Intravenous immunoglobulins exposed to heme (heme IVIG) are more efficient than IVIG in attenuating autoimmune diabetes

Clinical Immunology

Volumn 138, Issue 2, 2011, Pages 162-171

  Pavlovic, Sladjana ^a   Zdravkovic, Nemanja ^a   Dimitrov, Jordan D ^b   Djukic, Aleksandar ^a   Arsenijevic, Nebojsa ^a   Vassilev, Tchavdar L ^b   Lukic, Miodrag L ^a  

^a UNIVERSITY OF KRAGUJEVAC   (Serbia)

^b INSTITUTE OF MICROBIOLOGY   (Bulgaria)

Author keywords

Autoimmunity; IVIG; T1D; Treg cells

Indexed keywords

ANTIDIABETIC AGENT; GAMMA INTERFERON; GLUCOSE; HEME EXPOSED IMMUNOGLOBULIN; HEMOGLOBIN A1C; HUMAN IMMUNOGLOBULIN; IMMUNOGLOBULIN; INTERLEUKIN 12; INTERLEUKIN 17; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; C57BL 6 MOUSE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; DISEASE COURSE; DOWN REGULATION; GLUCOSE BLOOD LEVEL; GLUCOSURIA; LYMPH NODE; MALE; MOUSE; NONHUMAN; PANCREAS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STREPTOZOCIN DIABETES; TREATMENT DURATION;

ANIMALS; CYCLOPHOSPHAMIDE; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DOWN-REGULATION; GLYCOSURIA; HEME; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; HYPERGLYCEMIA; IMMUNOGLOBULINS, INTRAVENOUS; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES, REGULATORY;

EID: 79251598193     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2010.10.010     Document Type: Article

References (44)

