Complement component 5 contributes to poor disease outcome in humans and mice with pneumococcal meningitis

Journal of Clinical Investigation

Volumn 121, Issue 10, 2011, Pages 3943-3953

  Woehrl, Bianca ^a   Brouwer, Matthijs C ^b,c   Murr, Carmen ^a   Heckenberg, Sebastiaan G B ^b   Baas, Frank ^c   Pfister, Hans W ^a   Zwinderman, Aeilko H ^c   Paul Morgan, B ^d   Barnum, Scott R ^e   Van Ende, Arie Der ^c   Koedel, Uwe ^a,c   Van De Beek, Diederik ^b,c  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^e University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTRIAXONE; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5 ANTIBODY; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; DEXAMETHASONE; MONOCLONAL ANTIBODY; RECEPTOR ANTIBODY; TOLL LIKE RECEPTOR 2 ANTIBODY; TOLL LIKE RECEPTOR 4 ANTIBODY; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; C3 PLANT; CEREBROSPINAL FLUID; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PNEUMOCOCCAL MENINGITIS; PRIORITY JOURNAL; PROGNOSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AGED; ANIMALS; ANTIBODIES, MONOCLONAL; ARVICOLINAE; BRAIN; COHORT STUDIES; COMPLEMENT C5; DISEASE MODELS, ANIMAL; FEMALE; GENETIC ASSOCIATION STUDIES; HUMANS; MALE; MENINGITIS, PNEUMOCOCCAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROGNOSIS; PROSPECTIVE STUDIES; RECEPTOR, ANAPHYLATOXIN C5A;

EID: 80053419939     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI57522     Document Type: Article

References (60)

