CXC chemokine IP-10: A key actor in liver disease?

Hepatology International

Volumn 7, Issue 3, 2013, Pages 798-804

  Chen, Lin Jiao ^a   Lv, Juan ^a   Wen, Xiao Yu ^a   Niu, Jun Qi ^a  

^a JILIN UNIVERSITY   (China)

Author keywords

Chemokine; CXCL10; HCV; HIV; IP 10; Liver disease; Liver transplantation

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10;

ACUTE GRAFT REJECTION; DISEASE COURSE; DISEASE SEVERITY; ENDOTHELIUM; GENETIC POLYMORPHISM; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFLAMMATION; IP 10 GENE; LIVER CELL; LIVER DISEASE; LIVER FIBROSIS; LIVER INJURY; LIVER PARENCHYMA; LIVER SINUSOID; LIVER TRANSPLANTATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; MIXED INFECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RECEPTOR BINDING; REVIEW; T LYMPHOCYTE;

EID: 84884355959     PISSN: 19360533     EISSN: 19360541     Source Type: Journal    
DOI: 10.1007/s12072-013-9445-0     Document Type: Review

References (78)

1. Laing KJ, Secombes CJ. Chemokines. Dev Comp Immunol 2004;28:443-460
2. Luster AD. Chemokines - chemotactic cytokines that mediate inflammation. N Engl J Med 1998;338:436-445
3. Dewald B, Moser B, Barella L, Schumacher C, Baggiolini M, Clark-Lewis I. IP-10, a gamma-interferon-inducible protein related to interleukin-8, lacks neutrophil activating properties. Immunol Lett 1992;32:81-84
4. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, Baggiolini M, Moser B. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 1996;184:963-969
5. Apolinario A, Majano PL, Lorente R, Nunez O, Clemente G, Garcia-Monzon C. Gene expression profile of T-cell-specific chemokines in human hepatocyte-derived cells: evidence for a synergistic inducer effect of cytokines and hepatitis C virus proteins. J Viral Hepat 2005;12:27-37
6. Strieter RM, Polverini PJ, Arenberg DA, Kunkel SL. The role of CXC chemokines as regulators of angiogenesis. Shock 1995;4:155-160
7. Luster AD, Unkeless JC, Ravetch JV. Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature 1985;315:672-676
8. Luster AD, Jhanwar SC, Chaganti RS, Kersey JH, Ravetch JV. Interferon-inducible gene maps to a chromosomal band associated with a (4;11) translocation in acute leukemia cells. Proc Natl Acad Sci USA 1987;84:2868-2871
9. Luster AD, Ravetch JV. Biochemical characterization of a gamma interferon-inducible cytokine (IP-10). J Exp Med 1987;166:1084-1097
10. Romagnani P, Annunziato F, Lazzeri E, Cosmi L, Beltrame C, Lasagni L, Galli G, Francalanci M, Manetti R, Marra F, Vanini V, Maggi E, Romagnani S. Interferon-inducible protein 10, monokine induced by interferon gamma, and interferon-inducible T-cell alpha chemoattractant are produced by thymic epithelial cells and attract T-cell receptor (TCR) alphabeta+ CD8+ single-positive T cells, TCRgammadelta+ T cells, and natural killer-type cells in human thymus. Blood 2001;97:601-607
11. Romagnani P, Lazzeri E, Lasagni L, Mavilia C, Beltrame C, Francalanci M, Rotondi M, Annunziato F, Maurenzig L, Cosmi L, Galli G, Salvadori M, Maggi E, Serio M. IP-10 and Mig production by glomerular cells in human proliferative glomerulonephritis and regulation by nitric oxide. J Am Soc Nephrol 2002;13:53-64
