Mycophenolic acid suppresses granulopoiesis by inhibition of interleukin-17 production

Kidney International

Volumn 78, Issue 1, 2010, Pages 79-88

  Von Vietinghoff, Sibylle ^a   Ouyang, Hui ^a   Ley, Klaus ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

IL 17; Inosine monophosphate dehydrogenase; Mycophenolate; Neutropenia

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; MYCOPHENOLIC ACID; COLONY STIMULATING FACTOR; CYTOKINE; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLATE MOFETIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CELL PROLIFERATION; CONTROLLED STUDY; GRANULOCYTE; GRANULOPOIESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE; THYMUS; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; DRUG EFFECTS; FEMALE; IMMUNOLOGY; KNOCKOUT MOUSE; LEUKOPOIESIS; MALE; METABOLISM;

ANIMALS; CELL DIFFERENTIATION; COLONY-STIMULATING FACTORS; CYTOKINES; FEMALE; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-17; LEUKOPOIESIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOPHENOLIC ACID; NEUTROPENIA; NEUTROPHILS; RECEPTORS, INTERLEUKIN-17; T-LYMPHOCYTES;

EID: 77953682162     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2010.84     Document Type: Article

References (80)

1. Andres E, Maloisel F. Idiosyncratic drug-induced agranulocytosis or acute neutropenia. Curr Opin Hematol 2008; 15: 15-21.
2. Group RTS. A blinded, randomized clinical trial of mycophenolate mofetil for the prevention of acute rejection in cadaveric renal transplantation. The Tricontinental Mycophenolate Mofetil Renal Transplantation Study Group. Transplantation 1996; 61: 1029-1037.
3. Pfitzmann R, Klupp J, Langrehr JM et al. Mycophenolatemofetil for immunosuppression after liver transplantation: a follow-up study of 191 patients. Transplantation 2003; 76: 130-136.
4. Hardinger KL, Hebbar S, Bloomer T et al. Adverse drug reaction driven immunosuppressive drug manipulations: a single-center comparison of enteric-coated mycophenolate sodium vs mycophenolate mofetil. Clin Transplant 2008; 22: 555-561.
5. Pietruck F, Abbud-Filho M, Vathsala A et al. Conversion from mycophenolate mofetil to enteric-coated mycophenolate sodium in stable maintenance renal transplant patients: pooled results from three international, multicenter studies. Transplant Proc 2007; 39: 103-108.
6. Sterneck M, Fischer L, Gahlemann C et al. Mycophenolate mofetil for prevention of liver allograft rejection: initial results of a controlled clinical trial. Ann Transplant 2000; 5: 43-46.
7. Zafrani L, Truffaut L, Kreis H et al. Incidence, risk factors and clinical consequences of neutropenia following kidney transplantation: a retrospective study. Am J Transplant 2009; 8: 1816-1825.
8. Bullingham RE, Nicholls AJ, Kamm BR. Clinical pharmacokinetics of mycophenolate mofetil. Clin Pharmacokinet 1998; 34: 429-455.
9. Oellerich M, Shipkova M, Schutz E et al. Pharmacokinetic and metabolic investigations of mycophenolic acid in pediatric patients after renal transplantation: implications for therapeutic drug monitoring. German Study Group on Mycophenolate Mofetil Therapy in Pediatric Renal Transplant Recipients. Ther Drug Monit 2000; 22: 20-26.
10. Meier-Kriesche HU, Shaw LM, Korecka M et al. Pharmacokinetics of mycophenolic acid in renal insufficiency. Ther Drug Monit 2000; 22: 27-30.
11. Kaplan B. Mycophenolic acid trough level monitoring in solid organ transplant recipients treated with mycophenolate mofetil: association with clinical outcome. Curr Med Res Opin 2006; 22: 2355-2364.
12. van Gelder T. Mycophenolate blood level monitoring: recent progress. Am J Transplant 2009; 9: 1495-1499.
13. Ekberg H, Tedesco-Silva H, Demirbas A et al. Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J Med 2007; 357: 2562-2575.
14. Halloran PF. Immunosuppressive drugs for kidney transplantation. N Engl J Med 2004; 351: 2715-2729.
15. Ginzler EM, Dooley MA, Aranow C et al. Mycophenolate mofetil or intravenous cyclophosphamide for lupus nephritis. N Engl J Med 2005; 353: 2219-2228.
16. Walsh M, James M, Jayne D et al. Mycophenolate mofetil for induction therapy of lupus nephritis: a systematic review and meta-analysis. Clin J Am Soc Nephrol 2007; 2: 968-975.
17. Koukoulaki M, Jayne DR. Mycophenolate mofetil in anti-neutrophil cytoplasm antibodies-associated systemic vasculitis. Nephron Clin Pract 2006; 102: c100-c107.
18. Langford CA, Talar-Williams C, Sneller MC. Mycophenolate mofetil for remission maintenance in the treatment of Wegener's granulomatosis. Arthritis Rheum 2004; 51: 278-283.
