A recombinant vaccine effectively induces C5a-specific neutralizing antibodies and prevents arthritis

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Nandakumar, Kutty Selva ^a,b   Jansson, Åsa ^c   Xu, Bingze ^c   Rydell, Niclas ^c,e   Blom, Anna M ^d   Holmdahl, Rikard ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c Resistentia Pharmaceuticals AB   (Sweden)

^d LUND UNIVERSITY   (Sweden)

^e Thermo Fisher Scientific   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN ANTIBODY; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5B; COMPLEMENT MEMBRANE ATTACK COMPLEX; HYBRID PROTEIN; MALTOSE BINDING PROTEIN; MBP C5A; NEUTRALIZING ANTIBODY; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTHRITIS; ARTICLE; ASSAY; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE CONSTRUCT; GENETIC TRANSFECTION; HISTOLOGY; IMMUNE RESPONSE; IMMUNITY; INCIDENCE; INFLAMMATION; INFLAMMATORY DISEASE; LEUKEMIA CELL LINE; MALE; MAST CELL LEUKEMIA; MORPHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; VACCINATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL LINE; IMMUNOLOGY; METABOLISM; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MUS; RATTUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ARTHRITIS; BASE SEQUENCE; CELL LINE; COMPLEMENT C5A; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICE; MICE, INBRED BALB C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VACCINES, SYNTHETIC;

EID: 78149426505     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013511     Document Type: Article

References (54)

