High IP-10 levels decrease T cell function in HIV-1-infected individuals on ART

Journal of Leukocyte Biology

Volumn 96, Issue 6, 2014, Pages 1055-1063

  Ramirez, L A ^a   Arango, T A ^a   Thompson, E ^a   Naji, M ^a   Tebas, P ^a   Boyer, J D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Antiretroviral therapy; Chemokines; CXCL10; Immune responses; Infection

Indexed keywords

CD40 LIGAND; CHEMOKINE RECEPTOR CXCR3; EOTAXIN; FRACTALKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; ANTIGEN; CXCL10 PROTEIN, HUMAN; CXCR3 PROTEIN, HUMAN; CYTOKINE; HLA ANTIGEN; NEUTRALIZING ANTIBODY; RECOMBINANT PROTEIN;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CALCIUM SIGNALING; CELL FUNCTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSPOT ASSAY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOSTIMULATION; LYMPHOCYTE COUNT; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BLOOD LEVEL; T LYMPHOCYTE; ADULT; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BLOOD; CELL CULTURE; COMPARATIVE STUDY; CYTOTOXICITY; DRUG EFFECTS; HIV INFECTIONS; IMMUNOLOGY; INTERFERON GAMMA RELEASE ASSAY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; YOUNG ADULT;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; ANTI-HIV AGENTS; ANTIBODIES, NEUTRALIZING; ANTIGENS; CALCIUM SIGNALING; CELLS, CULTURED; CHEMOKINE CXCL10; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HIV INFECTIONS; HIV-1; HLA ANTIGENS; HUMANS; INTERFERON-GAMMA RELEASE TESTS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MIDDLE AGED; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CXCR3; RECOMBINANT PROTEINS; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84914132268     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0414-232RR     Document Type: Article

References (41)

