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Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Human Immunodeficiency Virus | Research

The combination of CXCL9, CXCL10 and CXCL11 levels during primary HIV infection predicts HIV disease progression

Authors: Xiaowan Yin, Zhuo Wang, Tong Wu, Meichen Ma, Zining Zhang, Zhenxing Chu, Qinghai Hu, Haibo Ding, Xiaoxu Han, Junjie Xu, Hong Shang, Yongjun Jiang

Published in: Journal of Translational Medicine | Issue 1/2019

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Abstract

Background

Chemokines are small chemotactic cytokines involved in inflammation, cell migration, and immune regulation in both physiological and pathological contexts. Here, we investigated the profile of chemokines during primary HIV infection (PHI).

Methods

Fifty-four participants with blood samples before and during HIV infection and clinical information available were selected from an HIV-negative man who have sex with men (MSM) prospective cohort. Thirty chemokines and 10 cytokines were measured pre- and post-HIV infection in the same individuals using a Bio-Plex Pro™ Human Chemokine Panel.

Results

Levels of 18 chemokines/cytokines changed significantly during PHI relative to pre-HIV infection levels; 14 were up-regulated and 4 down-regulated. Among them, CXCL9, CXCL10, and CXCL11 were the most prominently raised. Levels of CXCL9 and CXCL10 were much higher in the high-set point group (log viral load (lgVL) ≥ 4.5) than those in the low-set point group (lgVL < 4.5) and levels of CXCL9, CXCL10, and CXCL11 were higher in the low-CD4+ T-cell count group (CD4+ T-cell count ≥ 500). A formula to predict HIV disease progression using a combination panel comprising CXCL9, CXCL10, and CXCL11 was developed, where risk score = 0.007 × CXCL9 + 0.004 × CXCL10 − 0.033 × CXCL11 − 1.724, with risk score values higher than the cutoff threshold (0.5211) indicating more rapid HIV disease progression.

Conclusions

A panel of plasma CXCL9, CXCL10, and CXCL11 measured during primary HIV-1 infection could predict long-term HIV disease prognosis in an MSM group and has potential as a novel biomarker in the clinic.
Literature
1.
go back to reference Mellado M, Rodriguez-Frade JM, Vila-Coro AJ, de Ana AM, Martinez AC. Chemokine control of HIV-1 infection. Nature. 1999;400:723–4.PubMedCrossRef Mellado M, Rodriguez-Frade JM, Vila-Coro AJ, de Ana AM, Martinez AC. Chemokine control of HIV-1 infection. Nature. 1999;400:723–4.PubMedCrossRef
2.
go back to reference Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000;12:121–7.PubMedCrossRef Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000;12:121–7.PubMedCrossRef
3.
go back to reference Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol. 2014;32:659–702.PubMedCrossRef Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol. 2014;32:659–702.PubMedCrossRef
4.
go back to reference Stone MJ, Hayward JA, Huang C, Huma Z, Sanchez J. Mechanisms of Regulation of the chemokine-receptor network. Int J Mol Sci. 2017;18:342.PubMedCentralCrossRef Stone MJ, Hayward JA, Huang C, Huma Z, Sanchez J. Mechanisms of Regulation of the chemokine-receptor network. Int J Mol Sci. 2017;18:342.PubMedCentralCrossRef
6.
go back to reference Beer F, Kuo CH, Morohoshi K, Goodliffe J, Munro P, Aye CC, Dawson M, Richardson RM, Jones LH, Ikeda Y, et al. Role of beta-chemokines in mast cell activation and type I hypersensitivity reactions in the conjunctiva: in vivo and in vitro studies. Immunol Rev. 2007;217:96–104.PubMedCrossRef Beer F, Kuo CH, Morohoshi K, Goodliffe J, Munro P, Aye CC, Dawson M, Richardson RM, Jones LH, Ikeda Y, et al. Role of beta-chemokines in mast cell activation and type I hypersensitivity reactions in the conjunctiva: in vivo and in vitro studies. Immunol Rev. 2007;217:96–104.PubMedCrossRef
7.
go back to reference Choi J, Selmi C, Leung PS, Kenny TP, Roskams T, Gershwin ME. Chemokine and chemokine receptors in autoimmunity: the case of primary biliary cholangitis. Expert Rev Clin Immunol. 2016;12:661–72.PubMedPubMedCentralCrossRef Choi J, Selmi C, Leung PS, Kenny TP, Roskams T, Gershwin ME. Chemokine and chemokine receptors in autoimmunity: the case of primary biliary cholangitis. Expert Rev Clin Immunol. 2016;12:661–72.PubMedPubMedCentralCrossRef
8.