1. Monk PN, Scola AM, Madala P, Fairlie DP (2007) Function, structure and therapeutic potential of complement C5a receptors. Br J Pharmacol 152: 429-448.
2. Gasque P, Dean YD, McGreal EP, VanBeek J, Morgan BP (2000) Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 49: 171-186.
3. Markiewski MM, Deangelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, et al. (2008) Modulation of the antitumor immune response by complement. Nat Immunol 9: 1225-1235.
4. Hawlisch H, Belkaid Y, Baelder R, Hildeman D, Gerard C, et al. (2005) C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 22: 415-426.
5. Walport MJ (2001) Complement. First of two parts. N Engl J Med 344: 1058-1066.
6. Fischetti F, Durigutto P, Macor P, Marzari R, Carretta R, et al. (2007) Selective therapeutic control of C5a and the terminal complement complex by anti-C5 single-chain Fv in an experimental model of antigen-induced arthritis in rats. Arthritis Rheum 56: 1187-1197.
7. Sahu A, Lambris JD (2001) Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol Rev 180: 35-48.
8. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, et al. (2006) Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med 12: 682-687.
9. Guo RF, Ward PA (2005) Role of C5a in inflammatory responses. Annu Rev Immunol 23: 821-852.
10. Hawlisch H, Kohl J (2006) Complement and Toll-like receptors: key regulators of adaptive immune responses. Mol Immunol 43: 13-21.
11. Kohl J, Baelder R, Lewkowich IP, Pandey MK, Hawlisch H, et al. (2006) A regulatory role for the C5a anaphylatoxin in type 2 immunity in asthma. J Clin Invest 116: 783-796.
12. Kohl J (2001) Anaphylatoxins and infectious and non-infectious inflammatory diseases. Mol Immunol 38: 175-187.
13. Sprong T, Brandtzaeg P, Fung M, Pharo AM, Hoiby EA, et al. (2003) Inhibition of C5a-induced inflammation with preserved C5b-9-mediated bactericidal activity in a human whole blood model of meningococcal sepsis. Blood 102: 3702-3710.
14. Monach PA, Benoist C, Mathis D (2004) The role of antibodies in mouse models of rheumatoid arthritis, and relevance to human disease. Adv Immunol 82: 217-248.
15. Nandakumar KS, Holmdahl R (2006) Antibody-induced arthritis: disease mechanisms and genes involved at the effector phase of arthritis. Arthritis Res Ther 8: 223.
16. Uysal H, Bockermann R, Nandakumar KS, Sehnert B, Bajtner E, et al. (2009) Structure and pathogenicity of antibodies specific for citrullinated collagen type II in experimental arthritis. J Exp Med 206: 449-462.
17. Nandakumar KS (2010) Pathogenic antibody recognition of cartilage. Cell Tissue Res 339: 213-220.
18. Wang Y, Kristan J, Hao L, Lenkoski CS, Shen Y, et al. (2000) A role for complement in antibody-mediated inflammation: C5-deficient DBA/1 mice are resistant to collagen-induced arthritis. J Immunol 164: 4340-4347.
19. Dzhambazov B, Nandakumar KS, Kihlberg J, Fugger L, Holmdahl R, et al. (2006) Therapeutic vaccination of active arthritis with a glycosylated collagen type II peptide in complex with MHC class II molecules. J Immunol 176: 1525-1533.
20. Ricklin D, Lambris JD (2007) Complement-targeted therapeutics. Nat Biotechnol 25: 1265-1275.
21. Wagner E, Frank MM (2009) Therapeutic potential of complement modulation. Nat Rev Drug Discov 9: 43-56.
22. Blom AM, Nandakumar KS, Holmdahl R (2009) C4b-binding protein (C4BP) inhibits development of experimental arthritis in mice. Ann Rheum Dis 68: 136-142.
23. Hietala MA, Nandakumar KS, Persson L, Fahlen S, Holmdahl R, et al. (2004) Complement activation by both classical and alternative pathways is critical for the effector phase of arthritis. Eur J Immunol 34: 1208-1216.
24. Banda NK, Thurman JM, Kraus D, Wood A, Carroll MC, et al. (2006) Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis. J Immunol 177: 1904-1912.
25. Banda NK, Levitt B, Wood AK, Takahashi K, Stahl GL, et al. (2010) Complement activation pathways in murine immune complex-induced arthritis and in C3a and C5a generation in vitro. Clin Exp Immunol 159: 100-108.
26. Trouw LA, Bengtsson AA, Gelderman KA, Dahlback B, Sturfelt G, et al. (2007) C4b-binding protein and factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. J Biol Chem 282: 28540-28548.
27. Sjoberg A, Onnerfjord P, Morgelin M, Heinegard D, Blom AM (2005) The extracellular matrix and inflammation: fibromodulin activates the classical pathway of complement by directly binding C1q. J Biol Chem 280: 32301-32308.
28. Wetsel RA, Kolb WP (1983) Expression of C5a-like biological activities by the fifth component of human complement (C5) upon limited digestion with noncomplement enzymes without release of polypeptide fragments. J Exp Med 157: 2029-2048.
