Interferon-γ limits Th1 lymphocyte adhesion to inflamed endothelium: A nitric oxide regulatory feedback mechanism

European Journal of Immunology

Volumn 38, Issue 5, 2008, Pages 1368-1380

  Norman, M Ursula ^a,b   Zbytnuik, Lori ^a   Kubes, Paul ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Adhesion; CD4 T cells; Leukocyte recruitment

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; GAMMA INTERFERON RECEPTOR; ICAM1 PROTEIN, MOUSE; INTERFERON RECEPTOR; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NOS2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL INTERACTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CREMASTER MUSCLE; ENDOTHELIUM; FEEDBACK SYSTEM; FLUORESCENCE ANALYSIS; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY MECHANISM; TH1 CELL; ANIMAL; BAGG ALBINO MOUSE; BLOOD FLOW; C57BL MOUSE; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IMMUNOLOGY; LEUKOCYTE ROLLING; MALE; METABOLISM; MOUSE MUTANT; MUSCLE; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; SKIN; TH2 CELL; TRANSPLANTATION; VASCULAR ENDOTHELIUM; VASCULARIZATION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; ENDOTHELIUM, VASCULAR; FEEDBACK, BIOCHEMICAL; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; INTERFERON TYPE II; LEUKOCYTE ROLLING; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLES; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RECEPTORS, INTERFERON; REGIONAL BLOOD FLOW; SKIN; TH1 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 47049125295     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200737847     Document Type: Article

References (46)