go back to reference Nagarsheth N, Wicha MS, Zou W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat Rev Immunol. 2017;17:559–72.PubMedPubMedCentralCrossRef Nagarsheth N, Wicha MS, Zou W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat Rev Immunol. 2017;17:559–72.PubMedPubMedCentralCrossRef
9.
go back to reference Olsen RS, Nijm J, Andersson RE, Dimberg J, Wagsater D. Circulating inflammatory factors associated with worse long-term prognosis in colorectal cancer. World J Gastroenterol. 2017;23:6212–9.PubMedPubMedCentralCrossRef Olsen RS, Nijm J, Andersson RE, Dimberg J, Wagsater D. Circulating inflammatory factors associated with worse long-term prognosis in colorectal cancer. World J Gastroenterol. 2017;23:6212–9.PubMedPubMedCentralCrossRef
10.
go back to reference Weisheng B, Nezhat CH, Huang GF, Mao YQ, Sidell N, Huang RP. Discovering endometriosis biomarkers with multiplex cytokine arrays. Clin Proteomics. 2019;16:28.PubMedPubMedCentralCrossRef Weisheng B, Nezhat CH, Huang GF, Mao YQ, Sidell N, Huang RP. Discovering endometriosis biomarkers with multiplex cytokine arrays. Clin Proteomics. 2019;16:28.PubMedPubMedCentralCrossRef
11.
go back to reference Visser ME, Durao S, Sinclair D, Irlam JH, Siegfried N. Micronutrient supplementation in adults with HIV infection. Cochrane Database Syst Rev. 2017;5:CD003650.PubMed Visser ME, Durao S, Sinclair D, Irlam JH, Siegfried N. Micronutrient supplementation in adults with HIV infection. Cochrane Database Syst Rev. 2017;5:CD003650.PubMed
12.
go back to reference Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol. 1994;68:6103–10.PubMedPubMedCentral Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol. 1994;68:6103–10.PubMedPubMedCentral
13.
go back to reference Wilson JD, Ogg GS, Allen RL, Davis C, Shaunak S, Downie J, Dyer W, Workman C, Sullivan S, McMichael AJ, Rowland-Jones SL. Direct visualization of HIV-1-specific cytotoxic T lymphocytes during primary infection. AIDS. 2000;14:225–33.PubMedCrossRef Wilson JD, Ogg GS, Allen RL, Davis C, Shaunak S, Downie J, Dyer W, Workman C, Sullivan S, McMichael AJ, Rowland-Jones SL. Direct visualization of HIV-1-specific cytotoxic T lymphocytes during primary infection. AIDS. 2000;14:225–33.PubMedCrossRef
14.
go back to reference McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol. 2010;10:11–23.PubMedCrossRef McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol. 2010;10:11–23.PubMedCrossRef
15.
go back to reference Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV. Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16:83–92.PubMedCrossRef Liu Z, Cumberland WG, Hultin LE, Prince HE, Detels R, Giorgi JV. Elevated CD38 antigen expression on CD8+ T cells is a stronger marker for the risk of chronic HIV disease progression to AIDS and death in the Multicenter AIDS Cohort Study than CD4+ cell count, soluble immune activation markers, or combinations of HLA-DR and CD38 expression. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16:83–92.PubMedCrossRef
16.
go back to reference Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, Hunt P, Martin JN, Kahn JO, Levy J, et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood. 2004;104:942–7.PubMedCrossRef Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, Hunt P, Martin JN, Kahn JO, Levy J, et al. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood. 2004;104:942–7.PubMedCrossRef
17.
18.
19.
go back to reference Descours B, Petitjean G, Lopez-Zaragoza JL, Bruel T, Raffel R, Psomas C, Reynes J, Lacabaratz C, Levy Y, Schwartz O, et al. CD32a is a marker of a CD4 T-cell HIV reservoir harbouring replication-competent proviruses. Nature. 2017;543:564–7.PubMedCrossRef Descours B, Petitjean G, Lopez-Zaragoza JL, Bruel T, Raffel R, Psomas C, Reynes J, Lacabaratz C, Levy Y, Schwartz O, et al. CD32a is a marker of a CD4 T-cell HIV reservoir harbouring replication-competent proviruses. Nature. 2017;543:564–7.PubMedCrossRef
20.
go back to reference Wang Z, Shang H, Jiang Y. Chemokines and chemokine receptors: accomplices for human immunodeficiency virus infection and latency. Front Immunol. 2017;8:1274.PubMedPubMedCentralCrossRef Wang Z, Shang H, Jiang Y. Chemokines and chemokine receptors: accomplices for human immunodeficiency virus infection and latency. Front Immunol. 2017;8:1274.PubMedPubMedCentralCrossRef
21.
