Interleukin-17 positive cells accumulate in renal allografts during acute rejection and are independent predictors of worse graft outcome

Transplant International

Volumn 24, Issue 10, 2011, Pages 1008-1017

  Yapici, Ünsal ^a   Kers, Jesper ^a   Bemelman, Fréderike J ^a   Roelofs, Joris J T H ^a   Groothoff, Jaap W ^a   Van Der Loos, Chris M ^a   Van Donselaar Van Der Pant, Karlijn A M I ^a   Idu, Mirza M ^a   Claessen, Nike ^a   Ten Berge, Ineke J M ^a   Florquin, Sandrine ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

acute renal allograft rejection; Interleukin 17; mast cells; neutrophils; renal transplant outcome; T lymphocytes; T h17

Indexed keywords

INTERLEUKIN 17;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; GLOMERULUS FILTRATION RATE; HUMAN; HUMAN TISSUE; KIDNEY ALLOGRAFT; KIDNEY ALLOGRAFT REJECTION; KIDNEY BIOPSY; KIDNEY DISEASE; KIDNEY FIBROSIS; MAST CELL; NEUTROPHIL; PREDICTION; PRIORITY JOURNAL; T LYMPHOCYTE; TREATMENT OUTCOME; TUBULAR ATROPHY;

ADOLESCENT; ADULT; AGED; BIOPSY; FEMALE; GLOMERULAR FILTRATION RATE; GRAFT REJECTION; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; KIDNEY TRANSPLANTATION; MALE; MAST CELLS; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEUTROPHILS; RENAL INSUFFICIENCY; TREATMENT OUTCOME;

EID: 80052534948     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/j.1432-2277.2011.01302.x     Document Type: Article

References (42)