12. Harvey CE, Post JJ, Palladinetti P, Freeman AJ, Ffrench RA, Kumar RK, Marinos G, Lloyd AR. Expression of the chemokine IP-10 (CXCL10) by hepatocytes in chronic hepatitis C virus infection correlates with histological severity and lobular inflammation. J Leukoc Biol 2003;74:360-369
13. Zeremski M, Petrovic LM, Chiriboga L, Brown QB, Yee HT, Kinkhabwala M, Jacobson IM, Dimova R, Markatou M, Talal AH. Intrahepatic levels of CXCR3-associated chemokines correlate with liver inflammation and fibrosis in chronic hepatitis C. Hepatology 2008;48:1440-1450
14. Kimura K, Kakimi K, Wieland S, Guidotti LG, Chisari FV. Activated intrahepatic antigen-presenting cells inhibit hepatitis B virus replication in the liver of transgenic mice. J Immunol 2002;169:5188-5195
15. Nishioji K, Okanoue T, Itoh Y, Narumi S, Sakamoto M, Nakamura H, Morita A, Kashima K. Increase of chemokine interferon-inducible protein-10 (IP-10) in the serum of patients with autoimmune liver diseases and increase of its mRNA expression in hepatocytes. Clin Exp Immunol 2001;123:271-279
16. Mihm S, Schweyer S, Ramadori G. Expression of the chemokine IP-10 correlates with the accumulation of hepatic IFN-gamma and IL-18 mRNA in chronic hepatitis C but not in hepatitis B. J Med Virol 2003;70:562-570
17. Wang J, Zhao JH, Wang PP, Xiang GJ. Expression of CXC chemokine IP-10 in patients with chronic hepatitis B. Hepatobiliary Pancreat Dis Int 2008;7:45-50
18. Hintermann E, Bayer M, Pfeilschifter JM, Luster AD, Christen U. CXCL10 promotes liver fibrosis by prevention of NK cell mediated hepatic stellate cell inactivation. J Autoimmun 2010;35:424-435
19. Groom JR, Luster AD. CXCR3 in T cell function. Exp Cell Res 2011;317:620-631
20. Loetscher M, Loetscher P, Brass N, Meese E, Moser B. Lymphocyte-specific chemokine receptor CXCR3: regulation, chemokine binding and gene localization. Eur J Immunol 1998;28:3696-3705
21. Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, Koch AE, Moser B, Mackay CR. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 1998;101:746-754
22. Lo BK, Yu M, Zloty D, Cowan B, Shapiro J, McElwee KJ. CXCR3/ligands are significantly involved in the tumorigenesis of basal cell carcinomas. Am J Pathol 2010;176:2435-2446
23. Liu M, Guo S, Hibbert JM, Jain V, Singh N, Wilson NO, Stiles JK. CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 2011;22:121-130
24. Casrouge A, Decalf J, Ahloulay M, Lababidi C, Mansour H, Vallet-Pichard A, Mallet V, Mottez E, Mapes J, Fontanet A, Pol S, Albert ML. Evidence for an antagonist form of the chemokine CXCL10 in patients chronically infected with HCV. J Clin Invest 2011;121:308-317
25. Proost P, Schutyser E, Menten P, Struyf S, Wuyts A, Opdenakker G, Detheux M, Parmentier M, Durinx C, Lambeir AM, Neyts J, Liekens S, Maudgal PC, Billiau A, Van Damme J. Amino-terminal truncation of CXCR3 agonists impairs receptor signaling and lymphocyte chemotaxis, while preserving antiangiogenic properties. Blood 2001;98:3554-3561
26. Charles ED, Dustin LB. Chemokine antagonism in chronic hepatitis C virus infection. J Clin Invest 2011;121:25-27