go back to reference Keating SM, Heitman JW, Wu S, Deng X, Stacey AR, Zahn RC, de la Rosa M, Finstad SL, Lifson JD, Piatak M Jr, et al. Magnitude and quality of cytokine and chemokine storm during acute infection distinguish nonprogressive and progressive simian immunodeficiency virus infections of nonhuman primates. J Virol. 2016;90:10339–50.PubMedPubMedCentralCrossRef Keating SM, Heitman JW, Wu S, Deng X, Stacey AR, Zahn RC, de la Rosa M, Finstad SL, Lifson JD, Piatak M Jr, et al. Magnitude and quality of cytokine and chemokine storm during acute infection distinguish nonprogressive and progressive simian immunodeficiency virus infections of nonhuman primates. J Virol. 2016;90:10339–50.PubMedPubMedCentralCrossRef
22.
go back to reference Liovat AS, Rey-Cuille MA, Lecuroux C, Jacquelin B, Girault I, Petitjean G, Zitoun Y, Venet A, Barre-Sinoussi F, Lebon P, et al. Acute plasma biomarkers of T cell activation set-point levels and of disease progression in HIV-1 infection. PLoS ONE. 2012;7:e46143.PubMedPubMedCentralCrossRef Liovat AS, Rey-Cuille MA, Lecuroux C, Jacquelin B, Girault I, Petitjean G, Zitoun Y, Venet A, Barre-Sinoussi F, Lebon P, et al. Acute plasma biomarkers of T cell activation set-point levels and of disease progression in HIV-1 infection. PLoS ONE. 2012;7:e46143.PubMedPubMedCentralCrossRef
23.
go back to reference Huang X, Liu X, Meyers K, Liu L, Su B, Wang P, Li Z, Li L, Zhang T, Li N, et al. Cytokine cascade and networks among MSM HIV seroconverters: implications for early immunotherapy. Sci Rep. 2016;6:36234.PubMedPubMedCentralCrossRef Huang X, Liu X, Meyers K, Liu L, Su B, Wang P, Li Z, Li L, Zhang T, Li N, et al. Cytokine cascade and networks among MSM HIV seroconverters: implications for early immunotherapy. Sci Rep. 2016;6:36234.PubMedPubMedCentralCrossRef
24.
go back to reference Roberts L, Passmore JA, Williamson C, Little F, Bebell LM, Mlisana K, Burgers WA, van Loggerenberg F, Walzl G, Djoba Siawaya JF, et al. Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression. AIDS. 2010;24:819–31.PubMedCrossRef Roberts L, Passmore JA, Williamson C, Little F, Bebell LM, Mlisana K, Burgers WA, van Loggerenberg F, Walzl G, Djoba Siawaya JF, et al. Plasma cytokine levels during acute HIV-1 infection predict HIV disease progression. AIDS. 2010;24:819–31.PubMedCrossRef
25.
go back to reference Chen X, Lin M, Qian S, Zhang Z, Fu Y, Xu J, Han X, Ding H, Dong T, Shang H, Jiang Y. The early antibody-dependent cell-mediated cytotoxicity response is associated with lower viral set point in individuals with primary HIV infection. Front Immunol. 2018;9:2322.PubMedPubMedCentralCrossRef Chen X, Lin M, Qian S, Zhang Z, Fu Y, Xu J, Han X, Ding H, Dong T, Shang H, Jiang Y. The early antibody-dependent cell-mediated cytotoxicity response is associated with lower viral set point in individuals with primary HIV infection. Front Immunol. 2018;9:2322.PubMedPubMedCentralCrossRef
26.
go back to reference Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, Heldebrant C, Smith R, Conrad A, Kleinman SH, Busch MP. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS. 2003;17:1871–9.PubMedCrossRef Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, Heldebrant C, Smith R, Conrad A, Kleinman SH, Busch MP. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS. 2003;17:1871–9.PubMedCrossRef
27.
go back to reference Muller M, Carter S, Hofer MJ, Campbell IL. Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity–a tale of conflict and conundrum. Neuropathol Appl Neurobiol. 2010;36:368–87.PubMedCrossRef Muller M, Carter S, Hofer MJ, Campbell IL. Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity–a tale of conflict and conundrum. Neuropathol Appl Neurobiol. 2010;36:368–87.PubMedCrossRef
28.