1. Brouwer MC, Tunkel AR, van de Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin Microbiol Rev. 2010;23(3):467-492.
2. van de Beek D, De Gans J, Tunkel AR, Wijdicks EF. Community-acquired bacterial meningitis in adults. N Engl J Med. 2006;354(1):44-53. (Pubitemid 43048950)
3. van de Beek D, De Gans J, Spanjaard L, Weisfelt M, Reitsma JB, Vermeulen M. Clinical features and prognostic factors in adults with bacterial meningitis. N Engl J Med. 2004;351(18):1849-1859.
4. Tauber MG, Khayam-Bashi H, Sande MA. Effects of ampicillin and corticosteroids on brain water content, cerebrospinal fluid pressure, and cerebrospinal fluid lactate levels in experimental pneumococcal meningitis. J Infect Dis. 1985;151(3):528-534. (Pubitemid 15103807)
5. De Gans J, van de Beek D. Dexamethasone in adults with bacterial meningitis. N Engl J Med. 2002;347(20):1549-1556. (Pubitemid 35315835)
6. van de Beek D, De Gans J. Dexamethasone in adults with community-acquired bacterial meningitis. Drugs. 2006;66(4):415-427.
7. van de Beek D, et al. Adjunctive dexamethasone in bacterial meningitis: a meta-analysis of individual patient data. Lancet Neurol. 2010;9(3):254-263.
8. Brouwer MC, McIntyre P, De Gans J, Prasad K, van de Beek D. Corticosteroids for acute bacterial meningitis. Cochrane Database Syst Rev. 2010;(9):CD004405.
9. Brouwer MC, Heckenberg SG, De Gans J, Spanjaard L, Reitsma JB, van de Beek D. Nationwide implementation of adjunctive dexamethasone therapy for pneumococcal meningitis. Neurology. 2010;75(17):1533-1539.
10. Hamburg MA, Collins FS. The path to personalized medicine. N Engl J Med. 2010;363(4):301-304.
11. Brouwer MC, De Gans J, Heckenberg SG, Zwinderman AH, van der Poll T, van de Beek D. Host genetic susceptibility to pneumococcal and meningococcal disease: a systematic review and meta-analysis. Lancet Infect Dis. 2009;9(1):31-44.
12. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010;11(9):785-797.
13. Jönsson G, Truedsson L, Sturfelt G, Oxelius VA, Braconier JH, Sjöholm AG. Hereditary C2 deficiency in Sweden: frequent occurrence of invasive infection, atherosclerosis, and rheumatic disease. Medicine (Baltimore). 2005;84(1):23-34. (Pubitemid 40130182)
14. Sprong T, et al. Deficient alternative complement pathway activation due to factor D deficiency by 2 novel mutations in the complement factor D gene in a family with meningococcal infections. Blood. 2006;107(12):4865-4870. (Pubitemid 43882639)
15. Biesma DH, et al. A family with complement factor D deficiency. J Clin Invest. 2001;108(2):233-240. (Pubitemid 32656247)
16. Fijen CA, et al. Properdin deficiency: molecular basis and disease association. Mol Immunol. 1999;36(13-14):863-867. (Pubitemid 30100838)
17. Haralambous E, et al. Factor H, a regulator of complement activity, is a major determinant of meningococcal disease susceptibility in UK Caucasian patients. Scand J Infect Dis. 2006;38(9):764-771. (Pubitemid 44304965)
18. Davila S, et al. Genome-wide association study identifies variants in the CFH region associated with host susceptibility to meningococcal disease. Nat Genet. 2010;42(9):772-776.
19. Tuomanen E, Hengstler B, Zak O, Tomasz A. The role of complement in inflammation during experimental pneumococcal meningitis. Microb Pathog. 1986;1(1):15-32. (Pubitemid 16004448)
20. Paul R, et al. Myeloid Src kinases regulate phagocytosis and oxidative burst in pneumococcal meningitis by activating NADPH oxidase. J Leukoc Biol. 2008;84(4):1141-1150.
21. Rupprecht TA, et al. Complement C1q and C3 are critical for the innate immune response to Streptococcus pneumoniae in the central nervous system. J Immunol. 2007;178(3):1861-1869. (Pubitemid 46154659)
22. Gardner P. Clinical practice. Prevention of meningococcal disease. N Engl J Med. 2006;355(14):1466-1473. (Pubitemid 44511561)
23. Jennett B, Teasdale G, Braakman R, Minderhoud J, Knill-Jones R. Predicting outcome in individual patients after severe head injury. Lancet. 1976;1(7968):1031-1034.
24. Weisfelt M, van de Beek D, Spanjaard L, Reitsma JB, De Gans J. Clinical features, complications, and outcome in adults with pneumococcal meningitis: a prospective case series. Lancet Neurol. 2006;5(2):123-129. (Pubitemid 43107848)
25. Koedel U, et al. Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog. 2009;5(5):e1000461.
26. Brown JS, et al. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc Natl Acad Sci U S A. 2002;99(26):16969-16974. (Pubitemid 36034082)
27. Koedel U, Klein M, Pfister HW. New understandings on the pathophysiology of bacterial meningitis. Curr Opin Infect Dis. 2010;23(3):217-223.
28. Boos L, Campbell IL, Ames R, Wetsel RA, Barnum SR. Deletion of the complement anaphylatoxin C3a receptor attenuates, whereas ectopic expression of C3a in the brain exacerbates, experimental autoimmune encephalomyelitis. J Immunol. 2004;173(7):4708-4714. (Pubitemid 39280706)
29. Klein M, et al. Innate immunity to pneumococcal infection of the central nervous system depends on toll-like receptor (TLR) 2 and TLR4. J Infect Dis. 2008;198(7):1028-1036.
30. Tunkel AR, et al. Practice guidelines for the management of bacterial meningitis. Clin Infect Dis. 2004;39(9):1267-1284. (Pubitemid 39458512)
31. Armstrong PW, et al. Pexelizumab for acute ST-elevation myocardial infarction in patients undergoing primary percutaneous coronary intervention: a randomized controlled trial. JAMA. 2007;297(1):43-51.
32. Hillmen P, et al. The complement inhibitor eculizumab in paroxysmal nocturnal hemoglobinuria. N Engl J Med. 2006;355(12):1233-1243. (Pubitemid 44427447)
