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-Inducible Protein 10 (IP-10; CXCL10)-Deficient Mice Reveal a Role for IP-10 in Effector T Cell Generation and Trafficking1
*
Center for Immunology and Inflammatory Diseases, Division of Rheumatology, Allergy and Immunology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114; and
Department of Molecular Biology and Biochemistry, University of California, Irvine, CA 92697
IFN-
-inducible protein 10 (IP-10, CXCL10), a chemokine secreted
from cells stimulated with type I and II IFNs and LPS, is a
chemoattractant for activated T cells. Expression of IP-10 is seen in
many Th1-type inflammatory diseases, where it is thought to play an
important role in recruiting activated T cells into sites of tissue
inflammation. To determine the in vivo function of IP-10, we
constructed an IP-10-deficient mouse (IP-10-/-) by
targeted gene disruption. Immunological analysis revealed that
IP-10-/- mice had impaired T cell responses. T cell
proliferation to allogeneic and antigenic stimulation and IFN-
secretion in response to antigenic challenge were impaired in
IP-10-/- mice. In addition, IP-10-/- mice
exhibited an impaired contact hypersensitivity response, characterized
by decreased ear swelling and reduced inflammatory cell infiltrates. T
cells recovered from draining lymph nodes also had a decreased
proliferative response to Ag restimulation. Furthermore,
IP-10-/- mice infected with a neurotropic mouse hepatitis
virus had an impaired ability to control viral replication in the
brain. This was associated with decreased recruitment of
CD4+ and CD8+ lymphocytes into the brain,
reduced levels of IFN- and the IFN--induced chemokines monokine
induced by IFN- (Mig, CXCL9) and IFN-inducible T cell 
chemoattractant (I-TAC, CXCL11) in the brain, decreased numbers of
virus-specific IFN--secreting CD8+ cells in the spleen,
and reduced levels of demyelination in the CNS. Taken together, our
data suggest a role for IP-10 in both effector T cell generation and
trafficking in vivo.
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U. M. Nagarajan, D. M. Ojcius, L. Stahl, R. G. Rank, and T. Darville Chlamydia trachomatis Induces Expression of IFN-{gamma}-Inducible Protein 10 and IFN-{beta} Independent of TLR2 and TLR4, but Largely Dependent on MyD88 J. Immunol., July 1, 2005; 175(1): 450 - 460. [Abstract] [Full Text] [PDF]
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 C. E. Heise, A. Pahuja, S. C. Hudson, M. S. Mistry, A. L. Putnam, M. M. Gross, P. A. Gottlieb, W. S. Wade, M. Kiankarimi, D. Schwarz, et al. Pharmacological Characterization of CXC Chemokine Receptor 3 Ligands and a Small Molecule Antagonist J. Pharmacol. Exp. Ther., June 1, 2005; 313(3): 1263 - 1271. [Abstract] [Full Text] [PDF]
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G. Li, L. Tian, J.-m. Hou, Z.-y. Ding, Q.-m. He, P. Feng, Y.-j. Wen, F. Xiao, B. Yao, R. Zhang, et al. Improved Therapeutic Effectiveness by Combining Recombinant CXC Chemokine Ligand 10 with Cisplatin in Solid Tumors Clin. Cancer Res., June 1, 2005; 11(11): 4217 - 4224. [Abstract] [Full Text] [PDF]
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T. Feferman, P. K. Maiti, S. Berrih-Aknin, J. Bismuth, J. Bidault, S. Fuchs, and M. C. Souroujon Overexpression of IFN-Induced Protein 10 and Its Receptor CXCR3 in Myasthenia Gravis J. Immunol., May 1, 2005; 174(9): 5324 - 5331. [Abstract] [Full Text] [PDF]