27. Deng G, Zhou G, Zhang R, Zhai Y, Zhao W, Yan Z, Deng C, Yuan X, Xu B, Dong X, Zhang X, Yao Z, Shen Y, Qiang B, Wang Y, He F. Regulatory polymorphisms in the promoter of CXCL10 gene and disease progression in male hepatitis B virus carriers. Gastroenterology 2008;134:716-726
28. Lagging M, Romero AI, Westin J, Norkrans G, Dhillon AP, Pawlotsky JM, Zeuzem S, von Wagner M, Negro F, Schalm SW, Haagmans BL, Ferrari C, Missale G, Neumann AU, Verheij-Hart E, Hellstrand K. IP-10 predicts viral response and therapeutic outcome in difficult-to-treat patients with HCV genotype 1 infection. Hepatology 2006;44:1617-1625
29. Romero AI, Lagging M, Westin J, Dhillon AP, Dustin LB, Pawlotsky JM, Neumann AU, Ferrari C, Missale G, Haagmans BL, Schalm SW, Zeuzem S, Negro F, Verheij-Hart E, Hellstrand K. Interferon (IFN)-gamma-inducible protein-10: association with histological results, viral kinetics, and outcome during treatment with pegylated IFN-alpha 2a and ribavirin for chronic hepatitis C virus infection. J Infect Dis 2006;194:895-903
30. Kopydlowski KM, Salkowski CA, Cody MJ, van Rooijen N, Major J, Hamilton TA, Vogel SN. Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J Immunol 1999;163:1537-1544
31. Jaruga B, Hong F, Kim WH, Gao B. IFN-gamma/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1. Am J Physiol Gastrointest Liver Physiol 2004;287:G1044-G1052
32. Chuang YH, Lian ZX, Cheng CM, Lan RY, Yang GX, Moritoki Y, Chiang BL, Ansari AA, Tsuneyama K, Coppel RL, Gershwin ME. Increased levels of chemokine receptor CXCR3 and chemokines IP-10 and MIG in patients with primary biliary cirrhosis and their first degree relatives. J Autoimmun 2005;25:126-132
33. Zhou R, Tang W, Ren YX, He PL, Yang YF, Li YC, Zuo JP. Preventive effects of (5R)-5-hydroxytriptolide on concanavalin A-induced hepatitis. Eur J Pharmacol 2006;537:181-189
34. Bone-Larson CL, Hogaboam CM, Evanhoff H, Strieter RM, Kunkel SL. IFN-gamma-inducible protein-10 (CXCL10) is hepatoprotective during acute liver injury through the induction of CXCR2 on hepatocytes. J Immunol 2001;167:7077-7083
35. Njoku DB, Li Z, Mellerson JL, Sharma R, Talor MV, Barat N, Rose NR. IP-10 protects while MIP-2 promotes experimental anesthetic hapten-induced hepatitis. J Autoimmun 2009;32:52-59
36. Shields PL, Morland CM, Salmon M, Qin S, Hubscher SG, Adams DH. Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J Immunol 1999;163:6236-6243
37. Ji R, Lee CM, Gonzales LW, Yang Y, Aksoy MO, Wang P, Brailoiu E, Dun N, Hurford MT, Kelsen SG. Human type II pneumocyte chemotactic responses to CXCR3 activation are mediated by splice variant A. Am J Physiol Lung Cell Mol Physiol 2008;294:L1187-L1196
38. Shen Q, Zhang R, Bhat NR. MAP kinase regulation of IP10/CXCL10 chemokine gene expression in microglial cells. Brain Res 2006;1086:9-16
39. Datta D, Flaxenburg JA, Laxmanan S, Geehan C, Grimm M, Waaga-Gasser AM, Briscoe DM, Pal S. Ras-induced modulation of CXCL10 and its receptor splice variant CXCR3-B in MDA-MB-435 and MCF-7 cells: relevance for the development of human breast cancer. Cancer Res 2006;66:9509-9518