go back to reference Van Raemdonck K, Van den Steen PE, Liekens S, Van Damme J, Struyf S. CXCR3 ligands in disease and therapy. Cytokine Growth Factor Rev. 2015;26:311–27.PubMedCrossRef Van Raemdonck K, Van den Steen PE, Liekens S, Van Damme J, Struyf S. CXCR3 ligands in disease and therapy. Cytokine Growth Factor Rev. 2015;26:311–27.PubMedCrossRef
29.
go back to reference Rabin RL, Park MK, Liao F, Swofford R, Stephany D, Farber JM. Chemokine receptor responses on T cells are achieved through regulation of both receptor expression and signaling. J Immunol. 1999;162:3840–50.PubMed Rabin RL, Park MK, Liao F, Swofford R, Stephany D, Farber JM. Chemokine receptor responses on T cells are achieved through regulation of both receptor expression and signaling. J Immunol. 1999;162:3840–50.PubMed
30.
go back to reference Struyf S, Proost P, Van Damme J. Regulation of the immune response by the interaction of chemokines and proteases. Adv Immunol. 2003;81:1–44.PubMedCrossRef Struyf S, Proost P, Van Damme J. Regulation of the immune response by the interaction of chemokines and proteases. Adv Immunol. 2003;81:1–44.PubMedCrossRef
31.
32.
go back to reference Muthuswamy R, Urban J, Lee JJ, Reinhart TA, Bartlett D, Kalinski P. Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res. 2008;68:5972–8.PubMedPubMedCentralCrossRef Muthuswamy R, Urban J, Lee JJ, Reinhart TA, Bartlett D, Kalinski P. Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res. 2008;68:5972–8.PubMedPubMedCentralCrossRef
33.
go back to reference Smit MJ, Verdijk P, van der Raaij-Helmer EM, Navis M, Hensbergen PJ, Leurs R, Tensen CP. CXCR3-mediated chemotaxis of human T cells is regulated by a Gi- and phospholipase C-dependent pathway and not via activation of MEK/p44/p42 MAPK nor Akt/PI-3 kinase. Blood. 2003;102:1959–65.PubMedCrossRef Smit MJ, Verdijk P, van der Raaij-Helmer EM, Navis M, Hensbergen PJ, Leurs R, Tensen CP. CXCR3-mediated chemotaxis of human T cells is regulated by a Gi- and phospholipase C-dependent pathway and not via activation of MEK/p44/p42 MAPK nor Akt/PI-3 kinase. Blood. 2003;102:1959–65.PubMedCrossRef
34.
go back to reference Tworek D, Kuna P, Mlynarski W, Gorski P, Pietras T, Antczak A. MIG (CXCL9), IP-10 (CXCL10) and I-TAC (CXCL11) concentrations after nasal allergen challenge in patients with allergic rhinitis. Arch Med Sci. 2013;9:849–53.PubMedPubMedCentralCrossRef Tworek D, Kuna P, Mlynarski W, Gorski P, Pietras T, Antczak A. MIG (CXCL9), IP-10 (CXCL10) and I-TAC (CXCL11) concentrations after nasal allergen challenge in patients with allergic rhinitis. Arch Med Sci. 2013;9:849–53.PubMedPubMedCentralCrossRef
35.
go back to reference Ikeda A, Aoki N, Kido M, Iwamoto S, Nishiura H, Maruoka R, Chiba T, Watanabe N. Progression of autoimmune hepatitis is mediated by IL-18-producing dendritic cells and hepatic CXCL9 expression in mice. Hepatology. 2014;60:224–36.PubMedCrossRef Ikeda A, Aoki N, Kido M, Iwamoto S, Nishiura H, Maruoka R, Chiba T, Watanabe N. Progression of autoimmune hepatitis is mediated by IL-18-producing dendritic cells and hepatic CXCL9 expression in mice. Hepatology. 2014;60:224–36.PubMedCrossRef
36.
go back to reference Holt AP, Haughton EL, Lalor PF, Filer A, Buckley CD, Adams DH. Liver myofibroblasts regulate infiltration and positioning of lymphocytes in human liver. Gastroenterology. 2009;136:705–14.PubMedCrossRef Holt AP, Haughton EL, Lalor PF, Filer A, Buckley CD, Adams DH. Liver myofibroblasts regulate infiltration and positioning of lymphocytes in human liver. Gastroenterology. 2009;136:705–14.PubMedCrossRef
37.
go back to reference Vandercappellen J, Van Damme J, Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett. 2008;267:226–44.PubMedCrossRef Vandercappellen J, Van Damme J, Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett. 2008;267:226–44.PubMedCrossRef
38.
