;6:261-266.
17. Pugliatti M, Sotgiu S, Rosati G. The worldwide prevalence of multiple sclerosis. Clin Neurol Neurosurg 2002;104: 182-191.
18. Schoonen WM, Thomas SL, Somers EC, Smeeth L, Kim J, Evans S, Hall AJ. Do selected drugs increase the risk of lupus? A matched case-control study. Br J Clin Pharmacol 2010;70: 588-596.
19. Shoenfeld Y, Zandman-Goddard G, Stojanovich L, Cutolo M, Amital H, Levy Y, Abu-Shakra M, Barzilai O, Berkun Y, Blank M, de Carvalho JF, Doria A, Gilburd B, Katz U, Krause I, Langevitz P, Orbach H, Pordeus V, Ram M, Toubi E, Sherer Y. The mosaic of autoimmunity: hormonal and environmental factors involved in autoimmune diseases- 2008. Isr Med Assoc J 2008;10:8-12.
20. Shoenfeld Y, Gilburd B, Abu-ShakraM, Amital H, BarzilaiO, Berkun Y, Blank M, Zandman-Goddard G, KatzU, Krause I, Langevitz P, Levy Y, Orbach H, Pordeus V, Ram M, Sherer Y, Toubi E, Tomer Y. The mosaic of autoimmunity: genetic factors involved in autoimmune diseases-2008. Isr Med Assoc J 2008;10:3-7.
21. Zandman-Goddard G, Shoenfeld Y. Infections and SLE. Autoimmunity 2005;38:473-485.
22. Barabas AZ, Cole CD, Barabas AD, Lafreniere R. An experimental autoimmune kidney disease caused by pathogenic autoantibodies. In: Petrelli C, editor. New research on autoantibodies. Hauppauge NY: Nova Science Publishers, Inc. 2008. p 151-172.
23. Manson JJ, Mauri C, Ehrenstein MR. Natural serum IgM maintains immunological homeostasis and prevents autoimmunity. Springer Semin Immunopathol 2005;26: 425-432.
24. 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.
25. Quartier P, Potter PK, Ehrenstein MR,WalportMJ, Botto M. Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur J Immunol 2005;35:252-260.
26. Zwart B, Ciurana C, Rensink I, Manoe R, Hack CE, Aarden LA. Complement activation by apoptotic cells occurs predominantly via IgM and is limited to late apoptotic (secondary necrotic) cells. Autoimmunity 2004;37:95-102.
27. Ebringer A, Thorpe C, Pirt J, Wilson C, Cunningham P, Ettelaie C. Bovine spongiform encephalopathy: is it an autoimmune disease due to bacteria showing molecular mimicry with brain antigens? Environ Health Perspect 1997; 105:1172-1174.
28. Ebringer A, Rashid T, Wilson C. Rheumatoid arthritis: proposal for the use of anti-microbial therapy in early cases. Scand J Rheumatol 2003;32:2-11.
29. Ebringer A. Molecular mimicry as the basis of a new theory of autoimmunity. In: Zouali M, editor. Frontiers in Autoimmunity: fundamental aspects and clinical perspectives. Amsterdam Netherlands: IOS Press; 2003. p 79-99.
30. Ebringer A, Hughes L, Rashid T, Wilson C. Acinetobacter immune responses in multiple sclerosis: etiopathogenetic role and its possible use as a diagnostic marker. Arch Neurol 2005;62:33-36.
31. Ebringer A, Rashid T. Rheumatoid arthritis is caused by Proteus: the molecular mimicry theory and Karl Popper. Front Biosci (Elite Ed) 2009;1:577-586.
32. Mendrick DL, Noble B, Brentjens JR, Andres GA. Antibodymediated injury to proximal tubules in Heymann nephritis. Kidney Int 1980;18:328-343.
33. Barabas AZ, Cole CD, Barabas AD, Cowan JM, Yoon CS, Waisman DM, Lafreniere R. Presence of immunoglobulinM antibodies around the glomerular capillaries and in the mesangium of normal and passive Heymann nephritis rats. Int J Exp Pathol 2004;85:201-212.