40. Shahabuddin S, Ji R, Wang P, Brailoiu E, Dun N, Yang Y, Aksoy MO, Kelsen SG. CXCR3 chemokine receptor-induced chemotaxis in human airway epithelial cells: role of p38 MAPK and PI3K signaling pathways. Am J Physiol Cell Physiol 2006;291:C34-C39
41. Jinquan T, Jing C, Jacobi HH, Reimert CM, Millner A, Quan S, Hansen JB, Dissing S, Malling HJ, Skov PS, Poulsen LK. CXCR3 expression and activation of eosinophils: role of IFN-gamma-inducible protein-10 and monokine induced by IFN-gamma. J Immunol 2000;165:1548-1556
42. Wu Q, Zhai Y, Jiao SN, Wang J. The research progression of CXCL-10 in liver ischemia reperfusion injury. Lab Anim Sci 2008;25:37-40
43. Wakabayashi H, Ito T, Fushimi S, Nakashima Y, Itakura J, Qiuying L, Win MM, Cuiming S, Chen C, Sato M, Mino M, Ogino T, Makino H, Yoshimura A, Matsukawa A. Spred-2 deficiency exacerbates acetaminophen-induced hepatotoxicity in mice. Clin Immunol 2012;144:272-282
44. Wu J, Li J, Salcedo R, Mivechi NF, Trinchieri G, Horuzsko A. The proinflammatory myeloid cell receptor TREM-1 controls Kupffer cell activation and development of hepatocellular carcinoma. Cancer Res 2012;72:3977-3986
45. Chen SH, Wu HL, Kao JH, Hwang LH. Persistent hepatitis B viral replication in a FVB/N mouse model: impact of host and viral factors. PLoS ONE 2012;7:e36984
46. Sheridan DA, Bridge SH, Felmlee DJ, Crossey MM, Thomas HC, Taylor-Robinson SD, Toms GL, Neely RD, Bassendine MF. Apolipoprotein-E and hepatitis C lipoviral particles in genotype 1 infection: evidence for an association with interferon sensitivity. J Hepatol 2012;57:32-38
47. Feld JJ, Lutchman GA, Heller T, Hara K, Pfeiffer JK, Leff RD, Meek C, Rivera M, Ko M, Koh C, Rotman Y, Ghany MG, Haynes-Williams V, Neumann AU, Liang TJ, Hoofnagle JH. Ribavirin improves early responses to peginterferon through improved interferon signaling. Gastroenterology 2010;139:154-162 e154
48. Man K, Ng KT, Xu A, Cheng Q, Lo CM, Xiao JW, Sun BS, Lim ZX, Cheung JS, Wu EX, Sun CK, Poon RT, Fan ST. Suppression of liver tumor growth and metastasis by adiponectin in nude mice through inhibition of tumor angiogenesis and downregulation of Rho kinase/IFN-inducible protein 10/matrix metalloproteinase 9 signaling. Clin Cancer Res 2010;16:967-977
49. Qu J, Zhang Q, Li Y, Liu W, Chen L, Zhu Y, Wu J. The Tat protein of human immunodeficiency virus-1 enhances hepatitis C virus replication through interferon gamma-inducible protein-10. BMC Immunol 2012;13:15
50. Bedossa P, Valla D, Vidaud M, Marcellin P. Liver gene expression signature of mild fibrosis in patients with chronic hepatitis C. Gastroenterology 2005;129:2064-2075
51. Narumi S, Tominaga Y, Tamaru M, Shimai S, Okumura H, Nishioji K, Itoh Y, Okanoue T. Expression of IFN-inducible protein-10 in chronic hepatitis. J Immunol 1997;158:5536-5544
52. Reiberger T, Aberle JH, Kundi M, Kohrgruber N, Rieger A, Gangl A, Holzmann H, Peck-Radosavljevic M. IP-10 correlates with hepatitis C viral load, hepatic inflammation and fibrosis and predicts hepatitis C virus relapse or non-response in HIV-HCV coinfection. Antivir Ther 2008;13:969-976
53. Roe B, Coughlan S, Hassan J, Grogan A, Farrell G, Norris S, Bergin C, Hall WW. Elevated serum levels of interferon-gamma-inducible protein-10 in patients coinfected with hepatitis C virus and HIV. J Infect Dis 2007;196:1053-1057