go back to reference Huang W, Hu K, Luo S, Zhang M, Li C, Jin W, Liu Y, Griffin GE, Shattock RJ, Hu Q. Herpes simplex virus type 2 infection of human epithelial cells induces CXCL9 expression and CD4+ T cell migration via activation of p38-CCAAT/enhancer-binding protein-beta pathway. J Immunol. 2012;188:6247–57.PubMedCrossRef Huang W, Hu K, Luo S, Zhang M, Li C, Jin W, Liu Y, Griffin GE, Shattock RJ, Hu Q. Herpes simplex virus type 2 infection of human epithelial cells induces CXCL9 expression and CD4+ T cell migration via activation of p38-CCAAT/enhancer-binding protein-beta pathway. J Immunol. 2012;188:6247–57.PubMedCrossRef
39.
go back to reference Allers K, Fehr M, Conrad K, Epple HJ, Schurmann D, Geelhaar-Karsch A, Schinnerling K, Moos V, Schneider T. Macrophages accumulate in the gut mucosa of untreated HIV-infected patients. J Infect Dis. 2014;209:739–48.PubMedCrossRef Allers K, Fehr M, Conrad K, Epple HJ, Schurmann D, Geelhaar-Karsch A, Schinnerling K, Moos V, Schneider T. Macrophages accumulate in the gut mucosa of untreated HIV-infected patients. J Infect Dis. 2014;209:739–48.PubMedCrossRef
40.
go back to reference Vanpouille C, Introini A, Morris SR, Margolis L, Daar ES, Dube MP, Little SJ, Smith DM, Lisco A, Gianella S. Distinct cytokine/chemokine network in semen and blood characterize different stages of HIV infection. AIDS. 2016;30:193–201.PubMedCrossRef Vanpouille C, Introini A, Morris SR, Margolis L, Daar ES, Dube MP, Little SJ, Smith DM, Lisco A, Gianella S. Distinct cytokine/chemokine network in semen and blood characterize different stages of HIV infection. AIDS. 2016;30:193–201.PubMedCrossRef
41.
go back to reference Pereira NZ, Cardoso EC, Oliveira LM, de Lima JF, Branco AC, Ruocco RM, Zugaib M, de Oliveira Filho JB, Duarte AJ, Sato MN. Upregulation of innate antiviral restricting factor expression in the cord blood and decidual tissue of HIV-infected mothers. PLoS ONE. 2013;8:e84917.PubMedPubMedCentralCrossRef Pereira NZ, Cardoso EC, Oliveira LM, de Lima JF, Branco AC, Ruocco RM, Zugaib M, de Oliveira Filho JB, Duarte AJ, Sato MN. Upregulation of innate antiviral restricting factor expression in the cord blood and decidual tissue of HIV-infected mothers. PLoS ONE. 2013;8:e84917.PubMedPubMedCentralCrossRef
42.
go back to reference Milush JM, Stefano-Cole K, Schmidt K, Durudas A, Pandrea I, Sodora DL. Mucosal innate immune response associated with a timely humoral immune response and slower disease progression after oral transmission of simian immunodeficiency virus to rhesus macaques. J Virol. 2007;81:6175–86.PubMedPubMedCentralCrossRef Milush JM, Stefano-Cole K, Schmidt K, Durudas A, Pandrea I, Sodora DL. Mucosal innate immune response associated with a timely humoral immune response and slower disease progression after oral transmission of simian immunodeficiency virus to rhesus macaques. J Virol. 2007;81:6175–86.PubMedPubMedCentralCrossRef
43.
go back to reference Macura SL, Lathrop MJ, Gui J, Doncel GF, Asin SN, Rollenhagen C. Blocking CXCL9 decreases HIV-1 replication and enhances the activity of prophylactic antiretrovirals in human cervical tissues. J Acquir Immune Defic Syndr. 2016;71:474–82.PubMedPubMedCentralCrossRef Macura SL, Lathrop MJ, Gui J, Doncel GF, Asin SN, Rollenhagen C. Blocking CXCL9 decreases HIV-1 replication and enhances the activity of prophylactic antiretrovirals in human cervical tissues. J Acquir Immune Defic Syndr. 2016;71:474–82.PubMedPubMedCentralCrossRef
44.
go back to reference Lajoie J, Juno J, Burgener A, Rahman S, Mogk K, Wachihi C, Mwanjewe J, Plummer FA, Kimani J, Ball TB, Fowke KR. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 2012;5:277–87.PubMedCrossRef Lajoie J, Juno J, Burgener A, Rahman S, Mogk K, Wachihi C, Mwanjewe J, Plummer FA, Kimani J, Ball TB, Fowke KR. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 2012;5:277–87.PubMedCrossRef
45.
