Chemokine receptor Ccr2 deficiency reduces renal disease and prolongs survival in MRL/lpr lupus-prone mice

Journal of the American Society of Nephrology

Volumn 16, Issue 12, 2005, Pages 3592-3601

  De Lema, Guillermo Pérez ^a   Maier, Holger ^a   Franz, Tobias J ^b   Escribese, María ^c   Chilla, Silvia ^a   Segerer, Stephan ^a   Camarasa, Natalia ^c   Schmid, Holger ^a   Banas, Bernhard ^a   Kalaydjiev, Svetoslav ^b   Busch, Dirk H ^b,d   Pfeffer, Klaus ^e   Mampaso, Francisco ^c   Schlöndorff, Detlef ^a   Luckow, Bruno ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF ALCALÁ   (Spain)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CHEMOKINE RECEPTOR CCR2; DOUBLE STRANDED DNA ANTIBODY; UREA; CHEMOKINE RECEPTOR;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; AUTOIMMUNITY; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE MODEL; GLOMERULONEPHRITIS; HYPERGAMMAGLOBULINEMIA; KIDNEY DISEASE; LUPUS ERYTHEMATOSUS; LYMPHADENOPATHY; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; NONHUMAN; PRIORITY JOURNAL; SCORING SYSTEM; SPLENOMEGALY; SURVIVAL RATE; T LYMPHOCYTE; UREA NITROGEN BLOOD LEVEL; ANIMAL; COMPARATIVE STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LUPUS ERYTHEMATOSUS NEPHRITIS; MORTALITY; NEEDLE BIOPSY; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK FACTOR; SENSITIVITY AND SPECIFICITY; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; BIOPSY, NEEDLE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; IMMUNOHISTOCHEMISTRY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MICE; MICE, INBRED MRL LPR; RECEPTORS, CHEMOKINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; SENSITIVITY AND SPECIFICITY; SURVIVAL RATE;

EID: 33645903240     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005040426     Document Type: Article

References (50)