1. Katlama, C., Deeks, S. G., Autran, B., Martinez-Picado, J., van Lunzen, J., Rouzioux, C., Miller, M., Vella, S., Schmitz, J. E., Ahlers, J., Richman, D. D., Sekaly, R. P. (2013) Barriers to a cure for HIV: new ways to target and eradicate HIV-1 reservoirs. Lancet 381, 2109-2117.
2. Aberg, J. A. (2012) Aging, inflammation, and HIV infection. Top. Antiviral Med. 20, 101-105.
3. Appay, V., Almeida, J. R., Sauce, D., Autran, B., Papagno, L. (2007) Accelerated immune senescence and HIV-1 infection. Exp. Geron. 42, 432-437.
4. Deeks, S. G. (2009) Immune dysfunction, inflammation, and accelerated aging in patients on antiretroviral therapy. Top. HIV Med. 17, 118-123.
5. Ronsholt, F. F., Ullum, H., Katzenstein, T. L., Gerstoft, J., Ostrowski, S. R. (2013) Persistent inflammation and endothelial activation in HIV-1 infected patients after 12 years of antiretroviral therapy. PLoS One 8, e65182.
6. Dube, M. P., Sattler, F. R. (2010) Inflammation and complications of HIV disease. J. Infect. Dis. 201, 1783-1785.
7. Deeks, S. G. (2011) HIV infection, inflammation, immunosenescence, and aging. Annu. Rev. Med. 62, 141-155.
8. Liu, M., Guo, S., Hibbert, J. M., Jain, V., Singh, N., Wilson, N. O., Stiles, J. K. (2011) CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cyto. Growth Factor Rev. 22, 121-130.
9. Dyer, K. D., Percopo, C. M., Fischer, E. R., Gabryszewski, S. J., Rosenberg, H. F. (2009) Pneumoviruses infect eosinophils and elicit MyD88-dependent release of chemoattractant cytokines and interleukin-6. Blood 114, 2649-2656.
10. Luster, A. D., Ravetch, J. V. (1987) Biochemical characterization of a gamma interferon inducible cytokine (IP-10). J. Exp. Med. 166, 1084-1097.
11. Campbell, J. D., Gangur, V., Simons, F. E., HayGlass, K. T. (2004) Allergic humans are hyporesponsive to a CXCR3 ligand-mediated Th1 immunity-promoting loop. FASEB J. 18, 329-331.
12. Casrouge, A., Bisaux, A., Stephen, L., Schmolz, M., Mapes, J., Pfister, C., Pol, S., Mallet, V., Albert, M. L. (2011) Discrimination of agonist and antagonist forms of CXCL10 in biological samples. J. Trans. Immunol. 167, 137-148.
13. Lacotte, S., Brun, S., Muller, S., Dumortier, H. (2009) CXCR3, inflammation, and autoimmune diseases. Ann. N. Y. Acad. Sci. 1173, 310-317.
14. Lee, E. Y., Lee Z-H., Song, Y. K. (2009) CXCL10 and autoimmune diseases. Autoimmun. Rev. 8, 379-383.
15. Gray, C. M., Hong, H. A., Young, K., Lewis, D. A., Fallows, D., Manca, C., Gilla, K. (2013) Plasma interferon-gamma-inducible protein 10 can be used to predict viral load in HIV-1-infected individuals. J. Acquir. Immune Defic. Syndr. 63, e115-e116.
16. Rahman, S., Connolly, J. E., Manuel, S. L., Chehimi, J., Montaner, L. J., Jain, P. (2011) Unique cytokine/chemokine signatures for HIV-1 and HCV mono-infection versus co-infection as determined by the Luminex analyses. J. Clin. Cell. Immunol. 2, 1-11.
17. Ando, H., Sato, T., Tomaru, U., Yoshida, M., Utsunomiya, A., Yamauchi, J., Araya, N., Yagishita, N., Coler-Reilly, A., Shimizu, Y., Yudoh, K., Hasegawa, Y., Nishioka, K., Nakajima, T., Jacobson, S., Yamano, Y. (2013) Positive feedback loop via astrocytes causes chronic imflammation in virus-associated myelopathy. Brain 136, 2876-2887.
18. Sajadi, S. M., Khoramdelazad, H., Hassanshahi, G., Rafatpanah, H., Hosseini, J., Mahmoodi, M., Arababadi, M. K., Derakhshan, R., Hasheminasabzavareh, R., Hosseini-Zijoud, S. M., Ahmadi, Z. (2013) Plasma levels of CXCL1 (GRO-alpha) and CXCL10 (IP-10) are elevated in type 2 diabetic patients: evidence for the involvement of inflammation and angiogenesis/angiostasis in this disease state. Clin. Lab. 59, 133-137.
19. Hou, F-Q., Wu, X. J., Wang, Y., Chen, J., Liu, Y. Z., Ren, Y. Y., Song, G., Ding, Y-P., Yu, M., Wang, G-Q. (2013) Rapid downregulation of programmed death-1 and interferon-_-inducible protein-10 expression is associated with favourable outcome during antiviral treatment of chronic hepatitis B. J. Viral Hep. 20, 18-26.
20. Qu, J., Zhang, Q., Li, X., Liu, W., Chen, L., Zhu, Y., Wu, J. (2012) The Tat protein of human immunodeficiency virus-1 enhances hepatitis C virus replication through interferon gamma-inducible protein-10. BMC Immunol. 13, 1-12.
21. Chen, L-J., Lv, J., Wen, X-Y., Niu, J-Q. (2013) CXC chemokine IP-10: a key actor in liver disease? Hepatol. Int. 7, 798-804.
22. Ragab, D., Laird, M., Duffy, D., Casrouge, A., Mamdouh, R., Abass, A., Shenawy, D. E., Shebl, A. M., Elkashef, W. F., Zalata, K. R., Kamal, M., Esmat, G., Bonnard, P., Fontanet, A., Rafik, M., Albert, M. L. (2013) CXCL10 antagonism and plasma sDPPIV correlate with increasing liver disease in chronic HCV genotype 4 infected patients. Cytokine 63, 105-112.
