CXC chemokine ligand (CXCL) 9 and CXCL10 are antagonistic costimulation molecules during the priming of alloreactive T cell effectors

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3450-3460

  Rosenblum, Joshua M ^a,b   Shimoda, Naohiko ^c   Schenk, Austin D ^a,b   Zhang, Howard ^d   Kish, Danielle D ^b   Keslar, Karen ^b   Farber, Joshua M ^d   Fairchild, Robert L ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c HOKKAIDO UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17;

ALLOGRAFT; ALLOIMMUNITY; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; GRAFT RECIPIENT; HEART TRANSPLANTATION; HISTOINCOMPATIBILITY; INTERFERON PRODUCTION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; T LYMPHOCYTE; ALLOTRANSPLANTATION; ANIMAL; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CELL SEPARATION; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CHEMOKINE CXCL10; CHEMOKINE CXCL9; FLOW CYTOMETRY; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS;

EID: 77951630059     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903831     Document Type: Article

References (54)

1. Heeger, P. S. 2003. T-cell allorecognition and transplant rejection: a summary and update. Am. J. Transplant. 3: 525-533.
2. Hall, B. M., and S. E. Dorsch. 1984. Cells mediating allograft rejection. Immunol. Rev. 77: 31-59.
3. Hidalgo, L. G., and P. F. Halloran. 2002. Role of IFN-gamma in allograft rejection. Crit. Rev. Immunol. 22: 317-349.
4. Larsen, C. P., P. J. Morris, and J. M. Austyn. 1990. Migration of dendritic leukocytes from cardiac allografts into host spleens. A novel pathway for initiation of rejection. J. Exp. Med. 171: 307-314.
5. Trinchieri, G. 1995. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 13: 251-276.
6. Gorbachev, A. V., and R. L. Fairchild. 2004. CD40 engagement enhances antigen-presenting langerhans cell priming of IFN-gamma-producing CD4+ and CD8+ T cells independently of IL-12. J. Immunol. 173: 2443-2452.
7. Agostini, C., F. Calabrese, F. Rea, M. Facco, A. Tosoni, M. Loy, G. Binotto, M. Valente, L. Trentin, and G. Semenzato. 2001. Cxcr3 and its ligand CXCL10 are expressed by inflammatory cells infiltrating lung allografts and mediate chemotaxis of T cells at sites of rejection. Am. J. Pathol. 158: 1703-1711.
8. Duffner, U., B. Lu, G. C. Hildebrandt, T. Teshima, D. L. Williams, P. Reddy, R. Ordemann, S. G. Clouthier, K. Lowler, C. Liu, et al. 2003. Role of CXCR3- induced donor T-cell migration in acute GVHD. Exp. Hematol. 31: 897-902.
9. el-Sawy, T., N. M. Fahmy, and R. L. Fairchild. 2002. Chemokines: directing leukocyte infiltration into allografts. Curr. Opin. Immunol. 14: 562-568.
10. Hancock, W. W., B. Lu, W. 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: 1515-1520.
11. Fahmy, N. M., M. H. Yamani, R. C. Starling, N. B. Ratliff, J. B. Young, P. M. McCarthy, J. Feng, A. C. Novick, and R. L. Fairchild. 2003. Chemokine and receptor-gene expression during early and late acute rejection episodes in human cardiac allografts. Transplantation 75: 2044-2047.
12. Fahmy, N. M., M. H. Yamani, R. C. Starling, N. B. Ratliff, J. B. Young, P. M. McCarthy, J. Feng, A. C. Novick, and R. L. Fairchild. 2003. Chemokine and chemokine receptor gene expression indicates acute rejection of human cardiac transplants. Transplantation 75: 72-78. (Pubitemid 36139698)
13. Hu, H., B. D. Aizenstein, A. Puchalski, J. A. Burmania, M. M. Hamawy, and S. J. Knechtle. 2004. Elevation of CXCR3-binding chemokines in urine indicates acute renal-allograft dysfunction. Am. J. Transplant. 4: 432-437.
14. Miura, M., K. Morita, H. Kobayashi, T. A. Hamilton, M. D. Burdick, R. M. Strieter, and R. L. Fairchild. 2001. Monokine induced by IFN-gamma is a dominant factor directing T cells into murine cardiac allografts during acute rejection. J. Immunol. 167: 3494-3504. (Pubitemid 32852596)
15. Yun, J. J., M. P. Fischbein, D. Whiting, Y. Irie, M. C. Fishbein, M. D. Burdick, J. Belperio, R. M. Strieter, H. Laks, J. A. Berliner, and A. Ardehali. 2002. The role of MIG/CXCL9 in cardiac allograft vasculopathy. Am. J. Pathol. 161: 1307-1313.