1. Lahita RG: Systemic Lupus Erythematosus, New York, Academic Press, 2004
2. Theofilopoulos AN, Dixon FJ: Murine models of systemic lupus erythematosus. Adv Immunol 37: 269-390, 1985
3. Reilly CM, Gilkeson GS: Use of genetic knockouts to modulate disease expression in a murine model of lupus, MRL/lpr mice. Immunol Res 25: 143-153, 2002
4. Manderson AP, Botto M, Walport MJ: The role of complement in the development of systemic lupus erythematosus. Annu Rev Immunol 22: 431-456, 2004
5. Tesch GH, Maifert S, Schwarting A, Rollins BJ, Kelley VR: Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J Exp Med 190: 1813-1824, 1999
6. Pérez de Lema G, Maier H, Nieto E, Vielhauer V, Luckow B, Mampaso F, Schlöndorff D: Chemokine expression precedes inflammatory cell infiltration and chemokine receptor and cytokine expression during the initiation of murine lupus nephritis. J Am Soc Nephrol 12: 1369-1382, 2001
7. Segerer S, Nelson PJ, Schlöndorff D: Chemokines, chemokine receptors, and renal disease: From basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol 11: 152-176, 2000
8. Hasegawa H, Kohno M, Sasaki M, Inoue A, Ito MR, Terada M, Hieshima K, Maruyama H, Miyazaki J, Yoshie O, Nose M, Fujita S: Antagonist of monocyte chemoattractant protein 1 ameliorates the initiation and progression of lupus nephritis and renal vasculitis in MRL/lpr mice. Arthritis Rheum 48: 2555-2566, 2003
9. Shimizu S, Nakashima H, Masutani K, Inoue Y, Miyake K, Akahoshi M, Tanaka Y, Egashira K, Hirakata H, Otsuka T, Harada M: Anti-monocyte chemoattractant protein-1 gene therapy attenuates nephritis in MRL/lpr mice. Rheumatology (Oxford) 43: 1121-1128, 2004
10. Charo IF, Peters W: Chemokine receptor 2 (CCR2) in atherosclerosis, infectious diseases, and regulation of T-cell polarization. Microcirculation 10: 259-264, 2003
11. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr, Broxmeyer HE, Charo IF: Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest 100: 2552-2561, 1997
12. Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ: Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404: 407-411, 2000
13. Daly C, Rollins BJ: Monocyte chemoattractant protein-1 (CCL2) in inflammatory disease and adaptive immunity: Therapeutic opportunities and controversies. Microcirculation 10: 247-257, 2003
14. Schecter AD, Berman AB, Yi L, Ma H, Daly CM, Soejima K, Rollins BJ, Charo IF, Taubman MB: MCP-1-dependent signaling in CCR2(-/-) aortic smooth muscle cells. J Leukoc Biol 75: 1079-1085, 2004
15. Quinones MP, Ahuja SK, Jimenez F, Schaefer J, Garavito E, Rao A, Chenaux G, Reddick RL, Kuziel WA, Ahuja SS: Experimental arthritis in CC chemokine receptor 2-null mice closely mimics severe human rheumatoid arthritis. J Clin Invest 113: 856-866, 2004
16. Pérez de Lema G, De Wit C, Nieto E, Molina A, Banas B, Cohen CD, Luckow B, Vicente AB, Mampaso F, Schlöndorff D: Angiotensin inhibition reduces glomerular damage and renal chemokine expression in MRL/lpr mice. J Pharmacol Exp Ther 307: 275-281, 2003
17. Pérez de Lema G, Lucio-Cazana FJ, Molina A, Luckow B, Schmid H, de Wit C, Moreno-Manzano V, Banas B, Mampaso F, Schlöndorff D: Retinoic acid treatment protects MRL/lpr lupus mice from the development of glomerular disease. Kidney Int 66: 1018-1028, 2004
18. Segerer S, Hudkins KL, Taneda S, Wen M, Cui Y, Segerer M, Farr AG, Alpers CE: Oral interferon-alpha treatment of mice with cryoglobulinemic glomerulonephritis. Am J Kidney Dis 39: 876-888, 2002
19. Luckow B, Maier H, Chilla S, Pérez de Lema G: The mCK-5 multiprobe RNase protection assay kit can yield erroneous results for the murine chemokines IP-10 and MCP-1. Anal Biochem 286: 193-197, 2000
20. Luckow B, Joergensen J, Chilla S, Li JP, Henger A, Kiss E, Wieczorek G, Roth L, Hartmann N, Hoffmann R, Kretzler M, Nelson PJ, Pérez de Lema G, Maier H, Wurst W, Balling R, Pfeffer K, Gröne HJ, Schlöndorff D, Zerwes HG: Reduced intragraft mRNA expression of matrix metalloproteinases Mmp3, Mmp12, Mmp13 and Adam8, and diminished transplant arteriosclerosis in Ccr5-deficient mice. Eur J Immunol 34: 2568-2578, 2004
21. Mack M, Cihak J, Simonis C, Luckow B, Proudfoot AE, Plachy J, Brühl H, Frink M, Anders HJ, Vielhauer V, Pfirstinger J, Stangassinger M, Schlöndorff D: Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice. J Immunol 166: 4697-4704, 2001
22. Leenen PJ, de Bruijn MF, Voerman JS, Campbell PA, van Ewijk W: Markers of mouse macrophage development detected by monoclonal antibodies. J Immunol Methods 174: 5-19, 1994
23. Traynor TR, Herring AC, Dorf ME, Kuziel WA, Toews GB, Huffnagle GB: Differential roles of CC chemokine ligand 2/monocyte chemotactic protein-1 and CCR2 in the development of T1 immunity. J Immunol 168: 4659-4666, 2002
24. Bird JE, Giancarli MR, Kurihara T, Kowala MC, Valentine MT, Gitlitz PH, Pandya DG, French MH, Durham SK: Increased severity of glomerulonephritis in C-C chemokine receptor 2 knockout mice. Kidney Int 57: 129-136, 2000