1. Aktas O., Waiczies S., Grieger U., Wendling U., Zschenderlein R., Zipp F. Polyspecific immunoglobulins (IVIg) suppress proliferation of human (auto) antigen-specific T cells with-out inducing apoptosis. J. Neuroimmunol. 2001, 114:160-167.
2. Kazatchkine M.D., Kaveri S.V. Immunomodulation of autoimmune and inflammatory diseases with intravenous immuneglobulin. N Engl J. Med. 2001, 345:747-755.
3. Kaveri S.V., Lacroix-Desmazes S., Bayry J. The antiinflammatory IgG. N Engl J. Med. 2008, 359:307-309.
4. Vani J., Elluru S., Negi V.S., Lacroix-Desmazes S., Kazatchkine M.D., Bayary J., Kaveri S.V. Role of natural antibodies in immune homeostasis: IVIg perspective. Autoimmun. Rev. 2008, 7:440-444.
5. Kaveri S., Prasad N., Vassilev T., Hurez V., Pashov A., Lacroix-Desmazes S., Kazatchkine M. Modulation of autoimmune responses by intravenous immunoglobulin (IVIg). Mult. Scler. 1997, 3:121-128.
6. Anthony R.M., Wermeling F., Karlsson M.C., Ravetch J.V. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc. Natl Acad. Sci. 2008, 105:19571-19578.
7. Ephrem A., Chamat S., Miquel C., Fisson S., Mouthon L., Caligiuri G., Delignat S., Elluru S., Bayry J., Lacroix-Desmazes S., Cohen J.L., Salomon B.L., Kazatchkine M.D., Kaveri S.V., Misra N. Expansion of CD4+CD25+ regulatory T cells by intravenous immunoglobulin: a critical factor in controlling experimental autoimmune encephalomyelitis. Blood 2008, 111:715-722.
8. Bruley-Rosset M., Mouthon L., Chanseaud Y., Dhainaut F., Lirochon J., Bourel D. Polyreactive autoantibodies purified from human intravenous immunoglobulins prevent the development of experimental autoimmune diseases. Lab. Invest. 2003, 83:1013-1023.
9. Inoue Y., Kaifu T., Sugahara-Tobinai A., Nakamura A., Miyazaki J., Takai T. Activating Fc gamma receptors participate in the development of autoimmune diabetes in NOD mice. J. Immunol. 2007, 179:764-774.
10. Brode S., Raine T., Zaccone P., Cooke A. Cyclophosphamide-induced type-1 diabetes in the NOD mouse is associated with a reduction of CD4+CD25+Foxp3+ regulatory T cells. J. Immunol. 2006, 177:6603-6612.
11. Zdravkovic N., Shahin A., Arsenijevic N., Lukic M.L., Mensah-Brown E.P. Regulatory T cells and ST2 signaling control diabetes induction with multiple low doses of streptozotocin. Mol. Immunol. 2009, 47:28-36.
12. Dimitrov J.D., Roumenina L.T., Doltchinkova V.R., Mihaylova N.M., Lacroix-Desmazes S., Kaveri S.V., Vassilev T.L. Antibodies use hema as a cofactor to extend their pathogen elimination activity and to acquire new effector functions. J. Biol. Chem. 2007, 282:26696-26706.
13. Djoumerska I., Tchorbanov A., Pashov A., Vassilev T. The autoreactivity of therapeutic intravenous immunoglobulin (IVIG) preparations depends on the fractionation methods used. Scand. J. Immunol. 2005, 61:357-363.
14. Ablamunits V., Quintana F., Reshef T., Elias D., Cohen I.R. Acceleration of autoimmune diabetes by cyclophosphamide is associated with an enhanced IFN-gamma secretion pathway. J. Autoimmun. 1999, 13:383-392.
15. Dimitrov J.D., Roumenina L.T., Doltchinkova V.R., Vassilev T.L. Iron ions and haeme modulate the binding properties of complement subcomponent C1q and of immunoglobulins. Scand. J. Immunol. 2007, 65:230-239.
16. Achiron A., Mor F., Margalit R., Cohen I.R., Lider O., Miron S. Suppression of experimental autoimmune encephalomyelitis by intravenously administered polyclonal immunoglobulins. J. Autoimmun. 2000, 15:323-330.
17. Achiron A., Margalit R., Hershkoviz R., Markovits D., Reshef T., Melamed E., Cohen I.R., Lider O. Intravenous immunoglobulin treatment of experimental T cell-mediated autoimmune disease. Upregulation of T cell proliferation and downregulation of tumor necrosis factor alpha secretion. J. Clin. Invest. 1994, 93:600-605.
18. Gong F., Hu Y., Chen L., Gu W. The therapeutic effect of intravenous immunoglobulins and vitamin C on the progression of experimental autoimmune myocarditis in the mouse. Med. Sci. Monit. 2007, 13:240-246.
19. Dalakas M. IVIg in other autoimmune neurological disorders: current status and future prospects. J. Neurol. 2008, 255:12-16.
20. Andersson U.G., Bjork L., Skansen-Saphir U., Andersson J. Pooled human IgG modulates cytokine production in lymphocytes and monocytes. Immunol. Rev. 1994, 139:21-42.
