CCR5 blockade modulates inflammation and alloimmunity in primates

Journal of Immunology

Volumn 179, Issue 4, 2007, Pages 2289-2299

  Schröder, Carsten ^a,b   Pierson III, Richard N ^a,b,d   Nguyen, Bao Ngoc H ^a,b   Kawka, Douglas W ^c   Peterson, Laurence B ^c   Wu, Guosheng ^a,b   Zhang, Tianshu ^a,b   Springer, Martin S ^c   Siciliano, Sal J ^c   Iliff, Susan ^c   Ayala, Julia M ^c   Lu, Min ^c   Mudgett, John S ^c   Lyons, Kathy ^c   Mills, Sander G ^c   Miller, Geraldine G ^b   Singer, Irwin I ^c   Azimzadeh, Agnes M ^a,b   DeMartino, Julie A ^c  

^a UNIVERSITY OF MARYLAND   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIBODY; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CYCLOSPORIN A; N [3 [4 (3 BENZYL 1 ETHYL 5 PYRAZOLYL) 1 PIPERIDINYLMETHYL] 4 (3 FLUOROPHENYL)CYCLOPENTYL] N METHYLVALINE; CYCLOSPORIN; DRUG DERIVATIVE; IMMUNOSUPPRESSIVE AGENT; N (3 (3 FLUOROPHENYL) 4 ((4 (3 BENZYL 1 ETHYLPYRAZOL 5 YL)PIPERIDIN 1 YL)METHYL)CYCLOPENTYL) N METHYLVALINE; N-(3-(3-FLUOROPHENYL)-4-((4-(3-BENZYL-1-ETHYLPYRAZOL-5-YL)PIPERIDIN-1-YL)METHYL)CYCLOPENTYL)-N-METHYLVALINE; PYRAZOLE DERIVATIVE; UNCLASSIFIED DRUG; VALINE;

ACUTE GRAFT REJECTION; ALLOGRAFT; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CHRONIC GRAFT REJECTION; CONTROLLED STUDY; DRUG INHIBITION; GRAFT FAILURE; GRAFT SURVIVAL; HEART GRAFT; HOMOZYGOSITY; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; KIDNEY GRAFT; LEUKOCYTE COUNT; MONKEY; MONOTHERAPY; NONHUMAN; PERIOPERATIVE PERIOD; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRESS; ALLOTRANSPLANTATION; ANIMAL; ANTIBODY PRODUCTION; AUTOIMMUNITY; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; HEART TRANSPLANTATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; KIDNEY TRANSPLANTATION; MACACA; MACROPHAGE; MALE; PATHOLOGY; T LYMPHOCYTE; TRANSPLANTATION TOLERANCE; VASCULAR DISEASE;

ANIMALS; ANTIBODY FORMATION; AUTOIMMUNITY; CYCLOSPORINE; DISEASE MODELS, ANIMAL; GRAFT SURVIVAL; HEART TRANSPLANTATION; HIV INFECTIONS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION; ISOANTIBODIES; KIDNEY TRANSPLANTATION; MACACA FASCICULARIS; MACROPHAGES; MALE; PYRAZOLES; RECEPTORS, CCR5; STRESS; T-LYMPHOCYTES; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HOMOLOGOUS; VALINE; VASCULAR DISEASES;

EID: 34848869334     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.4.2289     Document Type: Article

References (52)

