C3a receptor deficiency accelerates the onset of renal injury in the MRL/lpr mouse

Molecular Immunology

Volumn 46, Issue 7, 2009, Pages 1397-1404

  Wenderfer, Scott E ^a   Wang, Hongyu ^a   Ke, Baozhen ^a   Wetsel, Rick A ^a   Braun, Michael C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Complement; Systemic lupus erythematosus; Transgenic knockout mice

Indexed keywords

AUTOANTIBODY; CHEMOKINE; CHEMOKINE RECEPTOR; COMPLEMENT COMPONENT C3A; COMPLEMENT RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOPATHOGENESIS; KIDNEY INJURY; KNOCKOUT MOUSE; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; DISEASE PROGRESSION; GENETIC PREDISPOSITION TO DISEASE; LUPUS NEPHRITIS; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, KNOCKOUT; RECEPTORS, COMPLEMENT; SURVIVAL ANALYSIS; TIME FACTORS;

MUS;

EID: 62549118640     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.12.004     Document Type: Article

References (70)

1. Acosta-Rodriguez E.V., Rivino L., Geginat J., Jarrossay D., Gattorno M., Lanzavecchia A., Sallusto F., and Napolitani G. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8 (2007) 639-646
2. Adalid-Peralta L., Mathian A., Tran T., Delbos L., Durand-Gasselin I., Berrebi D., Peuchmaur M., Couderc J., Emilie D., and Koutouzov S. Leukocytes and the kidney contribute to interstitial inflammation in lupus nephritis. Kidney Int. 73 (2008) 172-180
3. Addis-Lieser E., Kohl J., and Chiaramonte M.G. Opposing regulatory roles of complement factor 5 in the development of bleomycin-induced pulmonary fibrosis. J. Immunol. 175 (2005) 1894-1902
4. Ahamed J., Venkatesha R.T., Thangam E.B., and Ali H. C3a enhances nerve growth factor-induced nfat activation and chemokine production in a human mast cell line, hmc-1. J. Immunol. 172 (2004) 6961-6968
5. Ames R.S., Lee D., Foley J.J., Jurewicz A.J., Tornetta M.A., Bautsch W., Settmacher B., Klos A., Erhard K.F., Cousins R.D., Sulpizio A.C., Hieble J.P., McCafferty G., Ward K.W., Adams J.L., Bondinell W.E., Underwood D.C., Osborn R.R., Badger A.M., and Sarau H.M. Identification of a selective nonpeptide antagonist of the anaphylatoxin c3a receptor that demonstrates antiinflammatory activity in animal models. J. Immunol. 166 (2001) 6341-6348
6. Andrews B.S., Eisenberg R.A., Theofilopoulos A.N., Izui S., Wilson C.B., McConahey P.J., Murphy E.D., Roths J.B., and Dixon F.J. Spontaneous murine lupus-like syndromes, clinical and immunopathological manifestations in several strains. J. Exp. Med. 148 (1978) 1198-1215
7. Arnold C.N., Campbell D.J., Lipp M., and Butcher E.C. The germinal center response is impaired in the absence of T cell-expressed Cxcr5. Eur. J. Immunol. 37 (2007) 100-109
8. Baelder R., Fuchs B., Bautsch W., Zwirner J., Kohl J., Hoymann H.G., Glaab T., Erpenbeck V., Krug N., and Braun A. Pharmacological targeting of anaphylatoxin receptors during the effector phase of allergic asthma suppresses airway hyperresponsiveness and airway inflammation. J. Immunol. 174 (2005) 783-789
9. Balomenos D., Rumold R., and Theofilopoulos A.N. Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J. Clin. Invest. 101 (1998) 364-371
10. Bao L., Osawe I., Haas M., and Quigg R.J. Signaling through up-regulated c3a receptor is key to the development of experimental lupus nephritis. J. Immunol. 175 (2005) 1947-1955
