IL-10 suppresses chemokines, inflammation, and fibrosis in a model of chronic renal disease

Journal of the American Society of Nephrology

Volumn 16, Issue 12, 2005, Pages 3651-3660

  Mu, Wei ^a   Ouyang, Xiaosen ^a   Agarwal, Anupam ^c   Zhang, Li ^a   Long, David A ^a   Cruz, Pedro E ^b   Roncal, Carlos A ^a   Glushakova, Olena Y ^a   Chiodo, Vince A ^b   Atkinson, Mark A ^a   Hauswirth, William W ^b   Flotte, Terry R ^b   Rodriguez Iturbe, Bernardo ^d   Johnson, Richard J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c University of Alabama at Birmingham   (United States)

^d HOSPITAL UNIVERSITARIO DE MARACAIBO   (Venezuela)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CREATININE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; RANTES; CYTOKINE; MESSENGER RNA;

ACUTE GLOMERULONEPHRITIS; ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CREATININE CLEARANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; GLOMERULOSCLEROSIS; IMMUNOREGULATION; INFLAMMATION; KIDNEY DISEASE; KIDNEY FIBROSIS; MALE; NEPHRECTOMY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; ANIMAL; BLOOD; CHRONIC KIDNEY FAILURE; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; INTERSTITIAL NEPHRITIS; KIDNEY FUNCTION TEST; METABOLISM; NEEDLE BIOPSY; PATHOLOGY; PATHOPHYSIOLOGY; PROTEINURIA; REFERENCE VALUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SPRAGUE DAWLEY RAT;

ANIMALS; BIOPSY, NEEDLE; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; FIBROSIS; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; KIDNEY FAILURE, CHRONIC; KIDNEY FUNCTION TESTS; MALE; NEPHRITIS, INTERSTITIAL; PROTEINURIA; RATS; RATS, SPRAGUE-DAWLEY; REFERENCE VALUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY;

EID: 33645456424     PISSN: 10466673     EISSN: None     Source Type: Journal    
DOI: 10.1681/ASN.2005030297     Document Type: Article

References (54)