1. Piccotti JR, Chan SY, VanBuskirk AM, Eichwald EJ, Bishop DK,. Are Th2 helper T lymphocytes beneficial, deleterious, or irrelevant in promoting allograft survival? Transplantation 1997; 63: 619.
2. Song C, Luo L, Lei Z, et al. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J Immunol 2008; 181: 6117.
3. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K,. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005; 22: 285.
4. Michel ML, Keller AC, Paget C, et al. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 2007; 204: 995.
5. Lockhart E, Green AM, Flynn JL,. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006; 177: 4662.
6. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A,. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide- induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003; 170: 2106.
7. Ikeda K, Nakajima H, Suzuki K, et al. Mast cells produce interleukin-25 upon Fc epsilon RI-mediated activation. Blood 2003; 101: 3594.
8. de Boer OJ, van der Meer JJ, Teeling P, et al. Differential expression of interleukin-17 family cytokines in intact and complicated human atherosclerotic plaques. J Pathol 2010; 220: 499.
9. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH,. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 2006; 177: 7980.
10. Hofstetter HH, Ibrahim SM, Koczan D, et al. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol 2005; 237: 123.
11. van KC, Boonstra JG, Paape ME, et al. Interleukin-17 activates human renal epithelial cells in vitro and is expressed during renal allograft rejection. J Am Soc Nephrol 1998; 9: 1526.
12. Verleden GM, Vos R, Vanaudenaerde BM, Van RD, Dupont LJ,. Interleukin-17 and neutrophils are increased in BAL fluid during acute lung rejection. Chest 2007; 131: 1988.
13. Fabrega E, Lopez-Hoyos M, San SD, Casafont F, Pons-Romero F,. Changes in the serum levels of interleukin-17/interleukin-23 during acute rejection in liver transplantation. Liver Transpl 2009; 15: 629.
14. Tang JL, Subbotin VM, Antonysamy MA, Troutt AB, Rao AS, Thomson AW,. Interleukin-17 antagonism inhibits acute but not chronic vascular rejection. Transplantation 2001; 2: 348.
15. Res PC, Piskin G, de Boer OJ, et al. Overrepresentation of IL-17A and IL-22 producing CD8 T cells in lesional skin suggests their involvement in the pathogenesis of psoriasis. PLoS ONE 2010; 5: e14108.
16. Sis B, Mengel M, Haas M, et al. Banff '09 meeting report: antibody mediated graft deterioration and implementation of Banff working groups. Am J Transplant 2010; 10: 464.
17. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int 1999; 55: 713.
18. Scheepstra C, Bemelman FJ, van der Loos C, et al. B cells in cluster or in a scattered pattern do not correlate with clinical outcome of renal allograft rejection. Transplantation 2008; 86: 772.
19. Yapici U, Bemelman FJ, Scheepstra CG, et al. Intragraft FOXP3 protein or mRNA during acute renal allograft rejection correlates with inflammation, fibrosis, and poor renal outcome. Transplantation 2009; 87: 1377.
20. Gaber LW, Moore LW, Alloway RR, et al. Correlation between Banff classification, acute renal rejection scores and reversal of rejection. Kidney Int 1996; 49: 481.
21. Haas M, Kraus ES, Samaniego-Picota M, Racusen LC, Ni W, Eustace JA,. Acute renal allograft rejection with intimal arteritis: histologic predictors of response to therapy and graft survival. Kidney Int 2002; 61: 1516.
22. Dessing MC, Bemelman FJ, Claessen N, ten Berge IJ, Florquin S, Leemans JC,. Intragraft Toll-like receptor profiling in acute renal allograft rejection. Nephrol Dial Transplant 2010; 25: 4087.
23. Levey AS, Stevens LA,. Estimating GFR using the CKD Epidemiology Collaboration (CKD-EPI) creatinine equation: more accurate GFR estimates, lower CKD prevalence estimates, and better risk predictions. Am J Kidney Dis 2010; 55: 622.
24. Magee CC, Pascual M,. Update in renal transplantation. Arch Intern Med 2004; 164: 1373.
25. van Beelen AJ, Zelinkova Z, Taanman-Kueter EW, et al. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity 2007; 27: 660.
26. Ye P, Rodriguez FH, Kanaly S, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001; 194: 519.
27. Miyamoto M, Prause O, Sjostrand M, Laan M, Lotvall J, Linden A,. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J Immunol 2003; 170: 4665.
28. Loong CC, Hsieh HG, Lui WY, Chen A, Lin CY,. Evidence for the early involvement of interleukin 17 in human and experimental renal allograft rejection. J Pathol 2002; 197: 322.
29. Li J, Simeoni E, Fleury S, et al. Gene transfer of soluble interleukin-17 receptor prolongs cardiac allograft survival in a rat model. Eur J Cardiothorac Surg 2006; 29: 779.
30. Prause O, Bossios A, Silverpil E, et al. IL-17-producing T lymphocytes in lung tissue and in the bronchoalveolar space after exposure to endotoxin from Escherichia coli in vivo-effects of anti-inflammatory pharmacotherapy. Pulm Pharmacol Ther 2009; 22: 199.
31. Hirota K, Duarte JH, Veldhoen M, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 2011; 12: 255.
32. Einecke G, Reeve J, Sis B, et al. A molecular classifier for predicting future graft loss in late kidney transplant biopsies. J Clin Invest 2010; 120: 1862.
33. Sarwal M, Chua MS, Kambham N, et al. Molecular heterogeneity in acute renal allograft rejection identified by DNA microarray profiling. N Engl J Med 2003; 349: 125.
34. Alegre ML, Florquin S, Goldman M,. Cellular mechanisms underlying acute graft rejection: time for reassessment. Curr Opin Immunol 2007; 19: 563.
35. Bohmig GA, Exner M, Habicht A, et al. Capillary C4d deposition in kidney allografts: a specific marker of alloantibody-dependent graft injury. J Am Soc Nephrol 2002; 13: 1091.
36. Mengel M, Reeve J, Bunnag S, et al. Scoring total inflammation is superior to the current Banff inflammation score in predicting outcome and the degree of molecular disturbance in renal allografts. Am J Transplant 2009; 9: 1859.
37. Mannon RB, Matas AJ, Grande J, et al. Inflammation in areas of tubular atrophy in kidney allograft biopsies: a potent predictor of allograft failure. Am J Transplant 2010; 10: 2066.
38. Loverre A, Divella C, Castellano G, et al. T helper 1, 2 and 17 cell subsets in renal transplant patients with delayed graft function. Transpl Int 2011; 24: 233.
39. Deteix C, Attuil-Audenis V, Duthey A, et al. Intragraft Th17 infiltrate promotes lymphoid neogenesis and hastens clinical chronic rejection. J Immunol 2010; 184: 5344.
40. Katz Y, Nadiv O, Rapoport MJ, Loos M,. IL-17 regulates gene expression and protein synthesis of the complement system, C3 and factor B, in skin fibroblasts. Clin Exp Immunol 2000; 120: 22.
41. Sugihara T, Kobori A, Imaeda H, et al. The increased mucosal mRNA expressions of complement C3 and interleukin-17 in inflammatory bowel disease. Clin Exp Immunol 2010; 160: 386.
42. Sis B, Halloran PF,. Endothelial transcripts uncover a previously unknown phenotype: C4d-negative antibody-mediated rejection. Curr Opin Organ Transplant 2010; 15: 42.