11. Bao L., Zhou J., Holers V.M., and Quigg R.J. Excessive matrix accumulation in the kidneys of MRL/lpr lupus mice is dependent on complement activation. J. Am. Soc. Nephrol. 14 (2003) 2516-2525
12. Bautsch W., Hoymann H.G., Zhang Q., Meier-Wiedenbach I., Raschke U., Ames R.S., Sohns B., Flemme N., Meyer zu Vilsendorf A., Grove M., Klos A., and Kohl J. Cutting edge: Guinea pigs with a natural C3a-receptor defect exhibit decreased bronchoconstriction in allergic airway disease: evidence for an involvement of the c3a anaphylatoxin in the pathogenesis of asthma. J. Immunol. 165 (2000) 5401-5405
13. Boor P., Konieczny A., Villa L., Schult A.L., Bucher E., Rong S., Kunter U., van Roeyen C.R., Polakowski T., Hawlisch H., Hillebrandt S., Lammert F., Eitner F., Floege J., and Ostendorf T. Complement c5 mediates experimental tubulointerstitial fibrosis. J. Am. Soc. Nephrol. 18 (2007) 1508-1515
14. Braun M.C., Reins R.Y., Li T.B., Hollmann T.J., Dutta R., Rick W.A., Teng B.B., and Ke B. Renal expression of the c3a receptor and functional responses of primary human proximal tubular epithelial cells. J. Immunol. 173 (2004) 4190-4196
15. Cosmi L., Annunziato F., Maggi E., Romagnani S., and Manetti R. Chemoattractant receptors expressed on type 2 T cells and their role in disease. Int. Arch. Allergy Immunol. 125 (2001) 273-279
16. Couser W.G., Baker P.J., and Adler S. Complement and the direct mediation of immune glomerular injury: a new perspective. Kidney Int. 28 (1985) 879-890
17. Davalos-Misslitz A.C., Rieckenberg J., Willenzon S., Worbs T., Kremmer E., Bernhardt G., and Forster R. Generalized multi-organ autoimmunity in ccr7-deficient mice. Eur. J. Immunol. 37 (2007) 613-622
18. Debes G.F., Arnold C.N., Young A.J., Krautwald S., Lipp M., Hay J.B., and Butcher E.C. Chemokine receptor ccr7 required for T lymphocyte exit from peripheral tissues. Nat. Immunol. 6 (2005) 889-894
19. Drouin S.M., Corry D.B., Hollman T.J., Kildsgaard J., and Wetsel R.A. Absence of the complement anaphylatoxin c3a receptor suppresses th2 effector functions in a murine model of pulmonary allergy. J. Immunol. 169 (2002) 5926-5933
20. Duan B., Niu H., Xu Z., Sharpe A.H., Croker B.P., Sobel E.S., and Morel L. Intrafollicular location of marginal zone/cd1d(hi) B cells is associated with autoimmune pathology in a mouse model of lupus. Lab. Invest. 88 (2008) 1008-1020
21. Fan X., Patera A.C., Pong-Kennedy A., Deno G., Gonsiorek W., Manfra D.J., Vassileva G., Zeng M., Jackson C., Sullivan L., Sharif-Rodriguez W., Opdenakker G., Van Damme J., Hedrick J.A., Lundell D., Lira S.A., and Hipkin R.W. Murine cxcr1 is a functional receptor for gcp-2/cxcl6 and interleukin-8/cxcl8. J. Biol. Chem. 282 (2007) 11658-11666
22. Fischer W.H., and Hugli T.E. Regulation of B cell functions by c3a and c3a(desarg): suppression of tnf-alpha, IL-6, and the polyclonal immune response. J. Immunol. 159 (1997) 4279-4286
23. Fischer W.H., Jagels M.A., and Hugli T.E. Regulation of il-6 synthesis in human peripheral blood mononuclear cells by c3a and c3a(desarg). J. Immunol. 162 (1999) 453-459
24. Grimm P.C., Nickerson P., Gough J., McKenna R., Stern E., Jeffery J., and Rush D.N. Computerized image analysis of sirius red-stained renal allograft biopsies as a surrogate marker to predict long-term allograft function. J. Am. Soc. Nephrol. 14 (2003) 1662-1668