19. Hedstrom L, Gan L. IMP dehydrogenase: structural schizophrenia and an unusual base. Curr Opin Chem Biol 2006; 10: 520-525.
20. Carr SF, Papp E, Wu JC et al. Characterization of human type I and type II IMP dehydrogenases. J Biol Chem 1993; 268: 27286-27290.
21. Dayton JS, Lindsten T, Thompson CB et al. Effects of human T lymphocyte activation on inosine monophosphate dehydrogenase expression. J Immunol 1994; 152: 984-991.
22. Allison AC, Eugui EM. Mycophenolate mofetil and its mechanisms of action. Immunopharmacology 2000; 47: 85-118.
23. Quemeneur L, Gerland LM, Flacher M et al. Differential control of cell cycle, proliferation, and survival of primary T lymphocytes by purine and pyrimidine nucleotides. J Immunol 2003; 170: 4986-4995.
24. Gu JJ, Tolin AK, Jain J et al. Targeted disruption of the inosine 5-monophosphate dehydrogenase type I gene in mice. Mol Cell Biol 2003; 23: 6702-6712.
25. Lui SL, Ramassar V, Urmson J et al. Mycophenolate mofetil reduces production of interferon-dependent major histocompatibility complex induction during allograft rejection, probably by limiting clonal expansion. Transplant Immunol 1998; 6: 23-32.
26. Quemeneur L, Beloeil L, Michallet MC et al. Restriction of de novo nucleotide biosynthesis interferes with clonal expansion and differentiation into effector and memory CD8 T cells. J Immunol 2004; 173: 4945-4952.
27. Van Bruggen MC, Walgreen B, Rijke TP et al. Attenuation of murine lupus nephritis by mycophenolate mofetil. J Am Soc Nephrol 1998; 9: 1407-1415.
28. Nieto E, Escudero E, Navarro E et al. Effects of mycophenolate mofetil in mercury-induced autoimmune nephritis. J Am Soc Nephrol 2002; 13: 937-945.
29. Penny MJ, Boyd RA, Hall BM. Mycophenolate mofetil prevents the induction of active Heymann nephritis: association with Th2 cytokine inhibition. J Am Soc Nephrol 1998; 9: 2272-2282.
30. Metcalf D. Hematopoietic cytokines. Blood 2008; 111: 485-491.
31. Panopoulos AD, Watowich SS. Granulocyte colony-stimulating factor: molecular mechanisms of action during steady state and 'emergency' hematopoiesis. Cytokine 2008; 42: 277-288.
32. Christopher MJ, Link DC. Regulation of neutrophil homeostasis. Curr Opin Hematol 2007; 14: 3-8.
33. von Vietinghoff S, Ley K. Homeostatic regulation of blood neutrophil counts. J Immunol 2008; 181: 5183-5188.
34. Monteiro JP, Benjamin A, Costa ES et al. Normal hematopoiesis is maintained by activated bone marrow CD4+ T cells. Blood 2005; 105: 1484-1491.
35. Schwarzenberger P, La Russa V, Miller A et al. IL-17 stimulates granulopoiesis in mice: use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines. J Immunol 1998; 161: 6383-6389.
36. Forlow SB, Schurr JR, Kolls JK et al. Increased granulopoiesis through interleukin-17 and granulocyte colony-stimulating factor in leukocyte adhesion molecule-deficient mice. Blood 2001; 98: 3309-3314.
37. Kelly MN, Kolls JK, Happel K et al. Interleukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect Immun 2005; 73: 617-621.
38. Smith E, Stark MA, Zarbock A et al. IL-17A inhibits the expansion of IL-17A-producing T cells in mice through 'short-loop' inhibition via IL-17 receptor. J Immunol 2008; 181: 1357-1364.
39. Tan W, Huang W, Zhong Q et al. IL-17 receptor knockout mice have enhanced myelotoxicity and impaired hemopoietic recovery following gamma irradiation. J Immunol 2006; 176: 6186-6193.
40. 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: 519-527.
41. Tan W, Huang W, Gu X et al. IL-17F/IL-17R interaction stimulates granulopoiesis in mice. Exp Hematol 2008; 36: 1417-1427.
42. Kuestner RE, Taft DW, Haran A et al. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J Immunol 2007; 179: 5462-5473.
43. McAllister F, Henry A, Kreindler JL et al. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J Immunol 2005; 175: 404-412.
44. Bettelli E, Oukka M, Kuchroo VK. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007; 8: 345-350.
45. Stark MA, Huo Y, Burcin TL et al. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005; 22: 285-294.
46. Aggarwal S, Ghilardi N, Xie MH et al. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278: 1910-1914.
47. Bettelli E, Korn T, Oukka M et al. Induction and effector functions of T(H)17 cells. Nature 2008; 453: 1051-1057.
48. Harrington LE, Hatton RD, Mangan PR et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6: 1123-1132.
49. Zhou L, Ivanov II, Spolski R et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007; 8: 967-974.