1. Goldman M, Velu T: Interleukin-10 and its implications for immunopathology. Adv Nephrol Necker Hosp 24: 79-90, 1995
2. de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C, Johnson K, Kastelein R, Yssel H, de Vries JE: Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 174: 915-924, 1991
3. Willems F, Marchant A, Delville JP, Gerard C, Delvaux A, Velu T, de Boer M, Goldman M: Interleukin-10 inhibits B7 and intercellular adhesion molecule-1 expression on human monocytes. Eur J Immunol 24: 1007-1009, 1994
4. Petit-Bertron AF, Pedron T, Gross U, Coppee JY, Sansonetti PJ, Cavaillon JM, Adib-Conquy M: Adherence modifies the regulation of gene expression induced by interleukin-10. Cytokine 29: 1-12, 2005
5. Selzman CH, McIntyre RC Jr, Shames BD, Whitehill TA, Banerjee A, Harken AH: Interleukin-10 inhibits human vascular smooth muscle proliferation. J Mol Cell Cardiol 30: 889-896, 1998
6. Mazighi M, Pelle A, Gonzalez W, Mtairag el M, Philippe M, Henin D, Michel JB, Feldman LJ: IL-10 inhibits vascular smooth muscle cell activation in vitro and in vivo. Am J Physiol Heart Circ Physiol 287: H866-H871, 2004
7. Zimmerman MA, Reznikov LL, Raeburn CD, Selzman CH: Interleukin-10 attenuates the response to vascular injury. J Surg Res 121: 206-213, 2004
8. Feldman LJ, Aguirre L, Ziol M, Bridou JP, Nevo N, Michel JB, Steg PG: Interleukin-10 inhibits intimal hyperplasia after angioplasty or stent implantation in hypercholesterolemic rabbits. Circulation 101: 908-916, 2000
9. Kok MR, Yamano S, Lodde BM, Wang J, Couwenhoven RI, Yakar S, Voutetakis A, Leroith D, Schmidt M, Afione S, Pillemer SR, Tsutsui MT, Tak PP, Chiorini JA, Baum BJ: Local adeno-associated virus-mediated interleukin 10 gene transfer has disease-modifying effects in a murine model of Sjogren's syndrome. Hum Gene Ther 14: 1605-1618, 2003
10. Yoshidome H, Kato A, Edwards MJ, Lentsch AB: Interleukin-10 suppresses hepatic ischemia/reperfusion injury in mice: implications of a central role for nuclear factor kappaB. Hepatology 30: 203-208, 1999
11. Kitching AR, Katerelos M, Mudge SJ, Tipping PG, Power DA, Holdsworth SR: Interleukin-10 inhibits experimental mesangial proliferative glomerulonephritis. Clin Exp Immunol 128: 36-43, 2002
12. Choi YK, Kim YJ, Park HS, Choi K, Paik SG, Lee YI, Park JG: Suppression of glomerulosclerosis by adenovirus-mediated IL-10 expression in the kidney. Gene Ther 10: 559-568, 2003
13. Song S, Embury J, Laipis PJ, Berns KI, Crawford JM, Flotte TR: Stable therapeutic serum levels of human alpha-1 antitrypsin (AAT) after portal vein injection of recombinant adeno-associated virus (rAAV) vectors. Gene Ther 8:1299-1306, 2001
14. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO: Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28: 158-167, 2002
15. Kang DH, Yu ES, Yoon KI, Johnson R: The impact of gender on progression of renal disease: Potential role of estrogen-mediated vascular endothelial growth factor regulation and vascular protection. Am J Pathol 164: 679-688, 2004
16. Romero F, Rodriguez-Iturbe B, Parra G, Gonzalez L, Herrera-Acosta J, Tapia E: Mycophenolate mofetil prevents the progressive renal failure induced by 5/6 renal ablation in rats. Kidney Int 55: 945-955, 1999
17. Ikezumi Y, Atkins RC, Nikolic-Paterson DJ: Interferon-gamma augments acute macrophage-mediated renal injury via a glucocorticoid-sensitive mechanism. J Am Soc Nephrol 14: 888-898, 2003
18. Gerez L, Madar L, Shkolnik T, Kristal B, Arad G, Reshef A, Steinberger A, Ketzinel M, Sayar D, Shasha S, et al: Regulation of interleukin-2 and interferon-gamma gene expression in renal failure. Kidney Int 40: 266-272, 1991