25. Hardtke S., Ohl L., and Forster R. Balanced expression of cxcr5 and ccr7 on follicular T helper cells determines their transient positioning to lymph node follicles and is essential for efficient B-cell help. Blood 106 (2005) 1924-1931
26. Hicks J., and Bullard D.C. Review of autoimmune (lupus-like) glomerulonephritis in murine models. Ultrastruct. Pathol. 30 (2006) 345-359
27. Hollmann T.J., Mueller-Ortiz S.L., Braun M.C., and Wetsel R.A. Disruption of the c5a receptor gene increases resistance to acute Gram-negative bacteremia and endotoxic shock: opposing roles of c3a and c5a. Mol. Immunol. (2007)
28. Hopken U.E., Lu B., Gerard N.P., and Gerard C. The c5a chemoattractant receptor mediates mucosal defence to infection. Nature 383 (1996) 86-89
29. Humbles A.A., Lu B., Nilsson C.A., Lilly C., Israel E., Fujiwara Y., Gerard N.P., and Gerard C. A role for the c3a anaphylatoxin receptor in the effector phase of asthma. Nature 406 (2000) 998-1001
30. Jakubzick C., Tacke F., Llodra J., van Rooijen N., and Randolph G.J. Modulation of dendritic cell trafficking to and from the airways. J. Immunol. 176 (2006) 3578-3584
31. Kawamoto S., Yalcindag A., Laouini D., Brodeur S., Bryce P., Lu B., Humbles A.A., Oettgen H., Gerard C., and Geha R.S. The anaphylatoxin c3a downregulates the th2 response to epicutaneously introduced antigen. J. Clin. Invest. 114 (2004) 399-407
32. Kildsgaard J., Hollmann T.J., Matthews K.W., Bian K., Murad F., and Wetsel R.A. Cutting edge: targeted disruption of the c3a receptor gene demonstrates a novel protective anti-inflammatory role for c3a in endotoxin-shock. J. Immunol. 165 (2000) 5406-5409
33. Kirchhoff K., Weinmann O., Zwirner J., Begemann G., Gotze O., Kapp A., and Werfel T. Detection of anaphylatoxin receptors on cd83+ dendritic cells derived from human skin. Immunology 103 (2001) 210-217
34. Kocks J.R., Davalos-Misslitz A.C., Hintzen G., Ohl L., and Forster R. Regulatory T cells interfere with the development of bronchus-associated lymphoid tissue. J. Exp. Med. 204 (2007) 723-734
35. Kohl J., Baelder R., Lewkowich I.P., Pandey M.K., Hawlisch H., Wang L., Best J., Herman N.S., Sproles A.A., Zwirner J., Whitsett J.A., Gerard C., Sfyroera G., Lambris J.D., and Wills-Karp M. A regulatory role for the c5a anaphylatoxin in type 2 immunity in asthma. J. Clin. Invest. 116 (2006) 783-796
36. Kono D.H., and Theofilopoulos A.N. Genetics of systemic autoimmunity in mouse models of lupus. Int. Rev. Immunol. 19 (2000) 367-387
37. Kono D.H., and Theofilopoulos A.N. Genetics of SLE in mice. Springer Semin. Immunopathol. 28 (2006) 83-96
38. Liszewski M.K., Kahl L.E., and Atkinson J.P. The functional role of complement genes in systemic lupus erythematosus and Sjogren's syndrome. Curr. Opin. Rheumatol. 1 (1989) 347-352
39. Manderson A.P., Botto M., and Walport M.J. The role of complement in the development of systemic lupus erythematosus. Annu. Rev. Immunol. 22 (2004) 431-456
40. Mathieu M.C., Sawyer N., Greig G.M., Hamel M., Kargman S., Ducharme Y., Lau C.K., Friesen R.W., O'Neill G.P., Gervais F.G., and Therien A.G. The c3a receptor antagonist sb 290157 has agonist activity. Immunol. Lett. 100 (2005) 139-145
