IgG glycan hydrolysis by endoglycosidase S diminishes the proinflammatory properties of immune complexes from patients with systemic lupus erythematosus: A possible new treatment?

Arthritis and Rheumatism

Volumn 64, Issue 8, 2012, Pages 2698-2706

  Lood, Christian ^a   Allhorn, Maria ^b   Lood, Rolf ^b   Gullstrand, Birgitta ^b   Olin, Anders I ^b   Rönnblom, Lars ^c   Truedsson, Lennart ^b   Collin, Mattias ^b   Bengtsson, Anders A ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ENDOGLYCOSIDASE S; FC RECEPTOR; GLYCOSIDASE; IMMUNOGLOBULIN G ANTIBODY; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CHEMICAL STRUCTURE; CHEMOTAXIS; CLINICAL ARTICLE; COMPLEMENT ACTIVATION; COMPLEMENT CLASSICAL PATHWAY; FEMALE; GLYCOSYLATION; HUMAN; HUMAN TISSUE; HYDROLYSIS; INTERFERON PRODUCTION; MALE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RESPIRATORY BURST; STREPTOCOCCUS PYOGENES; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIGEN-ANTIBODY COMPLEX; BACTERIAL PROTEINS; CHEMOTAXIS; DENDRITIC CELLS; FEMALE; GLYCOSIDE HYDROLASES; HUMANS; HYDROLYSIS; IMMUNOGLOBULIN G; INFLAMMATION; INTERFERON-ALPHA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MIDDLE AGED; NEUTROPHILS; PHAGOCYTOSIS; POLYSACCHARIDES; RECEPTORS, IGG; YOUNG ADULT;

EID: 84864484027     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.34454     Document Type: Article

References (50)