19. Floege J, Alpers CE, Burns MW, Pritzl P, Gordon K, Couser WG, Johnson RJ: Glomerular cells, extracellular matrix accumulation, and the development of glomerulosclerosis in the remnant kidney model. Lab Invest 66: 485-497, 1992
20. Schiller B, Moran J: Focal glomerulosclerosis in the remnant kidney model-An inflammatory disease mediated by cytokines. Nephrol Dial Transplant 12: 430-437, 1997
21. Zhang YC, Pileggi A, Agarwal A, Molano RD, Powers M, Brusko T, Wasserfall C, Goudy K, Zahr E, Poggioli R, Scott-Jorgensen M, Campbell-Thompson M, Crawford JM, Nick H, Flotte T, Ellis TM, Ricordi C, Inverardi L, Atkinson MA: Adeno-associated virus-mediated IL-10 gene therapy inhibits diabetes recurrence in syngeneic islet cell transplantation of NOD mice. Diabetes 52: 708-716, 2003
22. Goudy KS, Burkhardt BR, Wasserfall C, Song S, Campbell-Thompson ML, Brusko T, Powers MA, Clare-Salzler MJ, Sobel ES, Ellis TM, Flotte TR, Atkinson MA: Systemic overexpression of IL-10 induces CD4+CD25+ cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion. J Immunol 171: 2270-2278, 2003
23. Goudy K, Song S, Wasserfall C, Zhang YC, Kapturczak M, Muir A, Powers M, Scott-Jorgensen M, Campbell-Thompson M, Crawford JM, Ellis TM, Flotte TR, Atkinson MA: Adeno-associated virus vector-mediated IL-10 gene delivery prevents type 1 diabetes in NOD mice. Proc Natl Acad Sci U S A 98: 13913-13918, 2001
24. You S, Chen C, Lee WH, Brusko T, Atkinson M, Liu CP: Presence of diabetes-inhibiting, glutamic acid decarboxylase-specific, IL-10-dependent, regulatory T cells in naive nonobese diabetic mice. J Immunol 173: 6777-6785, 2004
25. Conlon TJ, Flotte TR: Recombinant adeno-associated virus vectors for gene therapy. Expert Opin Biol Ther 4: 1093-1101, 2004
26. van der Leij J, van den Berg A, Blokzijl T, Harms G, van Goor H, Zwiers P, van Weeghel R, Poppema S, Visser L: Dimeric galectin-1 induces IL-10 production in T-lymphocytes: An important tool in the regulation of the immune response. J Pathol 204: 511-518, 2004
27. O'Farrell A-M, Liu Y, Moore KW, Mui AL-F: IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: Evidence for stat3- dependent and -independent pathways. EMBO J 17: 1006-1018, 1998
28. Wang P, Wu P, Siegel MI, Egan RW, Billah MM: Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J Biol Chem 270: 9558-9563, 1995
29. Hurme M, Henttinen T, Karppelin M, Varkila K, Matikainen S: Effect of interleukin-10 on NF-kappaB and AP-1 activities in interleukin-2 dependent CD8 T lymphoblasts. Immunol Lett 42: 129-133, 1994
30. Bogdan C, Vodovotz Y, Nathan C: Macrophage deactivation by interleukin 10. J Exp Med 174: 1549-1555, 1991
31. Ralph P, Nakoinz I, Sampson-Johannes A, Fong S, Lowe D, Min H-Y, Lin L: IL-10, T lymphocyte inhibitor of human blood cell production of IL-1 and tumor necrosis factor. J Immunol 148: 808-814, 1992
32. Murphy EE, Terres G, Macatonia SE, Hsieh C-S, Mattson J, Lanier L, Wysocka M, Trinchieri G, Murphy K, O'Garra A: B7 and interleukin-12 cooperate for proliferation and IFN production by mouse Th1 clones that are unresponsive to B7 costimulation. J Exp Med 180: 223-231, 1994
33. de Waal Malefyt R, Abrams J, Bennett B, Figdor C, de Vries J: IL-10 inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174: 1209-1220, 1991
34. Florentino DF, Zlotnik A, Mosmann TR, Howard MH, O'Garra A: IL-10 inhibits cytokine production by activated macrophages. J Immunol 147: 3815-3822, 1991
35. DeWaal Malefyt R, Figdor CG, Huijbens R, Mohan PS, Bennett B, Culpepper J, Dang W, Zurawski G, de Vries JE: Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol 151: 6370-6381, 1993
36. D'Andrea A, Aste AM, Valiante NM, Ma X, Kubin M, Trinchieri G: Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041-1048, 1993