1. Szabo, S. J., Sullivan, B. M., Peng, S. L. and Glimcher, L. H., Molecular mechanisms regulating Th1 immune responses. Annu. Rev. Immunol. 2003. 21: 713-758.
2. O'Garra, A. and Arai, N., The molecular basis of T helper 1 and T helper 2 cell differentiation. Trends Cell Biol. 2000. 10: 542-550.
3. Austrup, F., Vestweber, D., Borges, E., Lohning, M., Brauer, R., Herz, U., Renz, H. et al., P- and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflammed tissues. Nature 1997. 385: 81-83.
4. Borges, E., Tietz, W., Steegmaier, M., Moll, T., Hallmann, R., Hamann, A. and Vestweber, D., P-selectin glycoprotein ligand-1 (PSGL-1) on T helper 1 but not on T helper 2 cells binds to P-selectin and supports migration into inflamed skin. J. Exp. Med. 1997. 185: 573-578.
5. + T cells from non-infected and infected tissues. Eur. J. Immunol. 2004. 34: 3070-3081.
6. + memory T cell differentiation. J. Immunol. 1997. 159: 6018-6029.
7. Bonder, C. S., Norman, M. U., Macrae, T., Mangan, P. R., Weaver, C. T., Bullard, D. C., McCafferty, D.M. and Kubes, P., P-selectin can support both Th1 and Th2 lymphocyte rolling in the intestinal microvasculature. Am. J. Pathol. 2005. 167: 1647-1660.
8. Munder, M., Mallo, M., Eichmann, K. and Modolell, M., Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: A novel pathway of autocrine macrophage activation. J. Exp. Med. 1998. 187: 2103-2108.
9. + lymphoid dendritic cells. J. Exp. Med. 1999. 189: 1981-1986.
10. Boehm, U., Klamp, T., Groot, M. and Howard, J. C., Cellular responses to interferon-gamma. Annu. Rev. Immunol. 1997. 15: 749-795.
11. Billiau, A., Heremans, H., Vermeire, K. and Matthys, P., Immunomodulatory properties of interferon-gamma. An update. Ann. N. Y. Acad. Sci. 1998. 856: 22-32.
12. Issekutz, T. B., Effects of six different cytokines on lymphocyte adherence to microvascular endothelium and in vivo lymphocyte migration in the rat. J. Immunol. 1990. 144: 2140-2146.
13. Raab, M., Daxecker, H., Markovic, S., Karimi, A., Griesmacher, A. and Mueller, M. M., Variation of adhesion molecule expression on human umbilical vein endothelial cells upon multiple cytokine application. Clin. Chim. Acta 2002. 321: 11-16.
14. Hillyer, P., Mordelet, E., Flynn, G. and Male, D., Chemokines, chemokine receptors and adhesion molecules on different human endothelia: Discriminating the tissue-specific functions that affect leucocyte migration. Clin. Exp. Immunol. 2003. 134: 431-441.
15. Ding, Z., Xiong, K. and Issekutz, T. B., Regulation of chemokine-induced transendothelial migration of T lymphocytes by endothelial activation: Differential effects on naive and memory T cells. J. Leukoc. Biol. 2000. 67: 825-833.
16. Thornhill, M. H., Wellicome, S. M., Mahiouz, D. L., Lanchbury, J. S., Kyan-Aung, U. and Haskard, D. O., Tumor necrosis factor combines with IL-4 or IFN-gamma to selectively enhance endothelial cell adhesiveness for Tcells. The contribution of vascular cell adhesion molecule-1-dependent and -independent binding mechanisms. J. Immunol. 1991. 146: 592-598.
17. Feuerer, M., Eulenburg, K., Loddenkemper, C., Hamann, A. and Huehn, J., Self-limitation of Th1-mediated inflammation by IFN-gamma. J. Immunol. 2006. 176: 2857-2863.
18. Rosloniec, E. F., Latham, K. and Guedez, Y. B., Paradoxical roles of IFN-gamma in models of Th1-mediated autoimmunity. Arthritis Res. 2002. 4: 333-336.
19. Chu, C. Q., Wittmer, S. and Dalton, D. K., Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 2000. 192: 123-128.
20. Manoury-Schwartz, B., Chiocchia, G., Bessis, N., Abehsira-Amar, O., Batteux, F., Muller, S., Huang, S. et al., High susceptibility to collagen-induced arthritis in mice lacking IFN-gamma receptors. J. Immunol. 1997. 158: 5501-5506.
21. Vermeire, K., Heremans, H., Vandeputte, M., Huang, S., Billiau, A. and Matthys, P., Accelerated collagen-induced arthritis in IFN-gamma receptor-deficient mice. J. Immunol. 1997. 158: 5507-5513.
22. Dalton, D. K., Haynes, L., Chu, C. Q., Swain, S. L. and Wittmer, S., Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J. Exp. Med. 2000. 192: 117-122.
23. + T cell homeostasis. J. Immunol. 2006. 176: 735-739.
24. Refaeli, Y., Van Parijs, L., Alexander, S. I. and Abbas, A. K., Interferon gamma is required for activation-induced death of T lymphocytes. J. Exp. Med. 2002. 196: 999-1005.
25. Tarrant, T. K., Silver, P. B., Wahlsten, J. L., Rizzo, L. V., Chan, C. C., Wiggert, B. and Caspi, R. R., Interleukin 12 protects from a T helper type 1-mediated autoimmune disease, experimental autoimmune uveitis, through a mechanism involving interferon gamma, nitric oxide, and apoptosis. J. Exp. Med. 1999. 189: 219-230.