23. Casrouge, A., Decalf, J., Ahloulay, M., Lababidi, C., Mansour, H., Vallet-Pichard, A., Mallet, V., Mottez, E., Mapes, J., Fontanet, A., Pol, S., Albert, M. L. (2011) Evidence for an antagonist form of the chemokine CXCL10 in patients chronically infected with HCV. J. Clin. Invest. 121, 308-317.
24. Charles, E. D., Dustin, L. B. (2011) Chemokine antagonism in chronic hepatitis C virus infection. J. Clin. Invest. 121, 25-27.
25. Lajoie, J., Juno, J., Burgener, A., Rahman, S., Mogk, K., Wachihi, C., Mwanjewe, J., Plummer, F. A., Kimani, J., Ball, T. B., Fowke, K. R. (2012) A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Nature 5, 277-287.
26. Liovat, A-S., Rey-Cuille, M-A., Lecuroux, C., Jacquelin, B., Girault, I., Petitjean, G., Zitoun, Y., Venet, A., Barre-Sinoussi, F., Lebon, P., Meyer, L., Sinet, M., Muller-Trutwin, M. (2012) Acute plasma biomarkers of T cell activation set-point levels and disease progression in HIV-1 infection. PLoS One 7, e46143.
27. Bromley, S. K., Peterson, D. A., Gunn, M. D., Dustin, M. L. (2000) Cutting edge: hierarchy of chemokine and TCR signals regulating T cell migration and proliferation. J. Immunol. 165, 15-19.
28. Boyer, J. D., Robinson, T. M., Kutzler, M. A., Parkinson, R., Calarota, S. A., Sidhu, M. K., Muthumani, K., Lewis, M., Pavlakis, G., Felber, B., Weiner, D. (2005) SIV DNA vaccine co-administered with IL-12 expression plasmid enhances CD8 SIV cellular immune responses in cynomolgus macaques. J. Med. Primatol. 34, 262-270.
29. Betts, M. R., Brenchley, J. M., Price, D. A., De Rosa, S. C., Douek, D. C., Roederer, M., Koup, R. A. (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281, 65-78.
30. Streeck, H., Frahm, N., Walker, B. D. (2009) The role of IFN-gamma Elispot assay in HIV vaccine research. Nat. Protoc. 4, 461-469.
31. Gratton, J-P., Morales-Ruiz, M., Kureishi, Y., Fulton, D., Walsh, K., Sessa, W. C. (2001) Akt down-regulation of p38 signaling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J. Biol. Chem. 276, 30359-30365.
32. Kaufmann, D. E., Walker, B. D. (2009) PD-1 and CTLA-4 inhibitory cosignaling pathways in HIV infection and the potential for therapeutic intervention. J. Immunol. 182, 5891-5897.
33. Groom, J. R., Luster, A. D. (2011) CXCR3 in T cell function. Exp. Cell. Res. 317, 620-631.
34. Gorrell, M. D., Zekry, A., McCaughan, G. W., Lloyd, A. (2011) The long and the short of interferon-gamma-inducible protein 10 in hepatitis C virus infection. Hepatology 54, 1875-1879.
35. Soderholm, J., Waldenstrom, J., Askarieh, G., Pilli, M., Bochud P-Y, Negro, F., Pawlotsky, J-M, Zeuzem, S., Ferrari, C., Norkrans, G., Wejstal, R., Westin, J., Neumann, A. U., Haagmans, B. L., Lindh, M., Missale, G., Hellstrand, K., Lagging, M. (2013) Impact of soluble CD26 on treatment outcome and hepatitis C virus-specific T cells in chronic hepatitis C virus genotype 1 infection. PLos One 8, e56991.
36. Taub, D. D., Lloyd, A. R., Conlon, K., Wang, J. M., Ortaldo, J. R., Harada, A., Matsushima, K., Kelvin, D. J., Oppenhaim, J. J. (1993) Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 177, 1809-1814.
37. Newton, P., O’Boyle, G., Jenkins, Y., Ali, S., Kirby, J. A. (2009) T Cell extravasion: demonstration of synergy between activation of CXCR3 and the T cell receptor. Mol. Immunol. 47, 485-492.
38. Rosenblum, J. M., Shimoda, N., Schenk, A. D., Zhang, H., Kish, D. D., Keslar, K., Farber, J. M., Fairchild, R. L. (2010) CXC chemokine ligand (CXCL)9 and CXCL10 are antagonistic costimulation molecules during the priming of alloreactive T cell effectors. J. Immunol. 184, 3450-3460.
39. Migueles, S. A., Weeks, K. A., Nou, E., Berkley, A. M., Rood, J. E., Osborne, C. M., Hallahan, C. W., Cogliano-Shutta, N. A., Metcalf, J. A., McLaughlin, M., Kwan, R., Mican, J. M., Davey R. T., Jr., Connors, M. (2009) Defective human immunodeficiency virus-specific CD8+ T-cell polyfunctionality, proliferation, and cytotoxicity are not restored by antiretroviral therapy. J. Virol. 83, 11876-11889.
40. Shi, Z., Okuno, Y., Rifa’i, M., Enharti, A. T., Akane, K., Isobe, K., Suzuki, H. (2009) Human CD8+ CXCR3+ T cells have the same function as murine CD8+ CD122+ Treg. Eur. J. Immunol. 39, 2106-2119.
41. Papanicolaou, D. A., Wilder, R. L., Manolagas, S. C., Chrousos, G. P. (1998) The pathophysiologic roles of interleukin-6 in human disease. Ann. Intern. Med. 128, 127-137.