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J. F. Foley, C.-R. Yu, R. Solow, M. Yacobucci, K. W. C. Peden, and J. M. Farber 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., April 15, 2005; 174(8): 4892 - 4900. [Abstract] [Full Text] [PDF]
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Y. Jiang, J. Xu, C. Zhou, Z. Wu, S. Zhong, J. Liu, W. Luo, T. Chen, Q. Qin, and P. Deng Characterization of Cytokine/Chemokine Profiles of Severe Acute Respiratory Syndrome Am. J. Respir. Crit. Care Med., April 15, 2005; 171(8): 850 - 857. [Abstract] [Full Text] [PDF]
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S. J. Molesworth-Kenyon, J. E. Oakes, and R. N. Lausch A novel role for neutrophils as a source of T cell-recruiting chemokines IP-10 and Mig during the DTH response to HSV-1 antigen J. Leukoc. Biol., April 1, 2005; 77(4): 552 - 559. [Abstract] [Full Text] [PDF]
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A. Saudemont, N. Jouy, D. Hetuin, and B. Quesnel NK cells that are activated by CXCL10 can kill dormant tumor cells that resist CTL-mediated lysis and can express B7-H1 that stimulates T cells Blood, March 15, 2005; 105(6): 2428 - 2435. [Abstract] [Full Text] [PDF]
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M. Ejrnaes, N. Videbaek, U. Christen, A. Cooke, B. K. Michelsen, and M. von Herrath Different Diabetogenic Potential of Autoaggressive CD8+ Clones Associated with IFN-{gamma}-Inducible Protein 10 (CXC Chemokine Ligand 10) Production but Not Cytokine Expression, Cytolytic Activity, or Homing Characteristics J. Immunol., March 1, 2005; 174(5): 2746 - 2755. [Abstract] [Full Text] [PDF]
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D. Zipris, E. Lien, J. X. Xie, D. L. Greiner, J. P. Mordes, and A. A. Rossini TLR Activation Synergizes with Kilham Rat Virus Infection to Induce Diabetes in BBDR Rats J. Immunol., January 1, 2005; 174(1): 131 - 142. [Abstract] [Full Text] [PDF]
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 A. M. Tager, R. L. Kradin, P. LaCamera, S. D. Bercury, G. S. V. Campanella, C. P. Leary, V. Polosukhin, L.-H. Zhao, H. Sakamoto, T. S. Blackwell, et al. Inhibition of Pulmonary Fibrosis by the Chemokine IP-10/CXCL10 Am. J. Respir. Cell Mol. Biol., October 1, 2004; 31(4): 395 - 404. [Abstract] [Full Text] [PDF]
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R. A. Colvin, G. S. V. Campanella, J. Sun, and A. D. Luster Intracellular Domains of CXCR3 That Mediate CXCL9, CXCL10, and CXCL11 Function J. Biol. Chem., July 16, 2004; 279(29): 30219 - 30227. [Abstract] [Full Text] [PDF]
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M. S. Thomas, S. L. Kunkel, and N. W. Lukacs Regulation of Cockroach Antigen-Induced Allergic Airway Hyperreactivity by the CXCR3 Ligand CXCL9 J. Immunol., July 1, 2004; 173(1): 615 - 623. [Abstract] [Full Text] [PDF]
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D. Whiting, G. Hsieh, J. J. Yun, A. Banerji, W. Yao, M. C. Fishbein, J. Belperio, R. M. Strieter, B. Bonavida, and A. Ardehali Chemokine Monokine Induced by IFN-{gamma}/CXC Chemokine Ligand 9 Stimulates T Lymphocyte Proliferation and Effector Cytokine Production J. Immunol., June 15, 2004; 172(12): 7417 - 7424. [Abstract] [Full Text] [PDF]
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J. E. Christensen, A. Nansen, T. Moos, B. Lu, C. Gerard, J. P. Christensen, and A. R. Thomsen Efficient T-Cell Surveillance of the CNS Requires Expression of the CXC Chemokine Receptor 3 J. Neurosci., May 19, 2004; 24(20): 4849 - 4858. [Abstract] [Full Text] [PDF]