1. Crispin JC, Liossis SN, Kis-Toth K, Lieberman LA, Kyttaris VC, Juang YT, et al. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 2010; 16: 47-57.
2. Ronnblom L, Alm GV, Eloranta ML,. The type I interferon system in the development of lupus. Semin Immunol 2011; 23: 113-21.
3. Hanrotel-Saliou C, Segalen I, Le Meur Y, Youinou P, Renaudineau Y,. Glomerular antibodies in lupus nephritis. Clin Rev Allergy Immunol 2011; 40: 151-8.
4. Kronborg G, Fomsgaard A, Jensen ET, Kharazmi A, Hoiby N,. Induction of oxidative burst response in human neutrophils by immune complexes made in vitro of lipopolysaccharide and hyperimmune serum from chronically infected patients. APMIS 1993; 101: 887-94.
5. Grootscholten C, van Bruggen MC, van der Pijl JW, de Jong EM, Ligtenberg G, Derksen RH, et al, for the Dutch Working Party on Systemic Lupus Erythematosus. Deposition of nucleosomal antigens (histones and DNA) in the epidermal basement membrane in human lupus nephritis. Arthritis Rheum 2003; 48: 1355-62.
6. Hunder GG, McDuffie FC, Huston KA, Elveback LR, Hepper NG,. Pleural fluid complement, complement conversion, and immune complexes in immunologic and nonimmunologic diseases. J Lab Clin Med 1977; 90: 971-80.
7. Ju JH, Min JK, Jung CK, Oh SN, Kwok SK, Kang KY, et al. Lupus mesenteric vasculitis can cause acute abdominal pain in patients with SLE. Nat Rev Rheumatol 2009; 5: 273-81.
8. Gabrielli A, Corvetta A, Montroni M, Rupoli S, Danieli G,. Immune deposits in normal skin of patients with systemic lupus erythematosus: relationship to the serum capacity to solubilize immune complexes. Clin Immunol Immunopathol 1985; 36: 266-74.
9. Hoffman SA, Arbogast DN, Day TT, Shucard DW, Harbeck RJ,. Permeability of the blood cerebrospinal fluid barrier during acute immune complex disease. J Immunol 1983; 130: 1695-8.
10. Sher JH, Pertschuk LP,. Immunoglobulin G deposits in the choroid plexus of a child with systemic lupus erythematosus. J Pediatr 1974; 85: 385-7.
11. Palatinus A, Adams M,. Thrombosis in systemic lupus erythematosus. Semin Thromb Hemost 2009; 35: 621-9.
12. Vlachoyiannopoulos PG, Samarkos M, Sikara M, Tsiligros P,. Antiphospholipid antibodies: laboratory and pathogenetic aspects. Crit Rev Clin Lab Sci 2007; 44: 271-338.
13. Bave U, Magnusson M, Eloranta ML, Perers A, Alm GV, Ronnblom L,. FcγRIIa is expressed on natural IFN-α-producing cells (plasmacytoid dendritic cells) and is required for the IFN-α production induced by apoptotic cells combined with lupus IgG. J Immunol 2003; 171: 3296-302.
14. Vallin H, Blomberg S, Alm GV, Cederblad B, Ronnblom L,. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-α (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin Exp Immunol 1999; 115: 196-202.
15. Ronnblom L, Pascual V,. The innate immune system in SLE: type I interferons and dendritic cells. Lupus 2008; 17: 394-9.
16. Ronnblom LE, Alm GV, Oberg KE,. Possible induction of systemic lupus erythematosus by interferon-α treatment in a patient with a malignant carcinoid tumour. J Intern Med 1990; 227: 207-10.
17. Selmi C, Lleo A, Zuin M, Podda M, Rossaro L, Gershwin ME,. Interferon α and its contribution to autoimmunity. Curr Opin Investig Drugs 2006; 7: 451-6.
18. Wilson LE, Widman D, Dikman SH, Gorevic PD,. Autoimmune disease complicating antiviral therapy for hepatitis C virus infection. Semin Arthritis Rheum 2002; 32: 163-73.
19. Collin M, Olsen A,. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J 2001; 20: 3046-55.
20. Allhorn M, Olin AI, Nimmerjahn F, Collin M,. Human IgG/FcγR interactions are modulated by streptococcal IgG glycan hydrolysis. PLoS One 2008; 3: e1413.
21. Albert H, Collin M, Dudziak D, Ravetch JV, Nimmerjahn F,. In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner. Proc Natl Acad Sci U S A 2008; 105: 15005-9.
22. Allhorn M, Collin M,. Sugar-free antibodies-the bacterial solution to autoimmunity? Ann N Y Acad Sci 2009; 1173: 664-9.
23. Ronnblom L, Elkon KB,. Cytokines as therapeutic targets in SLE. Nat Rev Rheumatol 2010; 6: 339-47.
24. La Cava A,. Targeting B cells with biologics in systemic lupus erythematosus. Expert Opin Biol Ther 2010; 10: 1555-61.
25. Gladman DD, Ibanez D, Urowitz MB,. Systemic Lupus Erythematosus Disease Activity Index 2000. J Rheumatol 2002; 29: 288-91.
26. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982; 25: 1271-7.