33. Weisfelt M, van de Beek D, Spanjaard L, Reitsma JB, De Gans J. Attenuated cerebrospinal fluid leukocyte count and sepsis in adults with pneumococcal meningitis: a prospective cohort study. BMC Infect Dis. 2006;6:149.
34. Giampaolo C, Scheld M, Boyd J, Savory J, Sande M, Wills M. Leukocyte and bacterial interrelationships in experimental meningitis. Ann Neurol. 1981;9(4):328-333. (Pubitemid 11106548)
35. Tauber MG, Kennedy SL, Tureen JH, Lowenstein DH. Experimental pneumococcal meningitis causes central nervous system pathology without inducing the 72-kd heat shock protein. Am J Pathol. 1992;141(1):53-60.
36. Tortajada A, Montes T, Martinez-Barricarte R, Morgan BP, Harris CL, De Cordoba SR. The disease-protective complement factor H allotypic variant Ile62 shows increased binding affinity for C3b and enhanced cofactor activity. Hum Mol Genet. 2009;18(18):3452-3461.
37. Goicoechea de JE, et al. Gain-of-function mutations in complement factor B are associated with atypical hemolytic uremic syndrome. Proc Natl Acad Sci U S A. 2007;104(1):240-245.
38. Hillebrandt S, et al. Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nat Genet. 2005;37(8):835-843. (Pubitemid 41077109)
39. Gressner O, et al. Gc-globulin concentrations and C5 haplotype-tagging polymorphisms contribute to variations in serum activity of complement factor C5. Clin Biochem. 2007;40(11):771-775. (Pubitemid 46961957)
40. Ernst JD, Hartiala KT, Goldstein IM, Sande MA. Complement (C5)-derived chemotactic activity accounts for accumulation of polymorphonuclear leukocytes in cerebrospinal fluid of rabbits with pneumococcal meningitis. Infect Immun. 1984;46(1):81-86. (Pubitemid 14047199)
41. Kadurugamuwa JL, Hengstler B, Bray MA, Zak O. Inhibition of complement-factor-5a-induced inflammatory reactions by prostaglandin E2 in experimental meningitis. J Infect Dis. 1989;160(4):715-719. (Pubitemid 19247658)
42. Tuomanen EI, Saukkonen K, Sande S, Cioffe C, Wright SD. Reduction of inflammation, tissue damage, and mortality in bacterial meningitis in rabbits treated with monoclonal antibodies against adhesion-promoting receptors of leukocytes. J Exp Med. 1989;170(3):959-969. (Pubitemid 19226676)
43. Ritis K, et al. A novel C5a receptor-tissue factor cross-talk in neutrophils links innate immunity to coagulation pathways. J Immunol. 2006;177(7):4794-4802. (Pubitemid 44469814)
44. Markiewski MM, Nilsson B, Ekdahl KN, Mollnes TE, Lambris JD. Complement and coagulation: strangers or partners in crime? Trends Immunol. 2007;28(4):184-192. (Pubitemid 46476881)
45. Leung LL, Myles T, Nishimura T, Song JJ, Robinson WH. Regulation of tissue inflammation by thrombin- activatable carboxypeptidase B (or TAFI). Mol Immunol. 2008;45(16):4080-4083.
46. Vergouwen MD, Schut ES, Troost D, van de Beek D. Diffuse cerebral intravascular coagulation and cerebral infarction in pneumococcal meningitis. Neurocrit Care. 2010;13(2):217-227.
47. Kastenbauer S, Pfister HW. Pneumococcal meningitis in adults: spectrum of complications and prognostic factors in a series of 87 cases. Brain. 2003;126(pt 5):1015-1025. (Pubitemid 36522945)
48. Jacob A, Hack B, Chiang E, Garcia JG, Quigg RJ, Alexander JJ. C5a alters blood-brain barrier integrity in experimental lupus. FASEB J. 2010;24(6):1682-1688.
49. Liu ZM, et al. Silencing of C5a receptor gene with siRNA for protection from Gram-negative bacterial lipopolysaccharide-induced vascular permeability. Mol Immunol. 2010;47(6):1325-1333.
50. Farkas I, Baranyi L, Liposits ZS, Yamamoto T, Okada H. Complement C5a anaphylatoxin fragment causes apoptosis in TGW neuroblastoma cells. NeuroScience. 1998;86(3):903-911. (Pubitemid 28298745)
51. Yanamadala V, Friedlander RM. Complement in neuroprotection and neurodegeneration. Trends Mol Med. 2010;16(2):69-76.
52. Sprong T, et al. Inhibition of C5a-induced inflammation with preserved C5b-9-mediated bactericidal activity in a human whole blood model of meningococcal sepsis. Blood. 2003;102(10):3702-3710. (Pubitemid 37409391)
53. Brouwer MC, Read RC, van de Beek D. Host genetics and outcome in meningococcal disease: a systematic review and meta-analysis. Lancet Infect Dis. 2010;10(4):262-274.
54. Woodruff TM, et al. Antiarthritic activity of an orally active C5a receptor antagonist against antigeninduced monarticular arthritis in the rat. Arthritis Rheum. 2002;46(9):2476-2485.
55. Vergunst CE, et al. Blocking the receptor for C5a in patients with rheumatoid arthritis does not reduce synovial inflammation. Rheumatology (Oxford). 2007;46(12):1773-1778. (Pubitemid 350168291)
56. Osmers I, Szalai AJ, Tenner AJ, Barnum SR. Complement in BuB/BnJ mice revisited: serum C3 levels and complement opsonic activity are not elevated. Mol Immunol. 2006;43(10):1722-1725.
57. Malipiero U, et al. TGFbeta receptor II gene deletion in leucocytes prevents cerebral vasculitis in bacterial meningitis. Brain. 2006;129(pt 9):2404-2415. (Pubitemid 44522125)
58. Huugen D, et al. Inhibition of complement factor C5 protects against anti-myeloperoxidase antibody-mediated glomerulonephritis in mice. Kidney Int. 2007;71(7):646-654. (Pubitemid 46494558)
59. De Vries B, Matthijsen RA, Wolfs TG, van Bijnen AA, Heeringa P, Buurman WA. Inhibition of complement factor C5 protects against renal ischemia-reperfusion injury: inhibition of late apoptosis and inflammation. Transplantation. 2003;75(3):375-382. (Pubitemid 36222966)
60. Kastenbauer S, Koedel U, Becker BF, Pfister HW. Oxidative stress in bacterial meningitis in humans. Neurology. 2002;58(2):186-191. (Pubitemid 34084206)