Therapeutic inhibition of the alternative complement pathway attenuates chronic EAE

Molecular Immunology

Volumn 54, Issue 3-4, 2013, Pages 302-308

  Hu, Xianzhen ^a   Holers, V Michael ^b   Thurman, Joshua M ^c   Schoeb, Trent R ^d   Ramos, Theresa N ^a   Barnum, Scott R ^a  

^a University of Alabama at Birmingham   (United States)

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

^c UNIVERSITY OF COLORADO   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Alternative pathway; Complement; Demyelinating disease; Factor B

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 1379; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL SPECIFICITY; CHRONIC DISEASE; COMPLEMENT ALTERNATIVE PATHWAY; CONTROLLED STUDY; DEMYELINATION; DISEASE COURSE; INFLAMMATION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; COMPLEMENT FACTOR B; COMPLEMENT PATHWAY, ALTERNATIVE; COMPLEMENT SYSTEM PROTEINS; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INFLAMMATION; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES;

ANIMALIA; MUS;

EID: 84872547474     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.12.018     Document Type: Article

References (47)

1. Compston A. McAlpine's Multiple Sclerosis 2006, Philadelphia, Elsevier/Churchill Livingstone.
2. Flachenecker P., Stuke K. National MS registries. Journal of Neurology 2008, 255(Suppl. 6):102-108. doi: 10.1007/s00415-008-6019-5. Epub 2009/03/28. PubMed PMID: 19300969.
3. Dalakas M.C. Advances in the diagnosis, pathogenesis and treatment of CIDP. Nature Reviews Neurology 2011, 7(9):507-517. doi: 10.1038/nrneurol.2011.121. Epub 2011/08/17. PubMed PMID: 21844897.
4. Soliven B. Autoimmune neuropathies: insights from animal models. Journal of the Peripheral Nervous System: JPNS 2012, 17(Suppl 2):28-33. doi: 10.1111/j.1529-8027.2012.00392.x. Epub 2012/05/11. PubMed PMID: 22548620.
5. Vlam L., van den Berg L.H., Cats E.A., Piepers S., van der Pol W.L. Immune pathogenesis and treatment of multifocal motor neuropathy. Journal of Clinical Immunology 2012, doi: 10.1007/s10875-012-9779-8. PubMed PMID: 22941513. Epub 2012/09/04.
6. Dalakas M.C. Clinical trials in CIDP and chronic autoimmune demyelinating polyneuropathies. Journal of the Peripheral Nervous System: JPNS 2012, 17(Suppl. 2):34-39. doi: 10.1111/j.1529-8027.2012.00393.x. Epub 2012/05/11. PubMed PMID: 22548621.
7. Buck D., Hemmer B. Treatment of multiple sclerosis: current concepts and future perspectives. Journal of Neurology 2011, 258(10):1747-1762. doi: 10.1007/s00415-011-6101-2. Epub 2011/06/04. PubMed PMID: 21637950.
8. Saidha S., Eckstein C., Calabresi P.A. New and emerging disease modifying therapies for multiple sclerosis. Annals of the New York Academy of Sciences 2012, 1247:117-137. doi: 10.1111/j.1749-6632.2011.06272.x. Epub 2012/01/10. PubMed PMID: 22224673.
9. Weber M.S., Menge T., Lehmann-Horn K., Kronsbein H.C., Zettl U., Sellner J., et al. Current treatment strategies for multiple sclerosis - efficacy versus neurological adverse effects. Current Pharmaceutical Design 2012, 18(2):209-219. Epub 2012/01/11. PubMed PMID: 22229582.
10. Barnum S.R., Szalai A.J. Complement and demyelinating disease: no MAC needed?. Brain Research Reviews 2006, 52:58-68.