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B. Raju, Y. Hoshino, K. Kuwabara, I. Belitskaya, S. Prabhakar, A. Canova, J. A. Gold, R. Condos, R. I. Pine, S. Brown, et al. Aerosolized Gamma Interferon (IFN-{gamma}) Induces Expression of the Genes Encoding the IFN-{gamma}-Inducible 10-Kilodalton Protein but Not Inducible Nitric Oxide Synthase in the Lung during Tuberculosis Infect. Immun., March 1, 2004; 72(3): 1275 - 1283. [Abstract] [Full Text] [PDF]
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C. L. Afonso, M. E. Piccone, K. M. Zaffuto, J. Neilan, G. F. Kutish, Z. Lu, C. A. Balinsky, T. R. Gibb, T. J. Bean, L. Zsak, et al. African Swine Fever Virus Multigene Family 360 and 530 Genes Affect Host Interferon Response J. Virol., February 15, 2004; 78(4): 1858 - 1864. [Abstract] [Full Text] [PDF]
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 I. Tsunoda, T. E Lane, J. Blackett, and R. S Fujinami Distinct roles for IP-10/C XC L10 in three animal models, Theiler's virus infection, EA E, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10 Multiple Sclerosis, February 1, 2004; 10(1): 26 - 34. [Abstract] [PDF]
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M. J. Trifilo, C. Montalto-Morrison, L. N. Stiles, K. R. Hurst, J. L. Hardison, J. E. Manning, P. S. Masters, and T. E. Lane CXC Chemokine Ligand 10 Controls Viral Infection in the Central Nervous System: Evidence for a Role in Innate Immune Response through Recruitment and Activation of Natural Killer Cells J. Virol., January 15, 2004; 78(2): 585 - 594. [Abstract] [Full Text] [PDF]
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K. Abel, L. La Franco-Scheuch, T. Rourke, Z.-M. Ma, V. de Silva, B. Fallert, L. Beckett, T. A. Reinhart, and C. J. Miller Gamma Interferon-Mediated Inflammation Is Associated with Lack of Protection from Intravaginal Simian Immunodeficiency Virus SIVmac239 Challenge in Simian-Human Immunodeficiency Virus 89.6-Immunized Rhesus Macaques J. Virol., January 15, 2004; 78(2): 841 - 854. [Abstract] [Full Text] [PDF]
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R. S. Klein, L. Izikson, T. Means, H. D. Gibson, E. Lin, R. A. Sobel, H. L. Weiner, and A. D. Luster IFN-Inducible Protein 10/CXC Chemokine Ligand 10-Independent Induction of Experimental Autoimmune Encephalomyelitis J. Immunol., January 1, 2004; 172(1): 550 - 559. [Abstract] [Full Text] [PDF]
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U. Christen, D. B. McGavern, A. D. Luster, M. G. von Herrath, and M. B. A. Oldstone Among CXCR3 Chemokines, IFN-{gamma}-Inducible Protein of 10 kDa (CXC Chemokine Ligand (CXCL) 10) but Not Monokine Induced by IFN-{gamma} (CXCL9) Imprints a Pattern for the Subsequent Development of Autoimmune Disease J. Immunol., December 15, 2003; 171(12): 6838 - 6845. [Abstract] [Full Text] [PDF]
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G. D. Han, H. Koike, T. Nakatsue, K. Suzuki, H. Yoneyama, S. Narumi, N. Kobayashi, P. Mundel, F. Shimizu, and H. Kawachi IFN-Inducible Protein-10 Has a Differential Role in Podocyte during Thy 1.1 Glomerulonephritis J. Am. Soc. Nephrol., December 1, 2003; 14(12): 3111 - 3126. [Abstract] [Full Text] [PDF]
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C. M. U. Hilkens, J. F. Schlaak, and I. M. Kerr Differential Responses to IFN-{alpha} Subtypes in Human T Cells and Dendritic Cells J. Immunol., November 15, 2003; 171(10): 5255 - 5263. [Abstract] [Full Text] [PDF]
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G. Valbuena, W. Bradford, and D. H. Walker Expression Analysis of the T-Cell-Targeting Chemokines CXCL9 and CXCL10 in Mice and Humans with Endothelial Infections Caused by Rickettsiae of the Spotted Fever Group Am. J. Pathol., October 1, 2003; 163(4): 1357 - 1369. [Abstract] [Full Text] [PDF]