16. 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.
17. Kobayashi, H., S. Koga, A. C. Novick, H. Toma, and R. L. Fairchild. 2003. T-cell mediated induction of allogeneic endothelial cell chemokine expression. Transplantation 75: 529-536. (Pubitemid 36241151)
18. Park, M. K., D. Amichay, P. Love, E. Wick, F. Liao, A. Grinberg, R. L. Rabin, H. H. Zhang, S. Gebeyehu, T. M. Wright, et al. 2002. The CXC chemokine murine monokine induced by IFN-gamma (CXC chemokine ligand 9) is made by APCs, targets lymphocytes including activated B cells, and supports antibody responses to a bacterial pathogen in vivo. J. Immunol. 169: 1433-1443.
19. 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.
20. Sallusto, F., C. R. Mackay, and A. Lanzavecchia. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18: 593-620.
21. Whiting, D., G. Hsieh, J. J. Yun, A. Banerji, W. Yao, M. C. Fishbein, J. Belperio, R. M. Strieter, B. Bonavida, and A. Ardehali. 2004. Chemokine monokine induced by IFN-gamma/CXC chemokine ligand 9 stimulates T lymphocyte proliferation and effector cytokine production. J. Immunol. 172: 7417-7424.
22. Campbell, J. D., V. Gangur, F. E. Simons, and K. T. HayGlass. 2004. Allergic humans are hyporesponsive to a CXCR3 ligand-mediated Th1 immunity-promoting loop. FASEB J. 18: 329-331.
23. Gangur, V., F. E. Simons, and K. T. Hayglass. 1998. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-gamma over IL-4 responses. FASEB J. 12: 705-713. (Pubitemid 28247149)
24. Manicone, A. M., K. M. Burkhart, B. Lu, and J. G. Clark. 2008. CXCR3 ligands contribute to Th1-induced inflammation but not to homing of Th1 cells into the lung. Exp. Lung Res. 34: 391-407.
25. Corry, R. J., H. J. Winn, and P. S. Russell. 1973. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16: 343-350.
26. Cui, Y. Z., H. Hisha, G. X. Yang, T. X. Fan, T. Jin, Q. Li, Z. Lian, and S. Ikehara. 2002. Optimal protocol for total body irradiation for allogeneic bone marrow transplantation in mice. Bone Marrow Transplant. 30: 843-849. (Pubitemid 36097472)
27. Afanasyeva, M., D. Georgakopoulos, D. F. Belardi, A. C. Ramsundar, J. G. Barin, D. A. Kass, and N. R. Rose. 2004. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: correlation with cardiac function. Am. J. Pathol. 164: 807-815.
28. Farber, J. M. 1990. A macrophage mRNA selectively induced by gamma-interferon encodes a member of the platelet factor 4 family of cytokines. Proc. Natl. Acad. Sci. USA 87: 5238-5242.
29. Amichay, D., R. T. Gazzinelli, G. Karupiah, T. R. Moench, A. Sher, and J. M. Farber. 1996. Genes for chemokines MuMig and Crg-2 are induced in protozoan and viral infections in response to IFN-gamma with patterns of tissue expression that suggest nonredundant roles in vivo. J. Immunol. 157: 4511-4520. (Pubitemid 126449372)
30. Ebnet, K., M. M. Simon, and S. Shaw. 1996. Regulation of chemokine gene expression in human endothelial cells by proinflammatory cytokines and Borrelia burgdorferi. Ann. N. Y. Acad. Sci. 797: 107-117.
31. Schenk, A. D., J. M. Rosenblum, and R. L. Fairchild. 2008. Chemokine-directed strategies to attenuate allograft rejection. Clin. Lab. Med. 28: 441-454, vii.
32. Akashi, S., M. Sho, H. Kashizuka, K. Hamada, N. Ikeda, Y. Kuzumoto, Y. Tsurui, T. Nomi, T. Mizuno, H. Kanehiro, et al. 2005. A novel small-molecule compound targeting CCR5 and CXCR3 prevents acute and chronic allograft rejection. Transplantation 80: 378-384.
33. Schnickel, G. T., S. Bastani, G. R. Hsieh, A. Shefizadeh, R. Bhatia, M. C. Fishbein, J. Belperio, and A. Ardehali. 2008. Combined CXCR3/CCR5 blockade attenuates acute and chronic rejection. J. Immunol. 180: 4714-4721.
34. Turner, J. E., O. M. Steinmetz, R. A. Stahl, and U. Panzer. 2007. Targeting of Th1-associated chemokine receptors CXCR3 and CCR5 as therapeutic strategy for inflammatory diseases. Mini Rev. Med. Chem. 7: 1089-1096.