41. Melendi G.A., Hoffman S.J., Karron R.A., Irusta P.M., Laham F.R., Humbles A., Schofield B., Pan C.H., Rabold R., Thumar B., Thumar A., Gerard N.P., Mitzner W., Barnum S.R., Gerard C., Kleeberger S.R., and Polack F.P. C5 modulates airway hyperreactivity and pulmonary eosinophilia during enhanced respiratory syncytial virus disease by decreasing c3a receptor expression. J. Virol. 81 (2007) 991-999
42. Moepps B., Nuesseler E., Braun M., and Gierschik P. A homolog of the human chemokine receptor cxcr1 is expressed in the mouse. Mol. Immunol. 43 (2006) 897-914
43. Mueller-Ortiz S.L., Hollmann T.J., Haviland D.L., and Wetsel R.A. Ablation of the complement c3a anaphylatoxin receptor causes enhanced killing of Pseudomonas aeruginosa in a mouse model of pneumonia. Am. J. Physiol. Lung Cell Mol. Physiol. 291 (2006) L157-165
44. Nguyen C., Limaye N., and Wakeland E.K. Susceptibility genes in the pathogenesis of murine lupus. Arthritis Res. 4 Suppl. 3 (2002) S255-263
45. Nose M., Nishihara M., Kamogawa J., Terada M., and Nakatsuru S. Genetic basis of autoimmune disease in MRL/lpr mice: dissection of the complex pathological manifestations and their susceptibility loci. Rev. Immunogenet. 2 (2000) 154-164
46. Peake P.W., O'Grady S., Pussell B.A., and Charlesworth J.A. C3a is made by proximal tubular hk-2 cells and activates them via the c3a receptor. Kidney Int. 56 (1999) 1729-1736
47. Proctor L.M., Arumugam T.V., Shiels I., Reid R.C., Fairlie D.P., and Taylor S.M. Comparative anti-inflammatory activities of antagonists to c3a and c5a receptors in a rat model of intestinal ischaemia/reperfusion injury. Br. J. Pharmacol. 142 (2004) 756-764
48. Purwar R., Wittmann M., Zwirner J., Oppermann M., Kracht M., Dittrich-Breiholz O., Gutzmer R., and Werfel T. Induction of c3 and ccl2 by c3a in keratinocytes: a novel autocrine amplification loop of inflammatory skin reactions. J. Immunol. 177 (2006) 4444-4450
49. Qu C., Edwards E.W., Tacke F., Angeli V., Llodra J., Sanchez-Schmitz G., Garin A., Haque N.S., Peters W., van Rooijen N., Sanchez-Torres C., Bromberg J., Charo I.F., Jung S., Lira S.A., and Randolph G.J. Role of ccr8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J. Exp. Med. 200 (2004) 1231-1241
50. Riedemann N.C., Guo R.F., Hollmann T.J., Gao H., Neff T.A., Reuben J.S., Speyer C.L., Sarma J.V., Wetsel R.A., Zetoune F.S., and Ward P.A. Regulatory role of c5a in lps-induced il-6 production by neutrophils during sepsis. FASEB J. 18 (2004) 370-372
51. Rossi D.L., Hurst S.D., Xu Y., Wang W., Menon S., Coffman R.L., and Zlotnik A. Lungkine, a novel cxc chemokine, specifically expressed by lung bronchoepithelial cells. J. Immunol. 162 (1999) 5490-5497
52. Sakai N., Wada T., Yokoyama H., Lipp M., Ueha S., Matsushima K., and Kaneko S. Secondary lymphoid tissue chemokine (slc/ccl21)/ccr7 signaling regulates fibrocytes in renal fibrosis. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 14098-14103
53. Sayah S., Jauneau A.C., Patte C., Tonon M.C., Vaudry H., and Fontaine M. Two different transduction pathways are activated by c3a and c5a anaphylatoxins on astrocytes. Brain Res. Mol. Brain Res. 112 (2003) 53-60
54. Schraufstatter I.U., Trieu K., Sikora L., Sriramarao P., and DiScipio R. Complement c3a and c5a induce different signal transduction cascades in endothelial cells. J. Immunol. 169 (2002) 2102-2110
55. Schutyser E., Struyf S., and Van Damme J. The cc chemokine ccl20 and its receptor ccr6. Cytokine Growth Factor Rev. 14 (2003) 409-426