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D. J. J. Carr, J. Chodosh, J. Ash, and T. E. Lane Effect of Anti-CXCL10 Monoclonal Antibody on Herpes Simplex Virus Type 1 Keratitis and Retinal Infection J. Virol., September 15, 2003; 77(18): 10037 - 10046. [Abstract] [Full Text] [PDF]
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R. L. Rabin, M. A. Alston, J. C. Sircus, B. Knollmann-Ritschel, C. Moratz, D. Ngo, and J. M. Farber CXCR3 Is Induced Early on the Pathway of CD4+ T Cell Differentiation and Bridges Central and Peripheral Functions J. Immunol., September 15, 2003; 171(6): 2812 - 2824. [Abstract] [Full Text] [PDF]
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B. Johnston, C. H. Kim, D. Soler, M. Emoto, and E. C. Butcher Differential Chemokine Responses and Homing Patterns of Murine TCR{alpha}{beta} NKT Cell Subsets J. Immunol., September 15, 2003; 171(6): 2960 - 2969. [Abstract] [Full Text] [PDF]
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 S Futagami, T Hiratsuka, A Tatsuguchi, K Suzuki, M Kusunoki, Y Shinji, K Shinoki, T Iizumi, T Akamatsu, H Nishigaki, et al. Monocyte chemoattractant protein 1 (MCP-1) released from Helicobacter pylori stimulated gastric epithelial cells induces cyclooxygenase 2 expression and activation in T cells Gut, September 1, 2003; 52(9): 1257 - 1264. [Abstract] [Full Text]
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J. Melchjorsen, L. N. Sorensen, and S. R. Paludan Expression and function of chemokines during viral infections: from molecular mechanisms to in vivo function J. Leukoc. Biol., September 1, 2003; 74(3): 331 - 343. [Abstract] [Full Text] [PDF]
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E. M. Genden, A. Iskander, J. S. Bromberg, and L. Mayer The Kinetics and Pattern of Tracheal Allograft Re-Epithelialization Am. J. Respir. Cell Mol. Biol., June 1, 2003; 28(6): 673 - 681. [Abstract] [Full Text] [PDF]
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G. S. V. Campanella, E. M. J. Lee, J. Sun, and A. D. Luster CXCR3 and Heparin Binding Sites of the Chemokine IP-10 (CXCL10) J. Biol. Chem., May 2, 2003; 278(19): 17066 - 17074. [Abstract] [Full Text] [PDF]
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M. C.-J. Cheeran, S. Hu, W. S. Sheng, P. K. Peterson, and J. R. Lokensgard CXCL10 Production from Cytomegalovirus-Stimulated Microglia Is Regulated by both Human and Viral Interleukin-10 J. Virol., April 15, 2003; 77(8): 4502 - 4515. [Abstract] [Full Text] [PDF]
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 S. Nakae, Y. Komiyama, S. Narumi, K. Sudo, R. Horai, Y.-i. Tagawa, K. Sekikawa, K. Matsushima, M. Asano, and Y. Iwakura IL-1-induced tumor necrosis factor-{alpha} elicits inflammatory cell infiltration in the skin by inducing IFN-{gamma}-inducible protein 10 in the elicitation phase of the contact hypersensitivity response Int. Immunol., February 1, 2003; 15(2): 251 - 260. [Abstract] [Full Text] [PDF]
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C. M. Denkinger, M. Denkinger, J. J. Kort, C. Metz, and T. G. Forsthuber In Vivo Blockade of Macrophage Migration Inhibitory Factor Ameliorates Acute Experimental Autoimmune Encephalomyelitis by Impairing the Homing of Encephalitogenic T Cells to the Central Nervous System J. Immunol., February 1, 2003; 170(3): 1274 - 1282. [Abstract] [Full Text] [PDF]
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