go back to reference Yoder A, Yu D, Dong L, Iyer SR, Xu X, Kelly J, Liu J, Wang W, Vorster PJ, Agulto L, et al. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell. 2008;134:782–92.PubMedPubMedCentralCrossRef Yoder A, Yu D, Dong L, Iyer SR, Xu X, Kelly J, Liu J, Wang W, Vorster PJ, Agulto L, et al. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell. 2008;134:782–92.PubMedPubMedCentralCrossRef
46.
go back to reference Cassenote AJF, Grangeiro A, Escuder MM, Abe JM, Segurado AAC. Validation of CD4(+) T-cell and viral load data from the HIV-Brazil Cohort Study using secondary system data. BMC Infect Dis. 2018;18:617.PubMedPubMedCentralCrossRef Cassenote AJF, Grangeiro A, Escuder MM, Abe JM, Segurado AAC. Validation of CD4(+) T-cell and viral load data from the HIV-Brazil Cohort Study using secondary system data. BMC Infect Dis. 2018;18:617.PubMedPubMedCentralCrossRef
47.
go back to reference Pastor L, Urrea V, Carrillo J, Parker E, Fuente-Soro L, Jairoce C, Mandomando I, Naniche D, Blanco J. Dynamics of CD4 and CD8 T-Cell subsets and inflammatory biomarkers during early and chronic HIV infection in mozambican adults. Front Immunol. 1925;2017:8. Pastor L, Urrea V, Carrillo J, Parker E, Fuente-Soro L, Jairoce C, Mandomando I, Naniche D, Blanco J. Dynamics of CD4 and CD8 T-Cell subsets and inflammatory biomarkers during early and chronic HIV infection in mozambican adults. Front Immunol. 1925;2017:8.
48.
go back to reference Romagnani P, Crescioli C. CXCL10: a candidate biomarker in transplantation. Clin Chim Acta. 2012;413:1364–73.PubMedCrossRef Romagnani P, Crescioli C. CXCL10: a candidate biomarker in transplantation. Clin Chim Acta. 2012;413:1364–73.PubMedCrossRef
49.
go back to reference You E, Kim MH, Lee WI, Kang SY. Evaluation of IL-2, IL-10, IL-17 and IP-10 as potent discriminative markers for active tuberculosis among pulmonary tuberculosis suspects. Tuberculosis. 2016;99:100–8.PubMedCrossRef You E, Kim MH, Lee WI, Kang SY. Evaluation of IL-2, IL-10, IL-17 and IP-10 as potent discriminative markers for active tuberculosis among pulmonary tuberculosis suspects. Tuberculosis. 2016;99:100–8.PubMedCrossRef
50.
51.
go back to reference Lunardi S, Lim SY, Muschel RJ, Brunner TB. IP-10/CXCL10 attracts regulatory T cells: implication for pancreatic cancer. Oncoimmunology. 2015;4:e1027473.PubMedPubMedCentralCrossRef Lunardi S, Lim SY, Muschel RJ, Brunner TB. IP-10/CXCL10 attracts regulatory T cells: implication for pancreatic cancer. Oncoimmunology. 2015;4:e1027473.PubMedPubMedCentralCrossRef
52.
go back to reference Antonelli A, Ferrari SM, Corrado A, Ferrannini E, Fallahi P. CXCR3, CXCL10 and type 1 diabetes. Cytokine Growth Factor Rev. 2014;25:57–65.PubMedCrossRef Antonelli A, Ferrari SM, Corrado A, Ferrannini E, Fallahi P. CXCR3, CXCL10 and type 1 diabetes. Cytokine Growth Factor Rev. 2014;25:57–65.PubMedCrossRef
53.
go back to reference Singh UP, Singh NP, Guan H, Hegde VL, Price RL, Taub DD, Mishra MK, Nagarkatti M, Nagarkatti PS. The severity of experimental autoimmune cystitis can be ameliorated by anti-CXCL10 Ab treatment. PLoS ONE. 2013;8:e79751.PubMedPubMedCentralCrossRef Singh UP, Singh NP, Guan H, Hegde VL, Price RL, Taub DD, Mishra MK, Nagarkatti M, Nagarkatti PS. The severity of experimental autoimmune cystitis can be ameliorated by anti-CXCL10 Ab treatment. PLoS ONE. 2013;8:e79751.PubMedPubMedCentralCrossRef
54.