34. Barabas AZ, Cole CD, Barabas AD, Barabas AN, Lafreniere R. Reduced incidence of slowly progressive Heymann nephritis in rats immunized with a modified vaccination technique. Clin Dev Immunol 2006;13:17-24.
35. Salant DJ, Cybulsky AV. Experimental glomerulonephritis. Methods Enzymol 1988;162:421-461.
36. Stenglein B, Thoenes GH, Gunther E. Genetically controlled autologous immune complex glomerulonephritis in rats. J Immunol 1975;115:895-897.
37. Barabas AZ, Lannigan R. Auto-immune nephritis in rats. J Pathol 1969;97:537-543.
38. Barabas AZ, Cole CD, Barabas AD, Lafreniere R. Production of a new model of slowly progressive Heymann nephritis. Int J Exp Pathol 2003;84:245-258.
39. Edgington TS, Glassock RJ, Watson JI, Dixon FJ. Characterization and isolation of specific renal tubular epithelial antigens. J Immunol 1967;99:1199-1210.
40. Edgington TS, Glassock RJ, Dixon FJ. Autologous immune complex nephritis induced with renal tubular antigen. I. Identification and isolation of the pathogenetic antigen. J Exp Med 1968;127:555-572.
41. Kamata K, Baird LG, Erikson ME, Collins AB, McCluskey RT. Characterization of antigens and antibody specificities involved in Heymann nephritis. J Immunol 1985;135: 2400-2408.
42. Kerjaschki D, Farquhar MG. The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border. Proc Natl Acad Sci U S A 1982;79:5557-5581.
43. Naruse T, Fukasawa T, Miyakawa Y. Laboratory model of membranous glomerulonephritis in rats induced by pronasedigested homologous renal tubular epithelial antigen. Lab Invest 1975;33:141-146.
44. Natori Y, Hayakawa I, Shibata S. Passive Heymann nephritis with acute and severe proteinuria induced by heterologous antibody against renal tubular brush border glycoprotein gp108. Lab Invest 1986;55:63-70.
45. Singh AK, Makker SP. Circulatory antigens of Heymann nephritis. I. Identification and partial characterization. Immunology 1986;57:467-472.
46. Tsukada Y, Ono K, Maezawa A, Yano S, Naruse T. A major pathogenic antigen of Heymann nephritis is present exclusively in the renal proximal tubule brush border-studies with a monoclonal antibody against pronase-digested tubular antigen. Clin Exp Immunol 1994;96:303-310.
47. Challice J, Barabas AZ, Cornish J, Bruce JW, Lannigan R. Passive Heymann nephritis in pre- and post-natal rats. Br J Exp Pathol 1986;67:915-924.
48. Cornish J, Barabas AZ, Lannigan R. Modified immunofluorescent antibody test: demonstration of nephritogenic antigen in glomeruli of rats. Diagn Immunol 1984;2: 133-136.
49. Edgington TS, Glassock RJ, Dixon FJ. Autologous immunecomplex pathogenesis of experimental allergic glomerulonephritis. Science 1967;155:1432-1434.
50. Raychowdhury R, Zheng G, Brown D, McCluskey RT. Induction of Heymann nephritis with a gp330/megalin fusion protein. Am J Pathol 1996;148:1613-1623.
51. Barabas AZ, Nagi AH, Lannigan R. Induction of experimental autologous immune-complex glomerulonephritis by eluted gamma-globulin. Int Urol Nephrol 1971;3:283-288.
52. Couser WG, Steinmuller DR, Stilmant MM, Salant DJ, Lowenstein LM. Experimental glomerulonephritis in the isolated perfused rat kidney. J Clin Invest 1978;62: 1275-1287.
53. Makker SP, Moorthy B. In situ immune complex formation in isolated perfused kidney using homologous antibody. Lab Invest 1981;44:1-5.
54. Sugisaki T, Klassen J, Andres GA, Milgrom F, McCluskey RT. Passive transfer of Heymann nephritis with serum. Kidney Int 1973;3:66-73.
55. Barabas AZ, Cole CD, Barabas AD, Barabas AN, Lafreniere R. Effect of rat kidney fraction 3 (rKF3) antigen and specific IgM antibody against rKF3 on the progression of slowly progressive Heymann nephritis. Pathol Int 2006;56: 516-529.
