Reynders, Nathan; Luxembourg Institute of Health > Department of Infection and Immunity > Immuno-Pharmacology
Abboud, Dayana ; Université de Liège - ULiège > Molecular Biology of Diseases-Molecular Pharmacology
Baragli, Alexandra
Noman, Muhammad Zaeem
Rogister, Bernard ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Niclou, Simone
Heveker, Nikolaus
Janji, Bassam
Hanson, Julien ; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique
Szpakowska, Martyna
Chevigné, Andy
Language :
English
Title :
The Distinct Roles of CXCR3 Variants and Their Ligands in the Tumor Microenvironment
Publication date :
18 June 2019
Journal title :
Cells
eISSN :
2073-4409
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Basel, Switzerland
Zlotnik, A.; Yoshie, O. The chemokine superfamily revisited. Immunity 2012, 36, 705-716.
Thelen, M. Dancing to the tune of chemokines. Nat. Immunol. 2001, 2, 129-134.
Kleist, A.B.; Getschman, A.E.; Ziarek, J.J.; Nevins, A.M.; Gauthier, P.-A.; Chevigné, A.; Szpakowska, M.; Volkman, B.F. New paradigms in chemokine receptor signal transduction: Moving beyond the two-site model. Biochem. Pharmacol. 2016, 114, 53-68.
Szpakowska, M.; Dupuis, N.; Baragli, A.; Counson, M.; Hanson, J.; Piette, J.; Chevigné, A. Human herpesvirus 8-encoded chemokine vCCL2/vMIP-II is an agonist of the atypical chemokine receptor ACKR3/CXCR7. Biochem. Pharmacol. 2016, 114, 14-21.
Metzemaekers, M.; Vanheule, V.; Janssens, R.; Struyf, S.; Proost, P. Overview of the mechanisms that may contribute to the non-redundant activities of interferon-inducible CXC chemokine receptor 3 ligands. Front. Immunol. 2018, 8, 1970.
Moser, B.; Loetscher, P. Lymphocyte traffic control by chemokines. Nat. Immunol. 2001, 2, 123-128.
Griffith, J.W.; Sokol, C.L.; Luster, A.D. Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu. Rev. Immunol. 2014, 32, 659-702.
Thelen, M.; Stein, J.V. How chemokines invite leukocytes to dance. Nat. Immunol. 2008, 9, 953-959.
Luster, A.D. Chemokines—Chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 1998, 338, 436-445.
Balkwill, F. Cancer and the chemokine network. Nat. Rev. Cancer 2004, 4, 540-550.
Nagarsheth, N.; Wicha, M.S.; Zou, W. Chemokines in the cancer microenvironment and their relevance in cancer immunotherapy. Nat. Rev. Immunol. 2017, 17, 559-572.
Relation, T.; Dominici, M.; Horwitz, E.M. Concise review: An (Im) Penetrable shield: How the tumor microenvironment protects cancer stem cells. Stem Cells 2017, 35, 1123-1130.
Binnewies, M.; Roberts, E.W.; Kersten, K.; Chan, V.; Fearon, D.F.; Merad, M.; Coussens, L.M.; Gabrilovich, D.I.; Ostrand-Rosenberg, S.; Hedrick, C.C. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med. 2018, 24, 541-550.
Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 2005, 5, 263-274.
Franciszkiewicz, K.; Boissonnas, A.; Boutet, M.; Combadière, C.; Mami-Chouaib, F. Role of chemokines and chemokine receptors in shaping the effector phase of the antitumor immune response. Cancer Res. 2012, 72, 6325-6332.
Witsch, E.; Sela, M.; Yarden, Y. Roles for growth factors in cancer progression. Physiology 2010, 25, 85-101.
Wang, M.; Zhao, J.; Zhang, L.; Wei, F.; Lian, Y.; Wu, Y.; Gong, Z.; Zhang, S.; Zhou, J.; Cao, K. Role of tumor microenvironment in tumorigenesis. J. Cancer 2017, 8, 761-773.