go back to reference Ploquin MJ, Madec Y, Casrouge A, Huot N, Passaes C, Lecuroux C, Essat A, Boufassa F, Jacquelin B, Jochems SP, et al. Elevated basal pre-infection CXCL10 in plasma and in the small intestine after infection are associated with more rapid HIV/SIV disease onset. PLoS Pathog. 2016;12:e1005774.PubMedPubMedCentralCrossRef Ploquin MJ, Madec Y, Casrouge A, Huot N, Passaes C, Lecuroux C, Essat A, Boufassa F, Jacquelin B, Jochems SP, et al. Elevated basal pre-infection CXCL10 in plasma and in the small intestine after infection are associated with more rapid HIV/SIV disease onset. PLoS Pathog. 2016;12:e1005774.PubMedPubMedCentralCrossRef
55.
go back to reference Ramirez LA, Arango TA, Thompson E, Naji M, Tebas P, Boyer JD. High IP-10 levels decrease T cell function in HIV-1-infected individuals on ART. J Leukoc Biol. 2014;96:1055–63.PubMedPubMedCentralCrossRef Ramirez LA, Arango TA, Thompson E, Naji M, Tebas P, Boyer JD. High IP-10 levels decrease T cell function in HIV-1-infected individuals on ART. J Leukoc Biol. 2014;96:1055–63.PubMedPubMedCentralCrossRef
56.
go back to reference Wang Z, Wu T, Ma M, Zhang Z, Fu Y, Liu J, Xu J, Ding H, Han X, Chu Z, et al. Elevated interferon-gamma-induced protein 10 and its receptor CXCR3 impair NK cell function during HIV infection. J Leukoc Biol. 2017;102:163–70.PubMedCrossRef Wang Z, Wu T, Ma M, Zhang Z, Fu Y, Liu J, Xu J, Ding H, Han X, Chu Z, et al. Elevated interferon-gamma-induced protein 10 and its receptor CXCR3 impair NK cell function during HIV infection. J Leukoc Biol. 2017;102:163–70.PubMedCrossRef
57.
go back to reference Cecchinato V, Bernasconi E, Speck RF, Proietti M, Sauermann U, D’Agostino G, Danelon G, Rezzonico Jost T, Grassi F, Raeli L, et al. Impairment of CCR6+ and CXCR3+ Th cell migration in HIV-1 infection is rescued by modulating actin polymerization. J Immunol. 2017;198:184–95.PubMedCrossRef Cecchinato V, Bernasconi E, Speck RF, Proietti M, Sauermann U, D’Agostino G, Danelon G, Rezzonico Jost T, Grassi F, Raeli L, et al. Impairment of CCR6+ and CXCR3+ Th cell migration in HIV-1 infection is rescued by modulating actin polymerization. J Immunol. 2017;198:184–95.PubMedCrossRef
58.
go back to reference Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, Lin W, Boyd JG, Moser B, Wood DE, et al. Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med. 1998;187:2009–21.PubMedPubMedCentralCrossRef Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, Gladue RP, Lin W, Boyd JG, Moser B, Wood DE, et al. Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med. 1998;187:2009–21.PubMedPubMedCentralCrossRef
59.
go back to reference Antonelli A, Fallahi P, Ferrari SM, Corrado A, Sebastiani M, Giuggioli D, Miccoli M, Zignego AL, Sansonno D, Marchi S, Ferri C. Parallel increase of circulating CXCL11 and CXCL10 in mixed cryoglobulinemia, while the proinflammatory cytokine IL-6 is associated with high serum Th2 chemokine CCL2. Clin Rheumatol. 2013;32:1147–54.PubMedCrossRef Antonelli A, Fallahi P, Ferrari SM, Corrado A, Sebastiani M, Giuggioli D, Miccoli M, Zignego AL, Sansonno D, Marchi S, Ferri C. Parallel increase of circulating CXCL11 and CXCL10 in mixed cryoglobulinemia, while the proinflammatory cytokine IL-6 is associated with high serum Th2 chemokine CCL2. Clin Rheumatol. 2013;32:1147–54.PubMedCrossRef
60.
go back to reference Antonelli A, Ferrari SM, Corrado A, Ferrannini E, Fallahi P. Increase of interferon-gamma inducible CXCL9 and CXCL11 serum levels in patients with active Graves’ disease and modulation by methimazole therapy. Thyroid. 2013;23:1461–9.PubMedCrossRef Antonelli A, Ferrari SM, Corrado A, Ferrannini E, Fallahi P. Increase of interferon-gamma inducible CXCL9 and CXCL11 serum levels in patients with active Graves’ disease and modulation by methimazole therapy. Thyroid. 2013;23:1461–9.PubMedCrossRef
61.