56. Barabas AZ, Cole CD, Barabas AD, Lafreniere R. Downregulation of pathogenic autoantibody response in a slowly progressive Heymann nephritis kidney disease model. Int J Exp Pathol 2004;85:321-334.
57. Barabas AZ, Cole CD, Barabas AD, Graeff RM, Lafreniere R, Weir DM. Application of the modified vaccination technique for the prevention and cure of chronic ailments. Asian Pac J Trop Med 2010;3:160-166.
58. Doria A, Sarzi-Puttini P, Shoenfeld Y. Infections, rheumatism and autoimmunity: the conflicting relationship between humans and their environment. Autoimmun Rev 2008;8: 1-4.
59. Arbuckle MR, McClain MT, Rubertone MV, Scofield RH, Dennis GJ, James JA, Harley JB. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003;349:1526-1533.
60. Stenglein B, Thoenes GH, Gunther E. Genetic control of susceptibility to autologous immune complex glomerulonephritis in inbred rat strains. Clin Exp Immunol 1978;33: 88-94.
61. Alousi MA, Post RS, Heymann W. Experimental autoimmune nephrosis in rats. Morphogenesis of the glomerular lesion: immunohistochemical and electron microscopic studies. Am J Pathol 1969;54:47-71.
62. Glassock RJ, Edgington TS,Watson JI, Dixon FJ. Autologous immune complex nephritis induced with renal tubular antigen. II. The pathogenetic mechanism. J Exp Med 1968; 127:573-588.
63. Kerjaschki D, Farquhar MG. Immunocytochemical localization of the Heymann nephritis antigen (GP330) in glomerular epithelial cells of normal Lewis rats. J Exp Med 1983;157:667-686.
64. Makker SP. Analysis of glomeruli-eluted Gp330 autoantibodies and of Gp330 antigen of Heymann nephritis. J Immunol 1993;151:6500-6508.
65. Neale TJ, Couser WG, Salant DJ, Lowenstein LM, Wilson CB. Specific uptake of Heymann's nephritic kidney eluate by rat kidney: studies in vivo and in isolated perfused kidneys. Lab Invest 1982;46:450-453.
66. Neale TJ, Wilson CB. Glomerular antigens in Heymann's nephritis: reactivity of eluted and circulating antibody. J Immunol 1982;128:323-330.
67. Barabas AZ, Cole CD, Barabas AD, Lafreniere R. Downregulation of a pathogenic autoantibody response by IgM autoantibodies directed against the nephritogenic antigen in slowly progressive Heymann nephritis. Pathol Int 2006;56: 181-190.
68. Abrass CK, McVay J, Glassock RJ. Evaluation of homologous and isologous passive Heymann nephritis: influence on endogenous antibody production. J Immunol 1983;130: 195-202.
69. Singh AK, Schwartz MM. Circulatory antigen of Heymann nephritis. II. Isolation of a 70,000 MWantigen from normal rat serum which cross-reacts with Heymann nephritis antigen. Immunology 1986;59:451-458.
70. Makker SP, Makker DM. A simple technique for detecting the antigen of Heymann nephritis in glomeruli by immunofluorescence. Clin Exp Immunol 1986;64:615-622.
71. Barabas AZ, Cole CD, Weir DM, Lafreniere R. The primary target antigenic site in Heymann nephritis is the renal proximal convoluted tubules' brush border associated zone of cells. In: Petrov M, editor. Autoimmune Disorders: Symptoms, Diagnosis and Treatment. Hauppauge NY: Nova Science Publishers, Inc. 2011. p 281-292.
72. Batsford SR, Weghaupt R, Takamiya H, Vogt A. Studies on the mesangial handling of protein antigens: influence of size, charge and biologic activity. Nephron 1985;41: 146-151.
73. Rosenzweig LJ, Kanwar YS. Removal of sulfated (heparan sulfate) or nonsulfated (hyaluronic acid) glycosaminoglycans results in increased permeability of the glomerular basement membrane to 125I-bovine serum albumin. Lab Invest 1982; 47:177-184.
74. Barabas AZ, Cole CD, Barabas AD, Lafreniere R. Pathogenic and nonpathogenic autoimmune events - the good and/or the bad?. In: Dubois Q, editor. Autoantibodies research progress. Hauppauge NY: Nova Science Publishers, Inc. 2008. p 9-18.