1. Springer, T. A. 1995. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu. Rev. Physiol. 57: 827-872.
2. Flach, R., N. Spieled, S. Flohe, J. Borgermann, I. G. Dresen, J. Erhard, and F. U. Schade. 1998. Analysis of intragraft cytokine expression during early reperfusion after liver transplantation using semi-quantitative RT-PCR. Cytokine 10: 445-451.
3. Gu, L., S. Tseng, R. M. Horner, C. Tam, M. Loda, and B. J. Rollins. 2000. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404: 407-411.
4. Hancock, W. W., W. Gao, K. L. Faia, and V. Csizmadia. 2000. Chemokines and their receptors in allograft rejection. Curr. Opin. Immunol. 12: 511-516.
5. Murphy, P. M., M. Baggiolini, I. F. Charo, C. A. Hebert, R. Horuk, K. Matsushima, L. H. Miller, J. J. Oppenheim, and C. A. Power. 2000. International Union of Pharmacology, XXII: nomenclature for chemokine receptors. Pharmacol. Rev. 52: 145-176.
6. Luster, A. D. 1998. Chemokines: chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338: 436-445.
7. Foxman, E. F., J. J. Campbell, and E. C. Butcher. 1997. Multistep navigation and the combinatorial control of leukocyte chemotaxis. J. Cell Biol. 139: 1349-1360.
8. Qin, S., J. B. Rottman, P. Myers, N. Kassam, M. Weinblatt, M. Loetscher, A. E. Koch, B. Moser, and C. R. Mackay. 1998. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101: 746-754.
9. Miura, M., K. Morita, H. Kobayashi, T. A. Hamilton, M. D. Burdick, R. M. Strieter, and R. L. Fairchild. 2001. Monokine induced by IFN-γ is a dominant factor directing T cells into murine cardiac allografts during acute rejection. J. Immunol. 167: 3494-3504.
10. Gao, W., P. S. Topham, J. A. King, S. T. Smiley, V. Csizmadia, B. Lu, C. J. Gerard, and W. W. Hancock. 2000. Targeting of the chemokine receptor CCR1 suppresses development of acute and chronic cardiac allograft rejection. J. Clin. Invest. 105: 35-44.
11. Melter, M., A. Exeni, M. I. J. Reinders, J. C. Fang, G. McMahon, P. Ganz, W. W. Hancock, and D. M. Briscoe. 2001. Expression of the chemokine receptor CXCR3 and its ligand IP-10 during human cardiac allograft rejection. Circulation 104: 2558-2564.
12. Fischereder, M., B. Luckow, B. Hocher, R. P. Wuthrich, U. Rothenpieler, H. Schneeberger, U. Panzer, R. A. Stahl, I. A. Hauser, K. Budde, et al. 2001. CC chemokine receptor 5 and renal-transplant survival. Lancet 357: 1758-1761.
13. Zhou, Y., T. Kurihara, R. P. Ryseck, Y. Yang, C. Ryan, J. Loy, G. Warr, and R. Bravo. 1998. Impaired macrophage function and enhanced T cell-dependent immune response in mice lacking CCR5, the mouse homologue of the major HIV-1 coreceptor. J. Immunol. 160: 4018-4025.
14. Kuziel, W. A., S. J. Morgan, T. C. Dawson, S. Griffin, O. Smithies, K. Ley, and N. Maeda. 1997. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl. Acad. Sci. USA 94: 12053-12058.
15. Hancock, W. W., W. Gao, V. Csizmadia, K. L. Faia, N. Shemmeri, and A. D. Luster. 2001. Donor-derived IP-10 initiates development of acute allograft rejection. J. Exp. Med. 193: 975-980.
16. Koga, S., M. B. Aurerbach, T. M. Engeman, A. C. Novick, H. Toma, and R. L. Fairchild. 1999. T cell infiltration into class II MHC-disparate allografts and acute rejection is dependent on the IFN-γ-induced chemokine Mig. J. Immunol. 163: 4878-4885.
17. Hancock, W. W., B. Lu, B. Gao, V. Csizmadia, K. Faia, J. A. King, S. T. Smiley, M. Ling, N. P. Gerard, and C. Gerard. 2000. Requirement of the chemokine receptor CXCR3 for acute allograft rejection. J. Exp. Med. 192: 1515-1519.
18. Gao, W., K. L. Zaia, V. Csizmadia, S. T. Smiley, D. Soler, J. King, T. M. Danoff, and W. W. Hancock. 2001. Beneficial effects of targeting CCR5 in allograft recipients. Transplantation 72: 1199-1205.