37. Gruber MF, Williams CC, Gerrard TL: Macrophage-colony-stimulating factor expression by anti-CD45 stimulated human monocytes is transcriptionally up-regulated by IL-1 beta and inhibited by IL-4 and IL-10. J Immunol 152:1354-1361, 1994
38. Allavena P, Piemonti L, Longoni D, Bernasconi S, Stoppacciaro A, Ruco L, Mantovani A: IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages. Eur J Immunol 28: 359-369, 1998
39. Kalinski P, Schuitemaker JH, Hilkens CM, Kapsenberg ML: Prostaglandin E2 induces the final maturation of IL-12-deficient CD1aCCD83C dendritic cells: The levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J Immunol 161: 2804-2809, 1998
40. Fortsch D, Rollinghoff M, Stenger S: IL-10 converts human dendritic cells into macrophage-like cells with increased antibacterial activity against virulent mycobacterium tuberculosis. J Immunol 165: 978-987, 2000
41. DeWaal Malefyt R, Haanen J, Spits H, Roncarolo M-G, te Velde A, Figdor C, Johnson K, Kastelein R, Yssel H, de Vries JE: IL-10 and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II MHC expression. J Exp Med 174: 915-924, 1991
42. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, Moore KW, O'Garra A: IL-10 acts on the antigen presenting cell to inhibit cytokine production by Th1 cells. J Immunol 146: 3444-3451, 1991
43. Ding L, Shevach EM: IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage co-stimulatory function. J Immunol 148: 3133-3139, 1992
44. Hsu D-H, Moore KW, Spits H: Differential effects of interleukin-4 and -10 on interleukin-2-induced interferon-synthesis and lymphokine-activated killer activity. Int Immunol 4: 563-569, 1992
45. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A: Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765, 2001
46. Floege J, Burns MW, Alpers CE, Yoshimura A, Pritzl P, Gordon K, Seifert RA, Bowen-Pope DF, Couser WG, Johnson RJ: Glomerular cell proliferation and PDGF expression precede glomerulosclerosis in the remnant kidney model. Kidney Int 42: 297-309, 1992
47. Kitching AR, Tipping PG, Huang XR, Mutch DA, Holdsworth SR: Interleukin-4 and interleukin-10 attenuate established crescentic glomerulonephritis in mice. Kidney Int 52: 52-59, 1997
48. Kitching AR, Tipping PG, Timoshanko JR, Holdsworth SR: Endogenous interleukin-10 regulates Th1 responses that induce crescentic glomerulonephritis. Kidney Int 57: 518-525, 2000
49. Tipping PG, Kitching AR, Huang XR, Mutch DA, Holdsworth SR: Immune modulation with interleukin-4 and interleukin-10 prevents crescent formation and glomerular injury in experimental glomerulonephritis. Eur J Immunol 27: 530-537, 1997
50. Johnson RJ, Herrera-Acosta J, Schreiner GF, Rodriguez-Iturbe B: Role of immunocompetent cells in nonimmune renal diseases. Kidney Int 59: 1626-1640, 2001
51. Taal MW, Zandi-Nejad K, Weening B, Shahsafaei A, Kato S, Lee KW, Ziai F, Jiang T, Brenner BM, MacKenzie HS: Proinflammatory gene expression and macrophage recruitment in the rat remnant kidney. Kidney Int 58: 1664-1676, 2000
52. Ota T, Tamura M, Osajima A, Doi Y, Kudo H, Anai H, Miyazaki M, Nishino T, Nakashima Y: Expression of monocyte chemoattractant protein-1 in proximal tubular epithelial cells in a rat model of progressive kidney failure. J Lab Clin Med 140: 43-51, 2002
53. Yoshioka T, Okada T, Maeda Y, Ikeda U, Shimpo M, Nomoto T, Takeuchi K, Nonaka-Sarukawa M, Ito T, Takahashi M, Matsushita T, Mizukami H, Hanazono Y, Kume A, Ookawara S, Kawano M, Ishibashi S, Shimada K, Ozawa K: Adeno-associated virus vector-mediated interleukin-10 gene transfer inhibits atherosclerosis in apolipoprotein E-deficient mice. Gene Ther 11: 1772-1779, 2004
54. Tsuruta S, Nakamuta M, Enjoji M, Kotoh K, Hiasa K, Egashira K, Nawata H: Anti-monocyte chemoattractant protein-1 gene therapy prevents dimethylnitrosamine-induced hepatic fibrosis in rats. Int J Mol Med 14: 837-842, 2004