35. Wijtmans, M., D. Verzijl, R. Leurs, I. J. de Esch, and M. J. Smit. 2008. Towards small-molecule CXCR3 ligands with clinical potential. ChemMedChem 3: 861-872.
36. Rosenblum, J. M., Q. W. Zhang, G. Siu, T. L. Collins, T. Sullivan, D. J. Dairaghi, J. C. Medina, and R. L. Fairchild. 2009. CXCR3 antagonism impairs the development of donor-reactive, IFN-gamma-producing effectors and prolongs allograft survival. Transplantation 87: 360-369.
37. Dufour, J. H., M. Dziejman, M. T. Liu, J. H. Leung, T. E. Lane, and A. D. Luster. 2002. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 168: 3195-3204.
38. Martín-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 5: 1260-1265.
39. Bajénoff, M., B. Breart, A. Y. Huang, H. Qi, J. Cazareth, V. M. Braud, R. N. Germain, and N. Glaichenhaus. 2006. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 203: 619-631.
40. McNerney, M. E., K. M. Lee, P. Zhou, L. Molinero, M. Mashayekhi, D. Guzior, H. Sattar, S. Kuppireddi, C. R. Wang, V. Kumar, and M. L. Alegre. 2006. Role of natural killer cell subsets in cardiac allograft rejection. Am. J. Transplant. 6: 505-513.
41. Maier, S., C. Tertilt, N. Chambron, K. Gerauer, N. Hüser, C. D. Heidecke, and K. Pfeffer. 2001. Inhibition of natural killer cells results in acceptance of cardiac allografts in CD282/2 mice. Nat. Med. 7: 557-562.
42. Andrassy, M., H. C. Volz, J. C. Igwe, B. Funke, S. N. Eichberger, Z. Kaya, S. Buss, F. Autschbach, S. T. Pleger, I. K. Lukic, et al. 2008. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 117: 3216-3226.
43. Huang, Y., H. Yin, J. Han, B. Huang, J. Xu, F. Zheng, Z. Tan, M. Fang, L. Rui, D. Chen, et al. 2007. Extracellular hmgb1 functions as an innate immune-mediator implicated inmurine cardiac allograft acute rejection. Am. J. Transplant. 7: 799-808.
44. Rao, D. A., and J. S. Pober. 2008. Endothelial injury, alarmins, and allograft rejection. Crit. Rev. Immunol. 28: 229-248.
45. Bishop, D. K., S. Chan Wood, E. J. Eichwald, and C. G. Orosz. 2001. Immunobiology of allograft rejection in the absence of IFN-gamma: CD8+ effector cells develop independently of CD4+ cells and CD40-CD40 ligand interactions. J. Immunol. 166: 3248-3255.
46. Burrell, B. E., K. Csencsits, G. Lu, S. Grabauskiene, and D. K. Bishop. 2008. CD8+ Th17 mediate costimulation blockade-resistant allograft rejection in Tbet- deficient mice. J. Immunol. 181: 3906-3914.
47. Yuan, X., J. Paez-Cortez, I. Schmitt-Knosalla, F. D'Addio, B. Mfarrej, M. Donnarumma, A. Habicht, M. R. Clarkson, J. Iacomini, L. H. Glimcher, et al. 2008. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J. Exp. Med. 205: 3133-3144.
48. Colvin, R. A., G. S. Campanella, L. A. Manice, and A. D. Luster. 2006. CXCR3 requires tyrosine sulfation for ligand binding and a second extracellular loop arginine residue for ligand-induced chemotaxis. Mol. Cell. Biol. 26: 5838-5849.
49. Colvin, R. A., G. S. Campanella, J. Sun, and A. D. Luster. 2004. Intracellular domains of CXCR3 that mediate CXCL9, CXCL10, and CXCL11 function. J. Biol. Chem. 279: 30219-30227.
50. Germain, R. N., M. Bajénoff, F. Castellino, M. Chieppa, J. G. Egen, A. Y. Huang, M. Ishii, L. Y. Koo, and H. Qi. 2008. Making friends in out-of-theway places: how cells of the immune system get together and how they conduct their business as revealed by intravital imaging. Immunol. Rev. 221: 163-181.
51. Bajénoff, M., J. G. Egen, H. Qi, A. Y. Huang, F. Castellino, and R. N. Germain. 2007. Highways, byways and breadcrumbs: directing lymphocyte traffic in the lymph node. Trends Immunol. 28: 346-352. (Pubitemid 47077926)
52. Castellino, F., A. Y. Huang, G. Altan-Bonnet, S. Stoll, C. Scheinecker, and R. N. Germain. 2006. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 440: 890-895.
53. Beuneu, H., Z. Garcia, and P. Bousso. 2006. Cutting edge: cognate CD4 help promotes recruitment of antigen-specific CD8 T cells around dendritic cells. J. Immunol. 177: 1406-1410. (Pubitemid 44092471)
54. Koch, M. A., G. Tucker-Heard, N. R. Perdue, J. R. Killebrew, K. B. Urdahl, and D. J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10: 595-602.