19. Veazey, R. S., P. J. Klasse, T. J. Ketas, J. D. Reeves, M. Piatak, Jr., K. Kunstman, S. E. Kuhmann, P. A. Marx, J. D. Lifson, J. Dufour, et al. 2003. Use of a small molecule CCR5 inhibitor in macaques to treat simian immunodeficiency virus infection or prevent simian-human immunodeficiency virus infection. J. Exp. Med. 198: 1551-1562.
20. Wolinsky, S. M., R. S. Veazey, K. J. Kunstman, P. J. Klasse, J. Dufour, A. J. Marozsan, M. S. Springer, and J. P. Moore. 2004. Effect of a CCR5 inhibitor on viral loads in macaques dual-infected with R5 and X4 primate immunodeficiency viruses. Virology 328: 19-29.
21. Hale, J. J., R. J. Budhu, S. G. Mills, M. MacCoss, L. Malkowitz, S. Siciliano, S. L. Gould, J. A. DeMartino, and M. S. Springer. 2001. 1,3,4-Trisubstituted pyrrolidine CCR5 receptor antagonists, part 1: discovery of the pyrrolidine scaffold and determination of its stereochemical requirements. Bioorg. Med. Chem. Lett. 11: 1437-1440.
22. Hale, J. J., R. J. Budhu, E. B. Holson, P. E. Finke, B. Oates, S. G. Mills, M. MacCoss, S. L. Gould, J. A. DeMartino, M. S. Springer, et al. 2001. 1,3,4-Trisubstituted pyrrolidine CCR5 receptor antagonists, part 2: lead optimization affording selective, orally bioavailable compounds with potent anti-HIV activity. Bioorg. Med. Chem. Lett. 11: 2741-2745.
23. National Institutes of Health, Public Health Service. 1985. National Institutes of Health Publication 86-23: Guide for the Care and Use of Laboratory Animals. National Institutes of Health, Bethesda, MD.
24. Socha, W. W., and S. G. Lasano. 1997. Monoclonal antibodies against human blood group related antigens in tests with non-human primate red cells. Transfus. Clin. Biol. 4: 111-114.
25. Blancher, A., M. E. Reid, and W. W. Socha. 2000. Cross-reactivity of antibodies to human and primate red cell antigens. Transfus. Med. Rev. 14: 161-179.
26. Pierson, R. N. III, A. C. Chang, M. G. Blum, K. S. Blair, M. A. Scott, J. B. Atkinson, B. J. Collins, J. P. Zhang, D. W. Thomas, L. C. Burkly, and G. G. Miller. 1999. Prolongation of primate cardiac allograft survival by treatment with ANTI-CD40 ligand (CD154) antibody. Transplantation 68: 1800-1805.
27. Pierson, R. N. III, J. E. Crowe, Jr., S. Pfeiffer, J. Atkinson, A. Azimzadeh, and G. G. Miller. 2001. CD40-ligand in primate cardiac allograft and viral immunity. Immunol. Res. 23: 253-262.
28. Azimzadeh A. M., S. Pfeiffer, G. Wu, C. Schroder, G. L. Zorn, III, S. S. Kelishadi, E. Ozkaynak, M. Kehry, J. B. Atkinson, G. G. Miller, and R. N. Pierson, III. 2006. Alloimmunity in primate heart recipients with CD154 blockade: evidence for alternative costimulation mechanisms. Transplantation 81: 255-264.
29. McLean, I. W., and P. K. Nakane. 1974. Periodate-lysine-paraformaldehyde fixative: a new fixation for immunoelectron microscopy. J. Histochem. Cytochem. 22: 1077-1083.
30. Billingham, M. E., N. R. Cary, M. E. Hammond, J. Kemnitz, C. Marboe, H. A. McCallister, D. C. Snovar, G. L. Winters, and A. Zerbe. 1990. A working formulation for the standardization of nomenclature in the diagnosis of heart and lung rejection: Heart Rejection Study Group. J. Heart Transplant. 6: 587-593.
31. Billingham, M. E. 1992. Histopathology of graft coronary disease. J. Heart Lung Transplant. 11: 38-44.
32. Azimzadeh, A. M., S. Pfeiffer, G. S. Wu, C. Schroder, H. Zhou, G. L. Zorn, III, M. Kehry, G. G. Miller, M. L. Rose, and R. N. Pierson, III. 2005. Humoral immunity to vimentin is associated with cardiac allograft injury in nonhuman primates. Am. J. Transplant. 5: 2349-2359.