11. Willison H.J., Halstead S.K., Beveridge E., Zitman F.M., Greenshields K.N., Morgan B.P., et al. The role of complement and complement regulators in mediating motor nerve terminal injury in murine models of Guillain-Barre syndrome. Journal of Neuroimmunology 2008, 201-202:172-182. doi: 10.1016/j.jneuroim.2008.05.028. Epub 2008/07/31. PubMed PMID: 18664403.
12. Vogel C.W., Fritzinger D.C. Cobra venom factor: structure, function, and humanization for therapeutic complement depletion. Toxicon: Official Journal of the International Society on Toxinology 2010, 56(7):1198-1222. doi: 10.1016/j.toxicon.2010.04.007. Epub 2010/04/27. PubMed PMID: 20417224.
13. Nataf S., Carroll S.L., Wetsel R.A., Szalai A.J., Barnum S.R. Attenuation of experimental autoimmune demyelination in complement-deficient mice. Journal of Immunology 2000, 165(10):5867-5873. PubMed PMID: 11067947.
14. Szalai A.J., Hu X., Adams J.E., Barnum S.R. Complement in experimental autoimmune encephalomyelitis revisited: C3 is required for development of maximal disease. Molecular Immunology 2007, PubMed PMID: 17353050.
15. Muller-Eberhard H.J. Molecular organization and function of the complement system. Annual Review of Biochemistry 1988, 57:321-347. doi: 10.1146/annurev.bi.57.070188.001541. Epub 1988/01/01. PubMed PMID: 3052276.
16. Holers V.M. The complement system as a therapeutic target in autoimmunity. Clinical Immunology 2003, 107(3):140-151. Epub 2003/06/14. PubMed PMID: 12804527.
17. Holers V.M., Thurman J.M. The alternative pathway of complement in disease: opportunities for therapeutic targeting. Molecular immunology 2004, 41(2-3):147-152. doi: 10.1016/j.molimm.2004.03.012. Epub 2004/05/26. PubMed PMID: 15159060.
18. Holers V.M. The spectrum of complement alternative pathway-mediated diseases. Immunological Reviews 2008, 223:300-316. doi:IMR641[pii]10.1111/j.1600-065X.2008.00641.x. Epub 2008/07/11. PubMed PMID: 18613844.
19. Qiao F., Atkinson C., Song H., Pannu R., Singh I., Tomlinson S. Complement plays an important role in spinal cord injury and represents a therapeutic target for improving recovery following trauma. The American journal of Pathology 2006, 169(3):1039-1047. PubMed PMID: 16936276.
20. Leinhase I., Rozanski M., Harhausen D., Thurman J.M., Schmidt O.I., Hossini A.M., et al. Inhibition of the alternative complement activation pathway in traumatic brain injury by a monoclonal anti-factor B antibody: a randomized placebo-controlled study in mice. Journal of Neuroinflammation 2007, 4:13. doi: 1742-2094-4-13[pii]10.1186/1742-2094-4-13. Epub 2007/05/04. PubMed PMID: 17474994; PubMed Central PMCID: PMC1867808.
21. Matsumoto M., Fukuda W., Circolo A., Goellner J., Strauss-Schoenberger J., Wang X., et al. Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proceedings of the National Academy of Sciences of the United States of America 1997, 94(16):8720-8725. PubMed PMID: 0009238044.
22. Szalai A.J., Nataf S., Hu X.Z., Barnum S.R. Experimental allergic encephalomyelitis is inhibited in transgenic mice expressing human C-reactive protein. Journal of Immunology 2002, 168(11):5792-5797. PubMed PMID: 12023381.
23. Thurman J.M., Kraus D.M., Girardi G., Hourcade D., Kang H.J., Royer P.A., et al. A novel inhibitor of the alternative complement pathway prevents antiphospholipid antibody-induced pregnancy loss in mice. Molecular Immunology 2005, 42(1):87-97. PubMed PMID: 15488947.