54. Rider PJ, Liu F. Crosstalk between HIV and hepatitis C virus during co-infection. BMC Med 2012;10:32
55. Berenguer J, Fernandez-Rodriguez A, Jimenez-Sousa MA, Cosin J, Zarate P, Micheloud D, Lopez JC, Miralles P, Catalan P, Resino S. High plasma CXCL10 levels are associated with HCV-genotype 1, and higher insulin resistance, fibrosis, and HIV viral load in HIV/HCV coinfected patients. Cytokine 2012;57:25-29
56. Fattovich G, Covolo L, Bibert S, Askarieh G, Lagging M, Clement S, Malerba G, Pasino M, Guido M, Puoti M, Gaeta GB, Santantonio T, Raimondo G, Bruno R, Bochud PY, Donato F, Negro F. IL28B polymorphisms, IP-10 and viral load predict virological response to therapy in chronic hepatitis C. Aliment Pharmacol Ther 2011;33:1162-1172
57. Tacke F, Zimmermann HW, Berres ML, Trautwein C, Wasmuth HE. Serum chemokine receptor CXCR3 ligands are associated with progression, organ dysfunction and complications of chronic liver diseases. Liver Int 2011;31:840-849
58. Zeremski M, Dimova R, Brown Q, Jacobson IM, Markatou M, Talal AH. Peripheral CXCR3-associated chemokines as biomarkers of fibrosis in chronic hepatitis C virus infection. J Infect Dis 2009;200:1774-1780
59. Zeremski M, Dimova R, Astemborski J, Thomas DL, Talal AH. CXCL9 and CXCL10 chemokines as predictors of liver fibrosis in a cohort of primarily African-American injection drug users with chronic hepatitis C. J Infect Dis 2011;204:832-836
60. Butera D, Marukian S, Iwamaye AE, Hembrador E, Chambers TJ, Di Bisceglie AM, Charles ED, Talal AH, Jacobson IM, Rice CM, Dustin LB. Plasma chemokine levels correlate with the outcome of antiviral therapy in patients with hepatitis C. Blood 2005;106:1175-1182
61. Diago M, Castellano G, Garcia-Samaniego J, Perez C, Fernandez I, Romero M, Iacono OL, Garcia-Monzon C. Association of pretreatment serum interferon gamma inducible protein 10 levels with sustained virological response to peginterferon plus ribavirin therapy in genotype 1 infected patients with chronic hepatitis C. Gut 2006;55:374-379
62. Lagging M, Askarieh G, Negro F, Bibert S, Soderholm J, Westin J, Lindh M, Romero A, Missale G, Ferrari C, Neumann AU, Pawlotsky JM, Haagmans BL, Zeuzem S, Bochud PY, Hellstrand K. Response prediction in chronic hepatitis C by assessment of IP-10 and IL28B-related single nucleotide polymorphisms. PLoS ONE 2011;6:e17232
63. Beinhardt S, Aberle JH, Strasser M, Dulic-Lakovic E, Maieron A, Kreil A, Rutter K, Staettermayer AF, Datz C, Scherzer TM, Strassl R, Bischof M, Stauber R, Bodlaj G, Laferl H, Holzmann H, Steindl-Munda P, Ferenci P, Hofer H. Serum level of IP-10 increases predictive value of IL28B polymorphisms for spontaneous clearance of acute HCV infection. Gastroenterology 2012;142:78-85 e72
64. Zeremski M, Markatou M, Brown QB, Dorante G, Cunningham-Rundles S, Talal AH. Interferon gamma-inducible protein 10: a predictive marker of successful treatment response in hepatitis C virus/HIV-coinfected patients. J Acquir Immune Defic Syndr 2007;45:262-268