go back to reference Antonelli A, Fallahi P, Ferrari SM, Sebastiani M, Manfredi A, Mazzi V, Fabiani S, Centanni M, Marchi S, Ferri C. Circulating CXCL11 and CXCL10 are increased in hepatitis C-associated cryoglobulinemia in the presence of autoimmune thyroiditis. Mod Rheumatol. 2012;22:659–67.PubMedCrossRef Antonelli A, Fallahi P, Ferrari SM, Sebastiani M, Manfredi A, Mazzi V, Fabiani S, Centanni M, Marchi S, Ferri C. Circulating CXCL11 and CXCL10 are increased in hepatitis C-associated cryoglobulinemia in the presence of autoimmune thyroiditis. Mod Rheumatol. 2012;22:659–67.PubMedCrossRef
62.
go back to reference Foley JF, Yu CR, Solow R, Yacobucci M, Peden KW, Farber JM. Roles for CXC chemokine ligands 10 and 11 in recruiting CD4+ T cells to HIV-1-infected monocyte-derived macrophages, dendritic cells, and lymph nodes. J Immunol. 2005;174:4892–900.PubMedCrossRef Foley JF, Yu CR, Solow R, Yacobucci M, Peden KW, Farber JM. Roles for CXC chemokine ligands 10 and 11 in recruiting CD4+ T cells to HIV-1-infected monocyte-derived macrophages, dendritic cells, and lymph nodes. J Immunol. 2005;174:4892–900.PubMedCrossRef
63.
go back to reference Durudas A, Milush JM, Chen HL, Engram JC, Silvestri G, Sodora DL. Elevated levels of innate immune modulators in lymph nodes and blood are associated with more-rapid disease progression in simian immunodeficiency virus-infected monkeys. J Virol. 2009;83:12229–40.PubMedPubMedCentralCrossRef Durudas A, Milush JM, Chen HL, Engram JC, Silvestri G, Sodora DL. Elevated levels of innate immune modulators in lymph nodes and blood are associated with more-rapid disease progression in simian immunodeficiency virus-infected monkeys. J Virol. 2009;83:12229–40.PubMedPubMedCentralCrossRef
64.
go back to reference Karin N, Wildbaum G. The role of chemokines in adjusting the balance between CD4+ effector T cell subsets and FOXp3-negative regulatory T cells. Int Immunopharmacol. 2015;28:829–35.PubMedCrossRef Karin N, Wildbaum G. The role of chemokines in adjusting the balance between CD4+ effector T cell subsets and FOXp3-negative regulatory T cells. Int Immunopharmacol. 2015;28:829–35.PubMedCrossRef
65.
go back to reference Pineda-Tenor D, Berenguer J, Jimenez-Sousa MA, Guzman-Fulgencio M, Aldamiz-Echevarria T, Carrero A, Garcia-Alvarez M, Diez C, Tejerina F, Briz V, Resino S. CXCL9, CXCL10 and CXCL11 polymorphisms are associated with sustained virologic response in HIV/HCV-coinfected patients. J Clin Virol. 2014;61:423–9.PubMedCrossRef Pineda-Tenor D, Berenguer J, Jimenez-Sousa MA, Guzman-Fulgencio M, Aldamiz-Echevarria T, Carrero A, Garcia-Alvarez M, Diez C, Tejerina F, Briz V, Resino S. CXCL9, CXCL10 and CXCL11 polymorphisms are associated with sustained virologic response in HIV/HCV-coinfected patients. J Clin Virol. 2014;61:423–9.PubMedCrossRef
66.
go back to reference Zhou F, Liu X, Zuo D, Xue M, Gao L, Yang Y, Wang J, Niu L, Cao Q, Li X, et al. HIV-1 Nef-induced lncRNA AK006025 regulates CXCL9/10/11 cluster gene expression in astrocytes through interaction with CBP/P300. J Neuroinflamm. 2018;15:303.CrossRef Zhou F, Liu X, Zuo D, Xue M, Gao L, Yang Y, Wang J, Niu L, Cao Q, Li X, et al. HIV-1 Nef-induced lncRNA AK006025 regulates CXCL9/10/11 cluster gene expression in astrocytes through interaction with CBP/P300. J Neuroinflamm. 2018;15:303.CrossRef
Metadata
Title
The combination of CXCL9, CXCL10 and CXCL11 levels during primary HIV infection predicts HIV disease progression
Authors
Xiaowan Yin
Zhuo Wang
Tong Wu
Meichen Ma
Zining Zhang
Zhenxing Chu
Qinghai Hu
Haibo Ding
Xiaoxu Han
Junjie Xu
Hong Shang
Yongjun Jiang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-02172-3

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