27. Allhorn M, Briceno JG, Baudino L, Lood C, Olsson ML, Izui S, et al. The IgG-specific endoglycosidase EndoS inhibits both cellular and complement-mediated autoimmune hemolysis. Blood 2010; 115: 5080-8.
28. Lood C, Gullstrand B, Truedsson L, Olin AI, Alm GV, Ronnblom L, et al. C1q inhibits immune complex-induced interferon-α production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 2009; 60: 3081-90.
29. Lovgren T, Eloranta ML, Bave U, Alm GV, Ronnblom L,. Induction of interferon-α production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG. Arthritis Rheum 2004; 50: 1861-72.
30. Bave U, Alm GV, Ronnblom L,. The combination of apoptotic U937 cells and lupus IgG is a potent IFN-α inducer. J Immunol 2000; 165: 3519-26.
31. Collin M, Olsen A,. Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect Immun 2001; 69: 7187-9.
32. Fredrikson GN, Truedsson L, Sjoholm AG,. New procedure for the detection of complement deficiency by ELISA: analysis of activation pathways and circumvention of rheumatoid factor influence. J Immunol Methods 1993; 166: 263-70.
33. Hargraves MM, Richmond H, Morton R,. Presentation of two bone marrow elements; the tart cell and the L.E. cell. Proc Staff Meet Mayo Clin 1948; 23: 25-8.
34. Schett G, Steiner G, Smolen JS,. Nuclear antigen histone H1 is primarily involved in lupus erythematosus cell formation. Arthritis Rheum 1998; 41: 1446-55.
35. Bao L, Osawe I, Puri T, Lambris JD, Haas M, Quigg RJ,. C5a promotes development of experimental lupus nephritis which can be blocked with a specific receptor antagonist. Eur J Immunol 2005; 35: 2496-506.
36. Collin M, Svensson MD, Sjoholm AG, Jensenius JC, Sjobring U, Olsen A,. EndoS and SpeB from Streptococcus pyogenes inhibit immunoglobulin-mediated opsonophagocytosis. Infect Immun 2002; 70: 6646-51.
37. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J,. Induction of dendritic cell differentiation by IFN-α in systemic lupus erythematosus. Science 2001; 294: 1540-3.
38. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J,. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003; 19: 225-34.
39. Matikainen S, Paananen A, Miettinen M, Kurimoto M, Timonen T, Julkunen I, et al. IFN-α and IL-18 synergistically enhance IFN-γ production in human NK cells: differential regulation of Stat4 activation and IFN-γ gene expression by IFN-α and IL-12. Eur J Immunol 2001; 31: 2236-45.
40. Marrack P, Kappler J, Mitchell T,. Type I interferons keep activated T cells alive. J Exp Med 1999; 189: 521-30.
41. Hooks JJ, Moutsopoulos HM, Geis SA, Stahl NI, Decker JL, Notkins AL,. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med 1979; 301: 5-8.
42. Crow MK, Kirou KA, Wohlgemuth J,. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 2003; 36: 481-90.
43. Lood C, Amisten S, Gullstrand B, Jonsen A, Allhorn M, Truedsson L, et al. Platelet transcriptional profile and protein expression in patients with systemic lupus erythematosus: up-regulation of the type I interferon system is strongly associated with vascular disease. Blood 2010; 116: 1951-7.
44. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A 2010; 107: 9813-8.
45. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011; 3 (73): 73ra20.
46. Gullstrand B, Martensson U, Sturfelt G, Bengtsson AA, Truedsson L,. Complement classical pathway components are all important in clearance of apoptotic and secondary necrotic cells. Clin Exp Immunol 2009; 156: 303-11.
47. Hayakawa S, Nakabayashi K, Karube M, Arimura Y, Soejima A, Yamada A, et al. Tubulointerstitial immune complex nephritis in a patient with systemic lupus erythematosus: role of peritubular capillaritis with immune complex deposits in the pathogenesis of the tubulointerstitial nephritis. Clin Exp Nephrol 2006; 10: 146-51.
48. Collin M, Shannon O, Bjorck L,. IgG glycan hydrolysis by a bacterial enzyme as a therapy against autoimmune conditions. Proc Natl Acad Sci U S A 2008; 105: 4265-70.
49. Van Timmeren MM, van der Veen BS, Stegeman CA, Petersen AH, Hellmark T, Collin M, et al. IgG glycan hydrolysis attenuates ANCA-mediated glomerulonephritis. J Am Soc Nephrol 2010; 21: 1103-14.
50. Yang R, Otten MA, Hellmark T, Collin M, Bjorck L, Zhao MH, et al. Successful treatment of experimental glomerulonephritis with IdeS and EndoS, IgG-degrading streptococcal enzymes. Nephrol Dial Transplant 2010; 25: 2479-86.