65. Rotondi M, Minelli R, Magri F, Leporati P, Romagnani P, Baroni MC, Delsignore R, Serio M, Chiovato L. Serum CXCL10 levels and occurrence of thyroid dysfunction in patients treated with interferon-alpha therapy for hepatitis C virus-related hepatitis. Eur J Endocrinol 2007;156:409-414
66. Antonelli A, Ferri C, Fallahi P, Ferrari SM, Frascerra S, Carpi A, Nicolini A, Ferrannini E. Alpha-chemokine CXCL10 and beta-chemokine CCL2 serum levels in patients with hepatitis C-associated cryoglobulinemia in the presence or absence of autoimmune thyroiditis. Metabolism 2008;57:1270-1277
67. Antonelli A, Ferri C, Ferrari SM, Colaci M, Sansonno D, Fallahi P. Endocrine manifestations of hepatitis C virus infection. Nat Clin Pract Endocrinol Metab 2009;5:26-34
68. Toiyama Y, Fujikawa H, Kawamura M, Matsushita K, Saigusa S, Tanaka K, Inoue Y, Uchida K, Mohri Y, Kusunoki M. Evaluation of CXCL10 as a novel serum marker for predicting liver metastasis and prognosis in colorectal cancer. Int J Oncol 2012;40:560-566
69. Horiguchi K, Kitagawa-Sakakida S, Sawa Y, Li ZZ, Fukushima N, Shirakura R, Matsuda H. Selective chemokine and receptor gene expressions in allografts that develop transplant vasculopathy. J Heart Lung Transplant 2002;21:1090-1100
70. Matz M, Beyer J, Wunsch D, Mashreghi MF, Seiler M, Pratschke J, Babel N, Volk HD, Reinke P, Kotsch K. Early post-transplant urinary IP-10 expression after kidney transplantation is predictive of short- and long-term graft function. Kidney Int 2006;69:1683-1690
71. Xiao L, Wang QX, Ding G. Relationship of chemokine IP-10 and its solude CXCR3 in bile with acute graft rejection after liver transplantation. Acad J Sec Med Univ 2009;30:655-658
72. Chen G, Liu Y. Expression of IP-10 and MIP-3a in rat allografted liver. China J Mod Med 2005;15:2594-2596
73. Berres ML, Trautwein C, Schmeding M, Eurich D, Tacke F, Bahra M, Neuhaus P, Neumann UP, Wasmuth HE. Serum chemokine CXC ligand 10 (CXCL10) predicts fibrosis progression after liver transplantation for hepatitis C infection. Hepatology 2011;53:596-603
74. Liu LM, Xu ZH, Liu Y, Zhong YW, Mao YL, Wang HB, Wang HF, Xu DP. Relationship between single nucleotide polymorphism of chemokine CXCL10 G-210A and the chronicity and severity of HBV infection. Med J Chin PLA 2011;36:39-41
75. Mezger M, Steffens M, Beyer M, Manger C, Eberle J, Toliat MR, Wienker TF, Ljungman P, Hebart H, Dornbusch HJ, Einsele H, Loeffler J. Polymorphisms in the chemokine (C-X-C motif) ligand 10 are associated with invasive aspergillosis after allogeneic stem-cell transplantation and influence CXCL10 expression in monocyte-derived dendritic cells. Blood 2008;111:534-536
76. Moreira MA, Souza AL, Lana-Peixoto MA. Chemokines in cerebro-spinal fluid of patients with active and stable relapsing-remitting multiple sclerosis. Braz J Med Biol Res 2006;39:441-445
77. Hasegawa H, Inoue A, Kohno M, Muraoka M, Miyazaki T, Terada M, Nakayama T, Yoshie O, Nose M, Yasukawa M. Antagonist of interferon-inducible protein 10/CXCL10 ameliorates the progression of autoimmune sialadenitis in MRL/lpr mice. Arthritis Rheum 2006;54:1174-1183
78. Yang XL, Chu YW, Deng FG, Xiong SD. IP10 enhances anti-tumor immunity and its mechanisms. Chin J Immunol 2006;22:99-108