33. von Hundelshausen, P., K. S. Weber, Y. Huo, A. E. Proudfoot, P. J. Nelson, K. Ley, and C. Weber. 2002. RANTES desposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 103: 1772-1777.
34. Yun, J. J., M. P. Fischbein, H. Laks, M. C. Fishbein, M. L. Espejo, K. Ebrahimi, Y. Irie, J. Berliner, and A. Ardehali. 2000. Early and late chemokine production correlates with cellular recruitment in cardiac allograft vasculopathy. Transplantation 69: 2515-2524.
35. Yun, J. J., M. P. Fischbein, H. Laks, Y. Irie, M. L. Espejo, M. C. Fishbein, J. A. Berliner, and A. Ardehali. 2001. RANTES production during development of cardiac allograft vasculopathy. Transplantation 71: 1649-1656.
36. Amano, H., A. Bickerstaff, C. G. Orosz, A. C. Novick, H. Toma, and R. L. Fairchild. 2005. Absence of recipient CCR5 promotes early and increased allospecific antibody responses to cardiac allografts. J. Immunol. 174: 6499-6508.
37. Loetscher, M., B. Gerber, P. Loetscher, S. A. Jones, L. Piali, I. Clark-Lewis, M. Baggiolini, and B. Moser. 1996. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J. Exp. Med. 184: 963-969.
38. Sozzni, S., P. Allavena, G. D'Amico, W. Loini, G. Bianchi, M. Kataura, T. Imai, O. Yoshie, R. Bonecchi, and A. Mantovani. 1998. Cutting edge: differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J. Immunol. 161: 1083-1086.
39. Sallusto, F., P. Schaerli, P. Loetscher, C. Schaniel, D. Lenig, C. R. Mackay, S. Qin, and A. Lanzavecchia. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28: 2760-2769.
40. + regulatory T cells during acute graft-versus-host disease. Blood 106: 3300-3307.
41. Roth, J., and G. E. De Souza. 2001. Fever induction pathways: evidence from responses to systemic or local cytokine formation. Braz. J. Med. Biol. Res. 34: 301-314.
42. Dalai, S., and D. S. Zhukovsky. 2006. Pathophysiology and management of fever. J. Support. Oncol. 4: 9-16.
43. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12: 991-1045.
44. Gallucci, S., M. Lolkema, and P. Matzinger. 1999. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 5: 1249-1255.
45. Gallucci, S., and P. Matzinger. 2001. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13: 114-119.
46. Soares, M. P., Y. Lin, K. Sato, K. M. Stuhlmeier, and F. H. Back. 1999. Accommodation. Immunol. Today 20: 434-437.
47. Anderson, C. C., J. M. Carroll, S. Gallucci, J. P. Ridge, A. W. Cheever, and P. Matzinger. 2001. Testing time-, ignorance-, and danger-based models of tolerance. J. Immunol. 166: 3663-3671.
48. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296: 301-305.
49. Pethig, K., B. Heublein, I. Kutschka, and A. Haverich. 2000. Systemic inflammatory response in cardiac allograft vasculopathy: high-sensitive C-reactive protein is associated with progressive luminal obstruction. Circulation 102: 233-236.
50. Bholasingh, R., J. H. Cornel, O. Kamp, J. P. van Straalen, G. T. Sanders, L. Dijksman, J. G. Tijssen, and R. J. de Winter. 2003. The prognostic value of markers of inflammation in patients with troponin T-negative chest pain before discharge from the emergency department. Am. J. Med. 115: 521-528.
51. Kawai, T., M. Seki, K. Hiromatsu, J. W. Eastcott, G. F. Watts, M. Sugai, D. J. Smith, S. A. Porcelli, and M. A. Taubman. 1999. Selective diapedesis of Th1 cells induced by endothelial cell RANTES. J. Immunol. 163: 3269-3278.
52. Horiguchi, K., S. Kitagawa-Sakakida, Y. Sawa, Z. Z. Li, N. Fukushima, R. Shirakura, and H. Matsuda. 2002. Selective chemokine and receptor gene expressions in allografts that develop transplant vasculopathy. J. Heart Lung Transplant. 21: 1090-1100.