Balkwill, F.R.; Capasso, M.; Hagemann, T. The tumor microenvironment at a glance. J. Cell Sci. 2012, 125, 5591-5596.
Groom, J.R.; Luster, A.D. CXCR3 ligands: Redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 2011, 89, 207-215.
Tokunaga, R.; Zhang, W.; Naseem, M.; Puccini, A.; Berger, M.D.; Soni, S.; McSkane, M.; Baba, H.; Lenz, H.-J. CXCL9, CXCL10, CXCL11/CXCR3 axis for immune activation—A target for novel cancer therapy. Cancer Treat. Rev. 2018, 63, 40-47.
Van Raemdonck, K.; Van den Steen, P.E.; Liekens, S.; Van Damme, J.; Struyf, S. CXCR3 ligands in disease and therapy. Cytokine Growth Factor Rev. 2015, 26, 311-327.
Lasagni, L.; Francalanci, M.; Annunziato, F.; Lazzeri, E.; Giannini, S.; Cosmi, L.; Sagrinati, C.; Mazzinghi, B.; Orlando, C.; Maggi, E. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J. Exp. Med. 2003, 197, 1537-1549.
Loetscher, M.; Gerber, B.; Loetscher, P.; Jones, S.A.; 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.
Cole, K.E.; Strick, C.A.; Paradis, T.J.; Ogborne, K.T.; Loetscher, M.; Gladue, R.P.; Lin, W.; Boyd, J.G.; Moser, B.; Wood, D.E. 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, 2009-2021.
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.
Thompson, B.D.; Jin, Y.; Wu, K.H.; Colvin, R.A.; Luster, A.D.; Birnbaumer, L.; Wu, M.X. Inhibition of Gai2 activation by Gai3 in CXCR3-mediated signaling. J. Biol. Chem. 2007, 282, 9547-9555.
Smit, M.J.; Verdijk, P.; van der Raaij-Helmer, E.M.; Navis, M.; Hensbergen, P.J.; Leurs, R.; Tensen, C.P. 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, 1959-1965.
Mueller, A.; Meiser, A.; McDonagh, E.M.; Fox, J.M.; Petit, S.J.; Xanthou, G.; Williams, T.J.; Pease, J.E. CXCL4-induced migration of activated T lymphocytes is mediated by the chemokine receptor CXCR3. J. Leukoc. Biol. 2008, 83, 875-882.
Korniejewska, A.; McKnight, A.J.; Johnson, Z.; Watson, M.L.; Ward, S.G. Expression and agonist responsiveness of CXCR3 variants in human T lymphocytes. Immunology 2011, 132, 503-515.
Watts, A.O.; Scholten, D.J.; Heitman, L.H.; Vischer, H.F.; Leurs, R. Label-free impedance responses of endogenous and synthetic chemokine receptor CXCR3 agonists correlate with G i-protein pathway activation. Biochem. Biophys. Res. Commun. 2012, 419, 412-418.
Romagnani, P.; Beltrame, C.; Annunziato, F.; Lasagni, L.; Luconi, M.; Galli, G.; Cosmi, L.; Maggi, E.; Salvadori, M.; Pupilli, C. Role for interactions between IP-10/Mig and CXCR3 in proliferative glomerulonephritis. J. Am. Soc. Nephrol. 1999, 10, 2518-2526.
Bonacchi, A.; Romagnani, P.; Romanelli, R.G.; Efsen, E.; Annunziato, F.; Lasagni, L.; Francalanci, M.; Serio, M.; Laffi, G.; Pinzani, M. Signal transduction by the chemokine receptor CXCR3: Activation of Ras/ERK, Src, and phosphatidylinositol 3-kinase/Akt controls cell migration and proliferation in human vascular pericytes. J. Biol. Chem. 2001, 276, 9945-9954.
Billottet, C.; Quemener, C.; Bikfalvi, A. CXCR3, a double-edged sword in tumor progression and angiogenesis. Biochim. Et Biophys. Acta (BBA) Rev. Cancer 2013, 1836, 287-295.