24. Markiewski M.M., Nilsson B., Ekdahl K.N., Mollnes T.E., Lambris J.D. Complement and coagulation: strangers or partners in crime?. Trends in Immunology 2007, 28(4):184-192. doi: S1471-4906(07)00048-8 [pii]10.1016/j.it.2007.02.006. Epub 2007/03/06. PubMed PMID: 17336159.
25. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nature Immunology 2010, 11(9):785-797. doi: 10.1038/ni.1923. PubMed PMID: 20720586 Epub 2010/08/20. PubMed Central PMCID: PMC2924908.
26. Hillmen P., Young N.S., Schubert J., Brodsky R.A., Socie G., Muus P., et al. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. The New England Journal of Medicine 2006, 355(12):1233-1243. doi: 355/12/1233 [pii]10.1056/NEJMoa061648. Epub 2006/09/23. PubMed PMID: 16990386.
27. Rother R.P., Rollins S.A., Mojcik C.F., Brodsky R.A., Bell L. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nature Biotechnology 2007, 25(11):1256-1264. doi: nbt1344 [pii]10.1038/nbt1344. Epub 2007/11/09. PubMed PMID: 17989688.
28. Brodsky R.A., Young N.S., Antonioli E., Risitano A.M., Schrezenmeier H., Schubert J., et al. Multicenter phase 3 study of the complement inhibitor eculizumab for the treatment of patients with paroxysmal nocturnal hemoglobinuria. Blood 2008, 111(4):1840-1847. doi: blood-2007-06-094136 [pii]10.1182/blood-2007-06-094136. Epub 2007/12/07. PubMed PMID: 18055865.
29. Lapeyraque A.L., Malina M., Fremeaux-Bacchi V., Boppel T., Kirschfink M., Oualha M., et al. Eculizumab in severe Shiga-toxin-associated HUS. The New England Journal of Medicine 2011, 364(26):2561-2563. doi: 10.1056/NEJMc1100859. Epub 2011/05/27. PubMed PMID: 21612462.
30. Noris M., Mescia F., Remuzzi G. STEC-HUS, atypical HUS and TTP are all diseases of complement activation. Nature Reviews Nephrology 2012, 8(11):622-633. doi: 10.1038/nrneph.2012.195. Epub 2012/09/19. PubMed PMID: 22986360.
31. Zimmerhackl L.B., Hofer J., Cortina G., Mark W., Wurzner R., Jungraithmayr T.C., et al. Prophylactic eculizumab after renal transplantation in atypical hemolytic-uremic syndrome. The New England Journal of Medicine 2010, 362(18):1746-1748. doi: 10.1056/NEJMc1001060. Epub 2010/05/07. PubMed PMID: 20445192.
32. Zuber J., Fakhouri F., Roumenina L.T., Loirat C., Fremeaux-Bacchi V. Use of eculizumab for atypical haemolytic uraemic syndrome and C3 glomerulopathies. Nature Reviews Nephrology 2012, 8(11):643-657. doi: 10.1038/nrneph.2012.214. Epub 2012/10/03. PubMed PMID: 23026949.
33. Leinhase I., Holers V.M., Thurman J.M., Harhausen D., Schmidt O.I., Pietzcker M., et al. Reduced neuronal cell death after experimental brain injury in mice lacking a functional alternative pathway of complement activation. BMC Neuroscience 2006, 7:55. 1471-2202-7-55 [pii]10.1186/1471-2202-7-55. Epub 2006/07/18. PubMed PMID: 16842619; PubMed Central PMCID: PMC1540436.
34. Stahl G.L., Xu Y., Hao L., Miller M., Buras J.A., Fung M., et al. Role for the alternative complement pathway in ischemia/reperfusion injury. The American Journal of Pathology 2003, 162(2):449-455. 10.1016/S0002-9440(10)63839-4. Epub 2003/01/28. PubMed PMID: 12547703; PubMed Central PMCID: PMC1851150.
35. Thurman J.M., Ljubanovic D., Edelstein C.L., Gilkeson G.S., Holers V.M. Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. Journal of Immunology 2003, 170(3):1517-1523. Epub 2003/01/23. PubMed PMID: 12538716.