21. Mouzaki A., Theodoropoulou M., Gianakopoulos I., Vlaha V., Kyrtsonis M.C., Maniatis A. Expression patterns of Th1 and Th2 cytokine genes in childhood idiopathic thrombocytopenic purpura (ITP) at presentation and their modulation by intravenous immunoglobulin G (IVIg) treatment: their role in prognosis. Blood 2002, 100:1774-1779.
22. Bayry J., Lacroix-Desmazes S., Carbonneil C., Misra N., Donkova V., Pashov A., Chevailler A., Mouthon L., Weill B., Bruneval P., Kazatchkine M.D., Kaveri S.V. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood 2003, 101:758-765.
23. Ibáñez C., Montoro-Ronsano J.B. Intravenous immunoglobulin preparations and autoimmune disorders: mechanisms of action. Curr. Pharm. Biotechnol. 2003, 4:239-247.
24. Samuelsson A., Towers T.L., Ravetch J.V. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science 2001, 291:484-486.
25. Bruhns P., Samuelsson A., Pollard J.W., Ravetch J.V. Colony-stimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity 2003, 18:573-581.
26. Krause Mda.S., de Bittencourt P.I. Type 1 diabetes: can exercise impair the autoimmune event? The l-arginine/glutamine coupling hypothesis. Cell Biochem. Funct. 2008, 26:406-433.
27. Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000, 101:455-458.
28. Kessel A., Ammuri H., Peri R., Pavlotzky E.R., Blank M., Shoenfeld Y., Toubi E. Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J. Immunol. 2007, 179:5571-5575.
29. Aktas O., Zipp F. Regulation of self-reactive T cells by human immunoglobulins - implications for multiple sclerosis therapy. Curr. Pharm. Des. 2003, 9:245-256.
30. Roncarolo M.G., Battaglia M. Regulatory T-cell immunotherapy for tolerance to self antigens and alloantigens in humans. Nat. Rev. Immunol. 2007, 7:585-598.
31. Bayry J., Lacroix-Desmazes S., Dasgupta S., Kazatchkine M.D., Kaveri S.V. Efficacy of regulatory T-cell immunotherapy: are inflammatory cytokines key determinants?. Nat. Rev. Immunol. 2008, 8:1p.
32. Fuchs S., Feferman T., Zhu K.Y., Meidler R., Margalit R., Wang N., Laub O., Souroujon M.C. Suppression of experimental autoimmune myasthenia gravis by intravenous immunoglobulin and isolation of a disease-specific IgG fraction. Ann. NY Acad. Sci. 2007, 1110:550-558.
33. Polak L., Geleick H., Turk J.L. Reversal by cyclophosphamide of tolerance in contact sensitization: tolerance induced by prior feeding with DNCB. Immunology 1975, 28:939-942.
34. Yasunami R., Bach J.F. Anti-suppressor effect of cyclophosphamide on the development of spontaneous diabetes in NOD mice. Eur. J. Immunol. 1988, 18:481-484.
35. Mitsuoka A., Baba M., Morikawa S. Enhancement of delayed hypersensitivity by depletion of suppressor T cells with cyclophosphamide in mice. Nature 1976, 262:77-78.
36. Röllinghoff M., Starzinski-Powitz A., Pfizenmaier K., Wagner H. Cyclophosphamide-sensitive T lymphocytes suppress the in vivo generation ofantigen-specific cytotoxic T lymphocytes. J. Exp. Med. 1997, 145:455-459.
37. Charlton B., Bacelj A., Slattery R.M., Mandel T.E. Cyclophosphamide-induced diabetes in NOD/WEHI mice: evidence for suppression in spontaneous autoimmune diabetes mellitus. Diabetes 1989, 38:441-447.
38. Turk J.L., Poulter L.W. Selective depletion of lymphoid tissue by cyclophosphamide. Clin. Exp. Immunol. 1972, 10:285-296.
39. Turk J.L., Parker D., Poulter L.W. Functional aspects of the selective depletion of lymphoid tissue by cyclophosphamide. Immunology 1972, 23:493-501.
40. Beyer M., Kochanek M., Darabi K., Popov A., Jensen M., Endl E., Knolle P.A., Thomas R.K., von Bergwelt-Baildon M., Debey S., Hallek M., Schultze J.L. Reduced frequencies and suppressive function of CD4+CD25 hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 2005, 106:2018-2025.
41. Ghiringhelli F., Larmonier N., Schmitt E., Parcellier A., Cathelin D., Garrido C., Chauffert B., Solary E., Bonnotte B., Martin F. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. 2004, 34:336-344.
42. Lee T.S., Chau L.Y. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 2002, 8:240-246.
43. Sheng W.S., Hu S., Nettles A.R., Lokensgard J.R., Vercellotti G.M., Rock R.B. Hemin inhibits NO production by IL-1β-stimulated human astrocytes through induction of heme oxygenase-1 and reduction of p38 MAPK activation. J. Neuroinflammation 2010, 7:51.
44. Li M., Peterson S., Husney D., Inaba M., Guo K., Kappas A., Ikehara S., Abraham N.G. Long-lasting expression of HO-1 delays progression of type I diabetes in NOD mice. Cell Cycle 2007, 6:567-571.