26. Webb, E. F., Tzimas, M. N., Newsholme, S. J. and Griswold, D. E., Intralesional cytokines in chronic oxazolone-induced contact sensitivity suggest roles for tumor necrosis factor alpha and interleukin-4. J. Invest. Dermatol. 1998. 111: 86-92.
27. Issekutz, T. B., Stoltz, J. M. and van der Meide, P., The recruitment of lymphocytes into the skin by T cell lymphokines: The role of gamma-interferon. Clin. Exp. Immunol. 1988. 73: 70-75.
28. Niedbala,W., Cai, B. and Liew, F. Y., Role of nitric oxide in the regulation of T cell functions. Ann. Rheum. Dis. 2006. 65 Suppl 3: Iii37-iii40.
29. Staykova, M. A., Berven, L. A., Cowden, W. B., Willenborg, D. O. and Crouch, M. F., Nitric oxide induces polarization of actin in encephalitogenic T cells and inhibits their in vitro trans-endothelial migration in a p70S6 kinase-independent manner. FASEB J. 2003. 17: 1337-1339.
30. Sun, Y., Liu, J., Qian, F. and Xu, Q., Nitric oxide inhibits Tcell adhesion and migration by down-regulation of beta1-integrin expression in immunologically liver-injured mice. Int. Immunopharmacol. 2006. 6: 616-626.
31. Wong, D., Prameya, R., Wu, V., Dorovini-Zis, K. and Vincent, S. R., Nitric oxide reduces T lymphocyte adhesion to human brain microvessel endothelial cells via a cGMP-dependent pathway. Eur. J. Pharmacol. 2005. 514: 91-98.
32. Daniel, T., Alexander, M., Hubbard, W. J., Chaudry, I. H., Choudhry, M. A. and Schwacha, M. G., Nitric oxide contributes to the development of a post-injury Th2 T-cell phenotype and immune dysfunction. J. Cell. Physiol. 2006. 208: 418-427.
33. Enn, J. S., Suh, Y. H., Kim, D. K. and Jeon, H., Regulation of cytokine production by exogenous nitric oxide in murine splenocyte and peritoneal macrophage. Arch. Pharm. Res. 2000. 23: 531-534.
34. Miki, S., Takeyama, N., Tanaka, T. and Nakatani, T., Immune dysfunction in endotoxicosis: Role of nitric oxide produced by inducible nitric oxide synthase. Crit. Care Med. 2005. 33: 716-720.
35. Piguet, P. F., Grau, G. E., Hauser, C. and Vassalli, P., Tumor necrosis factor is a critical mediator in hapten induced irritant and contact hypersensitivity reactions. J. Exp. Med. 1991. 173: 673-679.
36. Saulnier, M., Huang, S., Aguet, M. and Ryffel, B., Role of interferon-gamma in contact hypersensitivity assessed in interferon-gamma receptor-deficient mice. Toxicology 1995. 102: 301-312.
37. Itakura, A., Kikuchi, Y., Kouro, T., Ikutani,M., Takaki, S., Askenase, P.W. and Takatsu, K., Interleukin 5 plays an essential role in elicitation of contact sensitivity through dual effects on eosinophils and B-1 cells. Int. Arch. Allergy Immunol. 2006. 140 Suppl 1: 8-16.
38. + T cells. J. Exp. Med. 1996. 183: 1001-1012.
39. Morita, H., Hori, M. and Kitano, Y., Modulation of picryl chloride-induced contact hypersensitivity reaction in mice by nitric oxide. J. Invest. Dermatol. 1996. 107: 549-552.
40. Ross, R., Gillitzer, C., Kleinz, R., Schwing, J., Kleinert, H., Forstermann, U. and Reske-Kunz, A. B., Involvement of NO in contact hypersensitivity. Int. Immunol. 1998. 10: 61-69.
41. Ross, R. and Reske-Kunz, A. B., The role of NO in contact hypersensitivity. Int. Immunopharmacol. 2001. 1: 1469-1478.
42. Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek, J. et al., Immune response in mice that lack the interferon-gamma receptor. Science 1993. 259: 1742-1745.
43. Bonder, C. S., Norman, M. U., Swain, M. G., Zbytnuik, L. D., Yamanouchi, J., Santamaria, P., Ajuebor, M. et al., Rules of recruitment for Th1 and Th2 lymphocytes in inflamed liver: A role for alpha-4 integrin and vascular adhesion protein-1. Immunity 2005. 23: 153-163.
44. Mangan, P. R., O'Quinn, D., Harrington, L., Bonder, C. S., Kubes, P., Kucik, D. F., Bullard, D. C. and Weaver, C. T., Both Th1 and Th2 cells require P-selectin glycoprotein ligand-1 for optimal rolling on inflamed endothelium. Am. J. Pathol. 2005. 167: 1661-1675.
45. Hickey, M. J., Kanwar, S., McCafferty, D. M., Granger, D. N., Eppihimer, M. J. and Kubes, P., Varying roles of E-selectin and P-selectin in different microvascular beds in response to antigen. J. Immunol. 1999. 162: 1137-1143.
46. Bauer, P. R., Van Der Heyde, H. C., Sun, G., Specian, R. D. and Granger, D. N., Regulation of endothelial cell adhesion molecule expression in an experimental model of cerebral malaria. Microcirculation 2002. 9: 463-470.