75. Ogden CA, Kowalewski R, Peng Y, Montenegro V, ElkonKB. IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity 2005; 38:259-264.
76. Wermeling F, Karlsson MC, McGaha TL. An anatomical view on macrophages in tolerance. Autoimmun Rev 2009;9: 49-52.
77. Noble B, Van Liew JB, Brentjens JR, Andres GA. Effect of reimmunization with Fx1A late in the course of Heymann nephritis. Lab Invest 1982;47:427-436.
78. Mevorach D, Mascarenhas JO, Gershov D, Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 1998;188:2313-2320.
79. PereiraWO, Amarante-Mendes GP. Apoptosis: a programme of cell death or cell disposal? Scand J Immunol 2011;73: 401-407.
80. Schulze C, Munoz LE, Franz S, Sarter K, Chaurio RA, Gaipl US, Herrmann M. Clearance deficiency-a potential link between infections and autoimmunity. Autoimmun Rev 2008;8:5-8.
81. Hogan SL, Muller KE, Jennette JC, Falk RJ. A review of therapeutic studies of idiopathic membranous glomerulopathy. Am J Kidney Dis 1995;25:862-875.
82. Perna A, Schieppati A, Zamora J, Giuliano GA, Braun N, Remuzzi G. Immunosuppressive treatment for idiopathic membranous nephropathy: a systematic review. Am J Kidney Dis 2004;44:385-401.
83. Dorner T, Radbruch A, Burmester GR. B-cell-directed therapies for autoimmune disease. Nat Rev Rheumatol 2009; 5:433-441.
84. Perosa F, Favoino E, CaragnanoMA, Prete M, Dammacco F. CD20: a target antigen for immunotherapy of autoimmune diseases. Autoimmun Rev 2005;4:526-531.
85. Townsend MJ, Monroe JG, Chan AC. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol Rev 2010;237:264-283.
86. Feldmann M, Steinman L. Design of effective immunotherapy for human autoimmunity. Nature 2005;435: 612-619.
87. Arnson Y, Shoenfeld Y, Amital H. Intravenous immunoglobulin therapy for autoimmune diseases. Autoimmunity 2009;42:553-560.
88. Durandy A, Kaveri SV, Kuijpers TW, Basta M, Miescher S, Ravetch JV, Rieben R. Intravenous immunoglobulins- understanding properties and mechanisms. Clin Exp Immunol 2009;158(Suppl 1):2-13.
89. Hartung HP,Mouthon L, Ahmed R, Jordan S, Laupland KB, Jolles S. Clinical applications of intravenous immunoglobulins (IVIg)-beyond immunodeficiencies and neurology. Clin Exp Immunol 2009;158(Suppl 1):23-33.
90. Sewell WA, Jolles S. Immunomodulatory action of intravenous immunoglobulin. Immunology 2002;107:387-393.
91. Barabas AZ, Cole CD, Barabas AD, Bahlis NJ, Lafreniere R. A vaccination technique to combat presently untreatable chronic ailments. BioProcess J 2007;6:12-18.
92. Barabas AZ, Cole CD, Barabas AD, Bahlis NJ, Lafreniere R. New vaccination technology for endogenous antigen-derived ailments. IDrugs 2008;11:111-115.
93. Barabas AZ, Weir DM, Cole CD, Barabas AD, Bahlis NJ, Graeff RM, Lafreniere R. Preventing and treating chronic disorders using the modified vaccination technique. Front Biosci 2009;14:3892-3898.
94. Barabas AZ, Cole CD, Barabas AD, Graeff RM, Lafreniere R, Weir DM. Correcting autoimmune anomalies in autoimmune disorders by immunological means, employing the modified vaccination technique. Autoimmun Rev 2009;8: 552-557.
95. Barabas AZ, ColeCD, BarabasAD, Graeff RM, Lafreniere R, Weir DM. Modified vaccination technique for prophylactic and therapeutic applications to combat endogenous antigeninduced disorders. Scandinav J Immunol 2010;71:125-133.