Mgrditchian, T.; Arakelian, T.; Paggetti, J.; Noman, M.Z.; Viry, E.; Moussay, E.; Van Moer, K.; Kreis, S.; Guerin, C.; Buart, S. Targeting autophagy inhibits melanoma growth by enhancing NK cells infiltration in a CCL5-dependent manner. Proc. Natl. Acad. Sci. USA 2017, 114, E9271-E9279.
Gooden, M.J.; de Bock, G.H.; Leffers, N.; Daemen, T.; Nijman, H.W. The prognostic influence of tumour-infiltrating lymphocytes in cancer: A systematic review with meta-analysis. Br. J. Cancer 2011, 105, 93-103.
Luster, A.D.; Leder, P. IP-10, a-CXC-chemokine, elicits a potent thymus-dependent antitumor response in vivo. J. Exp. Med. 1993, 178, 1057-1065.
Mullins, I.M.; Slingluff, C.L.; Lee, J.K.; Garbee, C.F.; Shu, J.; Anderson, S.G.; Mayer, M.E.; Knaus, W.A.; Mullins, D.W. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res. 2004, 64, 7697-7701.
Hensbergen, P.J.; Wijnands, P.G.B.; Schreurs, M.W.; Scheper, R.J.; Willemze, R.; Tensen, C.P. The CXCR3 targeting chemokine CXCL11 has potent antitumor activity in vivo involving attraction of CD8+ T lymphocytes but not inhibition of angiogenesis. J. Immunother. 2005, 28, 343-351.
Pan, J.; Burdick, M.D.; Belperio, J.A.; Xue, Y.Y.; Gerard, C.; Sharma, S.; Dubinett, S.M.; Strieter, R.M. CXCR3/CXCR3 ligand biological axis impairs RENCA tumor growth by a mechanism of immunoangiostasis. J. Immunol. 2006, 176, 1456-1464.
Reckamp, K.L.; Figlin, R.A.; Moldawer, N.; Pantuck, A.J.; Belldegrun, A.S.; Burdick, M.D.; Strieter, R.M. Expression of CXCR3 on mononuclear cells and CXCR3 ligands in patients with metastatic renal cell carcinoma in response to systemic IL-2 therapy. J. Immunother. 2007, 30, 417-424.
Mikucki, M.; Fisher, D.; Matsuzaki, J.; Skitzki, J.; Gaulin, N.; Muhitch, J.; Ku, A.; Frelinger, J.; Odunsi, K.; Gajewski, T. Non-redundant requirement for CXCR3 signalling during tumoricidal T-cell trafficking across tumour vascular checkpoints. Nat. Commun. 2015, 6, 7458.
Chheda, Z.S.; Sharma, R.K.; Jala, V.R.; Luster, A.D.; Haribabu, B. Chemoattractant receptors BLT1 and CXCR3 regulate antitumor immunity by facilitating CD8+ T cell migration into tumors. J. Immunol. 2016, 197, 2016-2026.
Oghumu, S.; Varikuti, S.; Terrazas, C.; Kotov, D.; Nasser, M.W.; Powell, C.A.; Ganju, R.K.; Satoskar, A.R. CXCR 3 deficiency enhances tumor progression by promoting macrophage M2 polarization in a murine breast cancer model. Immunology 2014, 143, 109-119.
Li, K.; Zhu, Z.; Luo, J.; Fang, J.; Zhou, H.; Hu, M.; Maskey, N.; Yang, G. Impact of chemokine receptor CXCR3 on tumor-infiltrating lymphocyte recruitment associated with favorable prognosis in advanced gastric cancer. Int. J. Clin. Exp. Pathol. 2015, 8, 14725.
Wendel, M.; Galani, I.E.; Suri-Payer, E.; Cerwenka, A. Natural killer cell accumulation in tumors is dependent on IFN-γ and CXCR3 ligands. Cancer Res. 2008, 68, 8437-8445.
Wenzel, J.; Bekisch, B.; Uerlich, M.; Haller, O.; Bieber, T.; Tüting, T. Type I interferon-associated recruitment of cytotoxic lymphocytes: A common mechanism in regressive melanocytic lesions. Am. J. Clin. Pathol. 2005, 124, 37-48.