25. Brown CR, Blaho VA, Loiacono CM: Susceptibility to experimental Lyme arthritis correlates with KC and monocyte chemoattractant protein-1 production in joints and requires neutrophil recruitment via CXCR2. J Immunol 171: 893-901, 2003
26. Boring L, Gosling J, Cleary M, Charo IF: Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394: 894-897, 1998
27. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ: CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 192: 899-905, 2000
28. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD: Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 192: 1075-1080, 2000
29. Gaupp S, Pitt D, Kuziel WA, Cannella B, Raine CS: Experimental autoimmune encephalomyelitis (EAE) in CCR2(-/-) mice: Susceptibility in multiple strains. Am J Pathol 162: 139-150, 2003
30. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ: Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 100: 7947-7952, 2003
31. Kurihara T, Warr G, Loy J, Bravo R: Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J Exp Med 186: 1757-1762, 1997
32. Sato N, Ahuja SK, Quinones M, Kostecki V, Reddick RL, Melby PC, Kuziel WA, Ahuja SS: CC chemokine receptor (CCR)2 is required for Langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells. Absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, B cell outgrowth, and sustained neutrophilic inflammation. J Exp Med 192: 205-218, 2000
33. Traynor TR, Kuziel WA, Toews GB, Huffnagle GB: CCR2 expression determines T1 versus T2 polarization during pulmonary Cryptococcus neoformans infection. J Immunol 164: 2021-2027, 2000
34. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM: Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193: 713-726, 2001
35. DePaolo RW, Rollins BJ, Kuziel W, Karpus WJ: CC chemokine ligand 2 and its receptor regulate mucosal production of IL-12 and TGF-beta in high dose oral tolerance. J Immunol 171: 3560-3567, 2003
36. Haas C, Ryffel B, Le Hir M: IFN-gamma is essential for the development of autoimmune glomerulonephritis in MRL/ Ipr mice. J Immunol 158: 5484-5491, 1997
37. Balomenos D, Rumold R, Theofilopoulos AN: Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J Clin Invest 101: 364-371, 1998
38. Diaz Gallo C, Jevnikar AM, Brennan DC, Florquin S, Pacheco-Silva A, Kelley VR: Autoreactive kidney-infiltrating T-cell clones in murine lupus nephritis. Kidney Int 42: 851-859, 1992
39. Carvalho-Pinto CE, Garcia MI, Mellado M, Rodriguez-Frade JM, Martin-Caballero J, Flores J, Martinez AC, Balomenos D: Autocrine production of IFN-gamma by macrophages controls their recruitment to kidney and the development of glomerulonephritis in MRL/lpr mice. J Immunol 169: 1058-1067, 2002
40. Peters W, Dupuis M, Charo IF: A mechanism for the impaired IFN-gamma production in C-C chemokine receptor 2 (CCR2) knockout mice: Role of CCR2 in linking the innate and adaptive immune responses. J Immunol 165: 7072-7077, 2000
41. Yopp AC, Fu S, Honig SM, Randolph GJ, Ding Y, Krieger NR, Bromberg JS: FTY720-enhanced T cell homing is dependent on CCR2, CCR5, CCR7, and CXCR4: Evidence for distinct chemokine compartments. J Immunol 173: 855-865, 2004
42. Reid S, Ritchie A, Boring L, Gosling J, Cooper S, Hangoc G, Charo IF, Broxmeyer HE: Enhanced myeloid progenitor cell cycling and apoptosis in mice lacking the chemokine receptor, CCR2. Blood 93: 1524-1533, 1999
43. Nansen A, Marker O, Bartholdy C, Thomsen AR: CCR2+ and CCR5+ CD8+ T cells increase during viral infection and migrate to sites of infection. Eur J Immunol 30: 1797-1806, 2000
44. Abdi R, Means TK, Ito T, Smith RN, Najafian N, Jurewicz M, Tchipachvili V, Charo I, Auchincloss H Jr, Sayegh MH, Luster AD: Differential role of CCR2 in islet and heart allograft rejection: Tissue specificity of chemokine/chemokine receptor function in vivo. J Immunol 172: 767-775, 2004
45. Wada T, Schwarting A, Chesnutt MS, Wofsy D, Kelley VR: Nephritogenic cytokines and disease in MRL-Fas(lpr) kidneys are dependent on multiple T-cell subsets. Kidney Int 59: 565-578, 2001
46. Tipping PG, Holdsworth SR: T cells in glomerulonephritis. Springer Semin Immunopathol 24: 377-393, 2003
47. Clynes R, Dumitru C, Ravetch JV: Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 279: 1052-1054, 1998
48. Kikawada E, Lenda DM, Kelley VR: IL-12 deficiency in MRL-Fas(lpr) mice delays nephritis and intrarenal IFN-gamma expression, and diminishes systemic pathology. J Immunol 170: 3915-3925, 2003
49. Lenda DM, Stanley ER, Kelley VR: Negative role of colony-stimulating factor-1 in macrophage, T cell, and B cell mediated autoimmune disease in MRL-Faslpr mice. J Immunol 173: 4744-4754, 2004
50. Schwarting A, Wada T, Kinoshita K, Tesch G, Kelley VR: IFN-gamma receptor signaling is essential for the initiation, acceleration, and destruction of autoimmune kidney disease in MRL-Fas(lpr) mice. J Immunol 161: 494-503, 1998