36. Thurman J.M., Royer P.A., Ljubanovic D., Dursun B., Lenderink A.M., Edelstein C.L., et al. Treatment with an inhibitory monoclonal antibody to mouse factor B protects mice from induction of apoptosis and renal ischemia/reperfusion injury. Journal of the American Society of Nephrology: JASN 2006, 17(3):707-715. doi: ASN. 2005070698 [pii]10.1681/ASN.2005070698. Epub 2006/02/10. PubMed PMID: 16467447.
37. Watanabe H., Garnier G., Circolo A., Wetsel R.A., Ruiz P., Holers V.M., et al. Modulation of renal disease in MRL/lpr mice genetically deficient in the alternative complement pathway factor B. Journal of Immunology 2000, 164(2):786-794. PubMed PMID: 10623824.
38. Bao L., Haas M., Kraus D.M., Hack B.K., Rakstang J.K., Holers V.M., et al. Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice. Journal of the American Society of Nephrology: JASN 2003, 14(3):670-679. Epub 2003/02/22. PubMed PMID: 12595503.
39. Taube C., Thurman J.M., Takeda K., Joetham A., Miyahara N., Carroll M.C., et al. Factor B of the alternative complement pathway regulates development of airway hyperresponsiveness and inflammation. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(21):8084-8089. doi: 0602357103 [pii]10.1073/pnas.0602357103. Epub 2006/05/17. PubMed PMID: 16702544; PubMed Central PMCID: PMC1472433.
40. Banda N.K., Thurman J.M., Kraus D., Wood A., Carroll M.C., Arend W.P., et al. Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis. Journal of Immunology 2006, 177(3):1904-1912. doi: 177/3/1904[pii]. Epub 2006/07/20. PubMed PMID: 16849503.
41. Hietala M.A., Jonsson I.M., Tarkowski A., Kleinau S., Pekna M. Complement deficiency ameliorates collagen-induced arthritis in mice. Journal of Immunology 2002, 169(1):454-459. Epub 2002/06/22. PubMed PMID: 12077276.
42. Morgan B.P., Harris C.L. Complement therapeutics; history and current progress. Molecular Immunology 2003, 40(2-4):159-170. PubMed PMID: 12914822.
43. Qu H., Ricklin D., Lambris J.D. Recent developments in low molecular weight complement inhibitors. Molecular Immunology 2009, 47(2-3):185-195. doi: 10.1016/j.molimm.2009.08.032. Epub 2009/10/06. PubMed PMID: 19800693; PubMed Central PMCID: PMC2788007.
44. Emlen W., Li W., Kirschfink M. Therapeutic complement inhibition: new developments. Seminars in Thrombosis and Hemostasis 2010, 36(6):660-668. doi: 10.1055/s-0030-1262888. Epub 2010/09/25. PubMed PMID: 20865643.
45. Hu X., Tomlinson S., Barnum S.R. Targeted inhibition of complement using complement receptor 2-conjugated inhibitors attenuates EAE. Neuroscience letters 2012, doi: 10.1016/j.neulet.2012.10.012. Epub 2012/10/20. PubMed PMID: 23079547.
46. Song H., He C., Knaak C., Guthridge J.M., Holers V.M., Tomlinson S. Complement receptor 2-mediated targeting of complement inhibitors to sites of complement activation. The Journal of Clinical Investigation 2003, 111(12):1875-1885. doi: 10.1172/JCI17348. Epub 2003/06/19. PubMed PMID: 12813023; PubMed Central PMCID: PMC161422.
47. Huang Y., Qiao F., Atkinson C., Holers V.M., Tomlinson S. A novel targeted inhibitor of the alternative pathway of complement and its therapeutic application in ischemia/reperfusion injury. Journal of Immunology 2008, 181(11):8068-8076. doi: 181/11/8068[pii]. Epub 2008/11/20. PubMed PMID: 19017999.