The Journal of Heart and Lung Transplantation
Volume 27, Issue 12 , Pages 1333-1339 , December 2008

CXCL12 Induction of Inducible Nitric Oxide Synthase in Human CD8 T Cells

  • Jonathan C. Choy, PhD

      Affiliations

    • Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut
    • ,
  • Tai Yi, MD, PhD

      Affiliations

    • Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut
    • ,
  • Deepak A. Rao, MPhil

      Affiliations

    • Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut
    • ,
  • George Tellides, MD, PhD

      Affiliations

    • Department of Surgery, Yale University School of Medicine, New Haven, Connecticut
    • ,
  • Karen Fox-Talbot, MA

      Affiliations

    • Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland
    • ,
  • William M. Baldwin III, MD, PhD

      Affiliations

    • Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland
    • ,
  • Jordan S. Pober, MD, PhD

      Affiliations

    • Department of Immunobiology, Yale University School of Medicine, New Haven, Connecticut
    • Department of Pathology, Yale University School of Medicine, New Haven, Connecticut
    • Department of Dermatology, Yale University School of Medicine, New Haven, Connecticut
    • Corresponding Author InformationReprint requests: Jordan S. Pober, MD, PhD, Department of Immunobiology, Yale University School of Medicine, 10 Amistad Street, Room 401D, New Haven, CT 06520-8089. Telephone: 203-737-2292. Fax: 203-737-2293

Received 27 May 2008 ,Revised 20 August 2008 ,Accepted 26 August 2008.