96. Blank M, Shoenfeld Y. B cell targeted therapy in autoimmunity. J Autoimmun 2007;28:62-68.
97. Byrd JC, Waselenko JK, Keating M, Rai K, Grever MR. Novel therapies for chronic lymphocytic leukemia in the 21st century. Semin Oncol 2000;27:587-597.
98. Ellis JH, Barber KA, Tutt A, Hale C, Lewis AP, Glennie MJ, Stevenson GT, Crowe JS. Engineered anti-CD38 monoclonal antibodies for immunotherapy of multiple myeloma. J Immunol 1995;155:925-937.
99. Martinelli E, De Palma R, Orditura M, De Vita F, Ciardiello F. Anti-epidermal growth factor receptor monoclonal antibodies in cancer therapy. Clin Exp Immunol 2009; 158:1-9.
100. Weir DM, Pinckard RN, Elson CJ, Suckling DE. Naturally occurring anti-tissue antibodies in rat sera. Clin Exp Immunol 1966;1:433-442.
101. Pinckard RN, Weir DM. Antibodies against the mitochondrial fraction of liver after toxic liver damage in rats. Clin Exp Immunol 1966;1:33-43.
102. Weir DM. The immune response after tissue injury. Pathol Eur 1966;1:108-118.
103. Andres G, Brentjens JR, Caldwell PR, Camussi G, Matsuo S. Formation of immune deposits and disease. Lab Invest 1986; 55:510-520.
104. Kerjaschki D. Molecular development of immune deposits and proteinuria in Heymann nephritis. Clin Investig 1993;71: 817-821.
105. Brown BA, Torabi M. Incidence of infusion-associated reactions with rituximab for treating multiple sclerosis: a retrospective analysis of patients treated at a US centre. Drug Safety 2011;34:117-123.
106. Barabas AZ, Cole CD, Weir DM, Lafreniere R. Immunopathological events in an experimental autoimmune kidney disease and how those events can be terminated to regain tolerance to self. In: Petrov M, editor. Autoimmune disorders: symptoms, diagnosis and treatment. Hauppauge NY: Nova Science Publishers, Inc. 2011. p 35-66.
107. Barabas AZ, Cole CD, Lafreniere R, Weir DM. Implicated autoantibodies in a kidney disease. In: Jenkins GE, Hall JI, editors Autoantibodies: detection, pathogenicity and health implications. Hauppauge NY: Nova Science Publishers, Inc.; 2012. In press.
108. Avrameas S. Natural autoantibodies: from 'horror autotoxicus' to 'gnothi seauton'. Immunol Today 1991;12:154-159.
109. Coutinho A, Kazatchkine MD, Avrameas S. Natural autoantibodies. Curr Opin Immunol 1995;7:812-818.
110. Ronco P, Debiec H. Molecular dissection of target antigens and nephritogenic antibodies in membranous nephropathy: towards epitope-driven therapies. J Am Soc Nephrol 2006; 17:1772-1774.
111. Ronco P, Debiec H. New insights into the pathogenesis of membranous glomerulonephritis. Curr Opin Nephrol Hypertens 2006;15:258-263.
112. PereiraWO, Amarante-Mendes GP. Apoptosis: a program of cell death or cell disposal? Scand J Immunol 2011;73: 401-407.
113. Amanna IJ, Slifka MK. Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol Rev 2010;236:125-138.
114. Chu VT, Beller A, Nguyen TT, Steinhauser G, Berek C. The long-term survival of plasma cells. Scand J Immunol 2011; 73:508-511.
115. Manz RA, Arce S, Cassese G, Hauser AE, Hiepe F, Radbruch A. Humoral immunity and long-lived plasma cells. Curr Opin Immunol 2002;14:517-521.
116. Yoshida T, Mei H, Dorner T, Hiepe F, Radbruch A, Fillatreau S, Hoyer BF. Memory B and memory plasma cells. Immunol Rev 2010;237:117-139.
117. Barabas AZ, Lafreniere R. Antigen-specific down-regulation of immunopathological events in an experimental autoimmune kidney disease. Autoimmun Rev 2005;4:565-570.
118. Barabas AZ, ColeCD, Barabas AD, Lafreniere R. A modified vaccination technique for the prevention and treatment of an experimental autoimmune kidney disease. Ann N Y Acad Sci 2007;1110:619-629.