29. Ward PA, Hill JH (1970) C5 chemotactic fragments produced by an enzyme in lysosomal granules of neutrophils. J Immunol 104: 535-543.
30. Huber-Lang M, Younkin EM, Sarma JV, Riedemann N, McGuire SR, et al. (2002) Generation of C5a by phagocytic cells. Am J Pathol 161: 1849-1859.
31. Gerard NP, Gerard C (1991) The chemotactic receptor for human C5a anaphylatoxin. Nature 349: 614-617.
32. Grant EP, Picarella D, Burwell T, Delaney T, Croci A, et al. (2002) Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J Exp Med 196: 1461-1471.
33. Shushakova N, Skokowa J, Schulman J, Baumann U, Zwirner J, et al. (2002) C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J Clin Invest 110: 1823-1830.
34. Konrad S, Ali SR, Wiege K, Syed SN, Engling L, et al. (2008) PI3Kgamma and PI3Kdelta: Linkers of coordinate C5aR-FcgammaR activation and immune complex-induced inflammation. J Biol Chem 283: 33296-33303.
35. Konrad S, Engling L, Schmidt RE, Gessner JE (2007) Characterization of the murine Fcgamma RIII and Fcgamma RIIB gene promoters: A single twonucleotide difference determines their inverse responsiveness to C5A. J Biol Chem 282: 37906-37912.
36. Huber-Lang MS, Riedeman NC, Sarma JV, Younkin EM, McGuire SR, et al. (2002) Protection of innate immunity by C5aR antagonist in septic mice. Faseb J 16: 1567-1574.
37. Woodruff TM, Strachan AJ, Dryburgh N, Shiels IA, Reid RC, et al. (2002) Antiarthritic activity of an orally active C5a receptor antagonist against antigeninduced monarticular arthritis in the rat. Arthritis Rheum 46: 2476-2485.
38. Woodruff TM, Crane JW, Proctor LM, Buller KM, Shek AB, et al. (2006) Therapeutic activity of C5a receptor antagonists in a rat model of neurodegeneration. FASEB J 20: 1407-1417.
39. Vergunst CE, Gerlag DM, Dinant H, Schulz L, Vinkenoog M, et al. (2007) Blocking the receptor for C5a in patients with rheumatoid arthritis does not reduce synovial inflammation. Rheumatology (Oxford) 46: 1773-1778.
40. Kohl J (2006) Drug evaluation: the C5a receptor antagonist PMX-53. Curr Opin Mol Ther 8: 529-538.
41. Rittirsch D, Flierl MA, Nadeau BA, Day DE, Huber-Lang M, et al. (2008) Functional roles for C5a receptors in sepsis. Nat Med 14: 551-557.
42. Andersson U, Erlandsson-Harris H (2004) HMGB1 is a potent trigger of arthritis. J Intern Med 255: 344-350.
43. Czermak BJ, Sarma V, Pierson CL, Warner RL, Huber-Lang M, et al. (1999) Protective effects of C5a blockade in sepsis. Nat Med 5: 788-792.
44. Hoesel LM, Niederbichler AD, Schaefer J, Ipaktchi KR, Gao H, et al. (2007) C5a-blockade improves burn-induced cardiac dysfunction. J Immunol 178: 7902-7910.
45. Ji H, Ohmura K, Mahmood U, Lee DM, Hofhuis FM, et al. (2002) Arthritis critically dependent on innate immune system players. Immunity 16: 157-168.
46. Lee H, Zahra D, Vogelzang A, Newton R, Thatcher J, et al. (2006) Human C5aR knock-in mice facilitate the production and assessment of anti-inflammatory monoclonal antibodies. Nat Biotechnol 24: 1279-1284.
47. Allegretti M, Moriconi A, Beccari AR, Di Bitondo R, Bizzarri C, et al. (2005) Targeting C5a: recent advances in drug discovery. Curr Med Chem 12: 217-236.
48. Thomas TC, Rollins SA, Rother RP, Giannoni MA, Hartman SL, et al. (1996) Inhibition of complement activity by humanized anti-C5 antibody and singlechain Fv. Mol Immunol 33: 1389-1401.
49. Nandakumar KS, Holmdahl R (2008) Therapeutic cleavage of IgG: new avenues for treating inflammation. Trends Immunol 29: 173-178.
50. Lindqvist AK, Johannesson M, Johansson AC, Nandakumar KS, Blom AM, et al. (2006) Backcross and partial advanced intercross analysis of nonobese diabetic gene-mediated effects on collagen-induced arthritis reveals an interactive effect by two major loci. J Immunol 177: 3952-3959.
51. Holmdahl R, Rubin K, Klareskog L, Larsson E, Wigzell H (1986) Characterization of the antibody response in mice with type II collagen-induced arthritis, using monoclonal anti-type II collagen antibodies. Arthritis Rheum 29: 400-410.
52. Schulte S, Unger C, Mo JA, Wendler O, Bauer E, et al. (1998) Arthritis-related B cell epitopes in collagen II are conformation-dependent and sterically privileged in accessible sites of cartilage collagen fibrils. J Biol Chem 273: 1551-1561.
53. Holmdahl R, Carlsen S, Mikulowska A, Vestberg M, Brunsberg U, et al. (1998) Genetic analysis of mouse models for rheumatoid arthritis. In: Adolph KW, ed. Human Genome methods. New York: CRC Press. pp 215-238.
54. Holmdahl R, Klareskog L, Andersson M, Hansen C (1986) High antibody response to autologous type II collagen is restricted to H-2q. Immunogenetics 24: 84-89.