References 

  1. Niedbala W, Wei XQ, Campbell C, et al. Nitric oxide preferentially induces type 1 T cell differentiation by selectively up-regulating IL-12 receptor beta 2 expression via cGMP. Proc Natl Acad Sci USA. 2002;99:16186–16191
  2. Liew FY. Regulation of lymphocyte functions by nitric oxide. Curr Opin Immunol. 1995;7:396–399
  3. Moncada S, Higgs EA. The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol. 2006;147(suppl 1):S193–S201
  4. Koh KP, Wang Y, Yi T, et al. T cell-mediated vascular dysfunction of human allografts results from IFN-gamma dysregulation of NO synthase. J Clin Invest. 2004;114:846–856
  5. Worrall NK, Chang K, Suau GM, et al. Inhibition of inducible nitric oxide synthase prevents myocardial and systemic vascular barrier dysfunction during early cardiac allograft rejection. Circ Res. 1996;78:769–779
  6. Schneemann M, Schoedon G. Species differences in macrophage NO production are important. Nat Immunol. 2002;3:102
  7. Taylor BS, de Vera ME, Ganster RW, et al. Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem. 1998;273:15148–15156
  8. Chan GC, Fish JE, Mawji IA, et al. Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells. J Immunol. 2005;175:3846–3861
  9. Szabolcs MJ, Ravalli S, Minanov O, et al. Apoptosis and increased expression of inducible nitric oxide synthase in human allograft rejection. Transplantation. 1998;65:804–812
  10. Lafond-Walker A, Chen CL, Augustine S, et al. Inducible nitric oxide synthase expression in coronary arteries of transplanted human hearts with accelerated graft arteriosclerosis. Am J Pathol. 1997;151:919–925
  11. Choy JC, Wang Y, Tellides G, Pober JS. Induction of inducible NO synthase in bystander human T cells increases allogeneic responses in the vasculature. Proc Natl Acad Sci USA. 2007;104:1313–1318
  12. Choi J, Enis DR, Koh KP, Shiao SL, Pober JS. T lymphocyte–endothelial cell interactions. Annu Rev Immunol. 2004;22:683–709
  13. Nagasawa T, Hirota S, Tachibana K, et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 1996;382:635–638
  14. Vandervelde S, van Luyn MJ, Tio RA, Harmsen MC. Signaling factors in stem cell-mediated repair of infarcted myocardium. J Mol Cell Cardiol. 2005;39:363–376
  15. Colamussi ML, Secchiero P, Gonelli A, et al. Stromal derived factor-1 alpha (SDF-1 alpha) induces CD4+ T cell apoptosis via the functional up-regulation of the Fas (CD95)/Fas ligand (CD95L) pathway. J Leukoc Biol. 2001;69:263–270
  16. Suzuki Y, Rahman M, Mitsuya H. Diverse transcriptional response of CD4(+) T cells to stromal cell-derived factor (SDF)-1: cell survival promotion and priming effects of SDF-1 on CD4(+) T cells. J Immunol. 2001;167:3064–3073
  17. Melter M, Exeni A, Reinders ME, et al. Expression of the chemokine receptor CXCR3 and its ligand IP-10 during human cardiac allograft rejection. Circulation. 2001;104:2558–2564
  18. Sakihama H, Masunaga T, Yamashita K, et al. Stromal cell-derived factor-1 and CXCR4 interaction is critical for development of transplant arteriosclerosis. Circulation. 2004;110:2924–2930
  19. Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med. 1996;184:1101–1109
  20. Dengler TJ, Pober JS. Human vascular endothelial cells stimulate memory but not naive CD8+ T cells to differentiate into CTL retaining an early activation phenotype. J Immunol. 2000;164:5146–5155
  21. Lorber MI, Wilson JH, Robert ME, et al. Human allogeneic vascular rejection after arterial transplantation and peripheral lymphoid reconstitution in severe combined immunodeficient mice. Transplantation. 1999;67:897–903
  22. Pablos JL, Amara A, Bouloc A, et al. Stromal-cell derived factor is expressed by dendritic cells and endothelium in human skin. Am J Pathol. 1999;155:1577–1586
  23. Bleul CC, Farzan M, Choe H, et al. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature. 1996;382:829–833
  24. Oberlin E, Amara A, Bachelerie F, et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature. 1996;382:833–835
  25. Burns JM, Summers BC, Wang Y, et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med. 2006;203:2201–2213
  26. Nicholson S, Bonecini-Almeida MG, Lapa e Silva JR, et al. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med. 1996;183:2293–2302
  27. Schneemann M, Schoedon G, Hofer S, et al. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis. 1993;167:1358–1363
  28. Weinberg JB, Misukonis MA, Shami PJ, et al. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood. 1995;86:1184–1195
  29. Warke VG, Nambiar MP, Krishnan S, et al. Transcriptional activation of the human inducible nitric-oxide synthase promoter by Kruppel-like factor 6. J Biol Chem. 2003;278:14812–14819
  30. Peacock JW, Jirik FR. TCR activation inhibits chemotaxis toward stromal cell-derived factor-1: evidence for reciprocal regulation between CXCR4 and the TCR. J Immunol. 1999;162:215–223
  31. Manes TD, Shiao SL, Dengler TJ, Pober JS. TCR signaling antagonizes rapid IP-10-mediated transendothelial migration of effector memory CD4+ T cells. J Immunol. 2007;178:3237–3243
  32. Moriuchi M, Moriuchi H, Turner W, Fauci AS. Cloning and analysis of the promoter region of CXCR4, a coreceptor for HIV-1 entry. J Immunol. 1997;159:4322–4329
  33. Kumar A, Humphreys TD, Kremer KN, et al. CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity. 2006;25:213–224
  34. Carding SR, Allan W, McMickle A, Doherty PC. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med. 1993;177:475–482
  35. Tough DF, Borrow P, Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science. 1996;272:1947–1950
  36. Tough DF, Sprent J. Viruses and T cell turnover: evidence for bystander proliferation. Immunol Rev. 1996;150:129–142
  37. Tough DF, Sprent J. Bystander stimulation of T cells in vivo by cytokines. Vet Immunol Immunopathol. 1998;63:123–129
  38. Garnica MR, Silva JS, de Andrade HF. Stromal cell-derived factor-1 production by spleen cells is affected by nitric oxide in protective immunity against blood-stage Plasmodium chabaudi CR in C57BL/6j mice. Immunol Lett. 2003;89:133–142
  39. Hoffmann U, Banas B, Kruger B, et al. SDF-1 expression is elevated in chronic human renal allograft rejection. Clin Transplant. 2006;20:712–718
  40. Yamani MH, Ratliff NB, Cook DJ, et al. Peritransplant ischemic injury is associated with up-regulation of stromal cell-derived factor-1. J Am Coll Cardiol. 2005;46:1029–1035
  41. Kim KW, Cho ML, Kim HR, et al. Up-regulation of stromal cell-derived factor 1 (CXCL12) production in rheumatoid synovial fibroblasts through interactions with T lymphocytes: role of interleukin-17 and CD40L–CD40 interaction. Arthritis Rheum. 2007;56:1076–1086

 Supported by the National Institutes of Health (Grant HL070295 to J.S.P., and G.T., and Grant P01-HL56091 to W.M.B.), a postdoctoral fellowship from the Canadian Institutes of Health Research (J.C.C.), and a research fellowship from the International Society for Heart and Lung Transplantation (J.C.C.).

PII: S1053-2498(08)00644-X

doi: 10.1016/j.healun.2008.08.014

The Journal of Heart and Lung Transplantation
Volume 27, Issue 12 , Pages 1333-1339 , December 2008

Article Tools

* Image Usage & Resolution