56. Schwarting A., Tesch G., Kinoshita K., Maron R., Weiner H.L., and Kelley V.R. Il-12 drives IFN-gamma-dependent autoimmune kidney disease in MRL-fas(lpr) mice. J. Immunol. 163 (1999) 6884-6891
57. Sekine H., Reilly C.M., Molano I.D., Garnier G., Circolo A., Ruiz P., Holers V.M., Boackle S.A., and Gilkeson G.S. Complement component c3 is not required for full expression of immune complex glomerulonephritis in MRL/lpr mice. J. Immunol. 166 (2001) 6444-6451
58. Settmacher B., Bock D., Saad H., Gartner S., Rheinheimer C., Kohl J., Bautsch W., and Klos A. Modulation of c3a activity: internalization of the human c3a receptor and its inhibition by c5a. J. Immunol. 162 (1999) 7409-7416
59. Steinmetz O.M., Velden J., Kneissler U., Marx M., Klein A., Helmchen U., Stahl R.A., and Panzer U. Analysis and classification of B-cell infiltrates in lupus and anca-associated nephritis. Kidney Int. 74 (2008) 448-457
60. Takahashi S., Fossati L., Iwamoto M., Merino R., Motta R., Kobayakawa T., and Izui S. Imbalance towards th1 predominance is associated with acceleration of lupus-like autoimmune syndrome in MRL mice. J. Clin. Invest. 97 (1996) 1597-1604
61. Tsuji R.F., Kawikova I., Ramabhadran R., Akahira-Azuma M., Taub D., Hugli T.E., Gerard C., and Askenase P.W. Early local generation of c5a initiates the elicitation of contact sensitivity by leading to early T cell recruitment. J. Immunol. 165 (2000) 1588-1598
62. Varona R., Villares R., Carramolino L., Goya I., Zaballos A., Gutierrez J., Torres M., Martinez A.C., and Marquez G. Ccr6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J. Clin. Invest. 107 (2001) R37-45
63. Venkatesha R.T., Berla Thangam E., Zaidi A.K., and Ali H. Distinct regulation of c3a-induced mcp-1/ccl2 and rantes/ccl5 production in human mast cells by extracellular signal regulated kinase and pi3 kinase. Mol. Immunol. 42 (2005) 581-587
64. Welch T.R., Frenzke M., Witte D., and Davis A.E. C5a is important in the tubulointerstitial component of experimental immune complex glomerulonephritis. Clin. Exp. Immunol. 130 (2002) 43-48
65. Wenderfer S.E., Ke B., Hollmann T.J., Wetsel R.A., Lan H.Y., and Braun M.C. C5a receptor deficiency attenuates T cell function and renal disease in MRL/lpr mice. J. Am. Soc. Nephrol. 16 (2005) 3572-3582
66. Werfel T., Kirchhoff K., Wittmann M., Begemann G., Kapp A., Heidenreich F., Gotze O., and Zwirner J. Activated human T lymphocytes express a functional c3a receptor. J. Immunol. 165 (2000) 6599-6605
67. Wetsel R.A. Structure, function and cellular expression of complement anaphylatoxin receptors. Curr. Opin. Immunol. 7 (1995) 48-53
68. Wuyts A., Haelens A., Proost P., Lenaerts J.P., Conings R., Opdenakker G., and Van Damme J. Identification of mouse granulocyte chemotactic protein-2 from fibroblasts and epithelial cells. Functional comparison with natural kc and macrophage inflammatory protein-2. J. Immunol. 157 (1996) 1736-1743
69. Yin Z., Bahtiyar G., Zhang N., Liu L., Zhu P., Robert M.E., McNiff J., Madaio M.P., and Craft J. IL-10 regulates murine lupus. J. Immunol. 169 (2002) 2148-2155
70. Zwirner J., Gotze O., Begemann G., Kapp A., Kirchhoff K., and Werfel T. Evaluation of c3a receptor expression on human leucocytes by the use of novel monoclonal antibodies. Immunology 97 (1999) 166-172