50. Garrett-Sinha LA, John S, Gaffen SL. IL-17 and the Th17 lineage in systemic lupus erythematosus. Curr Opin Rheumatol 2008; 20: 519-525.
51. Langrish CL, Chen Y, Blumenschein WM et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201: 233-240.
52. Hamada S, Umemura M, Shiono T et al. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against Listeria monocytogenes infection in the liver. J Immunol 2008; 181: 3456-3463.
53. 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: 4662-4669.
54. Umemura M, Yahagi A, Hamada S et al. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 2007; 178: 3786-3796.
55. Heller T, Geide A, Bonitz U et al. Effect of the antioxidant idebenone on adverse events under mycophenolate mofetil therapy in a rat model. Transplantation 2008; 85: 739-747.
56. Manel N, Unutmaz D, Littman DR. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008; 9: 641-649.
57. European Mycophenolate Mofetil Cooperative Study Group. Placebo-controlled study of mycophenolate mofetil combined with cyclosporin and corticosteroids for prevention of acute rejection. Lancet 1995; 345: 1321-1325.
58. Surh CD, Sprent J. Homeostasis of naive and memory T cells. Immunity 2008; 29: 848-862.
59. Jensen KD, Su X, Shin S et al. Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 2008; 29: 90-100.
60. Mathur AN, Chang HC, Zisoulis DG et al. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 2006; 108: 1595-1601.
61. McGeachy MJ, Chen Y, Tato CM et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 2009; 10: 314-324.
62. Broxmeyer HE, Bruns HA, Zhang S et al. Th1 cells regulate hematopoietic progenitor cell homeostasis by production of oncostatin M. Immunity 2002; 16: 815-825.
63. Abadja F, Videcoq C, Alamartine E et al. Differential effect of cyclosporine and mycophenolic acid on the human regulatory T cells and TH-17 cells balance. Transplant Proc 2009; 41: 3367-3370.
64. Gonzalez-Alvaro I, Ortiz AM, Dominguez-Jimenez C et al. Inhibition of tumour necrosis factor and IL-17 production by leflunomide involves the JAK/STAT pathway. Ann Rheum Dis 2009; 68: 1644-1650.
65. Liu Z, Yuan X, Luo Y et al. Evaluating the effects of immunosuppressants on human immunity using cytokine profiles of whole blood. Cytokine 2009; 45: 141-147.
66. Gu JJ, Stegmann S, Gathy K et al. Inhibition of T lymphocyte activation in mice heterozygous for loss of the IMPDH II gene. J Clin Invest 2000; 106: 599-606.
67. Quemeneur L, Flacher M, Gerland LM et al. Mycophenolic acid inhibits IL-2-dependent T cell proliferation, but not IL-2-dependent survival and sensitization to apoptosis. J Immunol 2002; 169: 2747-2755.
68. Loong CC, Hsieh HG, Lui WY et al. Evidence for the early involvement of interleukin 17 in human and experimental renal allograft rejection. J Pathol 2002; 197: 322-332.
69. Van Kooten C, 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: 1526-1534.
70. San Segundo D, Lopez-Hoyos M, Fernandez-Fresnedo G et al. T(H)17 versus treg cells in renal transplant candidates: effect of a previous transplant. Transplant Proc 2008; 40: 2885-2888.
71. Burrell BE, Csencsits K, Lu G et al. CD8+ Th17 mediate costimulation blockade-resistant allograft rejection in T-bet-deficient mice. J Immunol 2008; 181: 3906-3914.
72. Summers SA, Steinmetz OM, Li M et al. Th1 and Th17 cells induce proliferative glomerulonephritis. J Am Soc Nephrol 2009; 20: 2518-2524.
73. Paust HJ, Turner JE, Steinmetz OM et al. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009; 20: 969-979.
74. Ooi JD, Phoon RK, Holdsworth SR et al. IL-23, not IL-12, directs autoimmunity to the Goodpasture antigen. J Am Soc Nephrol 2009; 20: 980-989.
75. Hsu HC, Yang P, Wang J et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 2008; 9: 166-175.
76. Nogueras F, Espinosa MD, Mansilla A et al. Mycophenolate mofetil-induced neutropenia in liver transplantation. Transplant Proc 2005; 37: 1509-1511.
77. Clark OA, Lyman G, Castro AA et al. Colony stimulating factors for chemotherapy induced febrile neutropenia. Cochrane Database Syst Rev 2003; CD003039.
78. Caproni M, Antiga E, Melani L et al. Serum levels of IL-17 and IL-22 are reduced by etanercept, but not by acitretin, in patients with psoriasis: a randomized-controlled trial. J Clin Immunol 2009; 29: 210-214.
79. Nakae S, Komiyama Y, Nambu A et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002; 17: 375-387.
80. Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003; 31: e154.