Redjimi, N.; Raffin, C.; Raimbaud, I.; Pignon, P.; Matsuzaki, J.; Odunsi, K.; Valmori, D.; Ayyoub, M. CXCR3+ T regulatory cells selectively accumulate in human ovarian carcinomas to limit type I immunity. Cancer Res. 2012, 72, 4351-4360.
Li, C.X.; Ling, C.C.; Shao, Y.; Xu, A.; Li, X.C.; Ng, K.T.-P.; Liu, X.B.; Ma, Y.Y.; Qi, X.; Liu, H. CXCL10/CXCR3 signaling mobilized-regulatory T cells promote liver tumor recurrence after transplantation. J. Hepatol. 2016, 65, 944-952.
Winkler, A.E.; Brotman, J.J.; Pittman, M.E.; Judd, N.P.; Lewis, J.S.; Schreiber, R.D.; Uppaluri, R. CXCR3 enhances a T cell dependent epidermal proliferative response and promotes skin tumorigenesis. Cancer Res. 2011, 71, 5707-5716.
Schumacher, K.; Haensch, W.; Röefzaad, C.; Schlag, P.M. Prognostic significance of activated CD8+ T cell infiltrations within esophageal carcinomas. Cancer Res. 2001, 61, 3932-3936.
Sackstein, R.; Schatton, T.; Barthel, S.R. T-lymphocyte homing: An underappreciated yet critical hurdle for successful cancer immunotherapy. Lab. Investig. 2017, 97, 669-697.
Pauken, K.E.; Jenkins, M.K.; Azuma, M.; Fife, B.T. PD-1, but not PD-L1, expressed by islet-reactive CD4+ T cells suppresses infiltration of the pancreas during type 1 diabetes. Diabetes 2013, 62, 2859-2869.
Maru, S.V.; Holloway, K.A.; Flynn, G.; Lancashire, C.L.; Loughlin, A.J.; Male, D.K.; Romero, I.A. Chemokine production and chemokine receptor expression by human glioma cells: Role of CXCL10 in tumour cell proliferation. J. Neuroimmunol. 2008, 199, 35-45.
Giuliani, N.; Bonomini, S.; Romagnani, P.; Lazzaretti, M.; Morandi, F.; Colla, S.; Tagliaferri, S.; Lasagni, L.; Annunziato, F.; Crugnola, M. CXCR3 and its binding chemokines in myeloma cells: Expression of isoforms and potential relationships with myeloma cell proliferation and survival. Haematologica 2006, 91, 1489-1497.
Bai, M.; Chen, X.; Ba, Y. CXCL10/CXCR3 overexpression as a biomarker of poor prognosis in patients with stage II colorectal cancer. Mol. Clin. Oncol. 2016, 4, 23-30.
Urra, S.; Fischer, M.C.; Martínez, J.R.; Véliz, L.; Orellana, P.; Solar, A.; Bohmwald, K.; Kalergis, A.; Riedel, C.; Corvalán, A.H. Differential expression profile of CXCR3 splicing variants is associated with thyroid neoplasia. Potential role in papillary thyroid carcinoma oncogenesis? Oncotarget 2018, 9, 2445-2467.
Klatte, T.; Seligson, D.B.; Leppert, J.T.; Riggs, S.B.; Yu, H.; Zomorodian, N.; Kabbinavar, F.F.; Strieter, R.M.; Belldegrun, A.S.; Pantuck, A.J. The chemokine receptor CXCR3 is an independent prognostic factor in patients with localized clear cell renal cell carcinoma. J. Urol. 2008, 179, 61-66.
Kawada, K.; Sonoshita, M.; Sakashita, H.; Takabayashi, A.; Yamaoka, Y.; Manabe, T.; Inaba, K.; Minato, N.; Oshima, M.; Taketo, M.M. Pivotal role of CXCR3 in melanoma cell metastasis to lymph nodes. Cancer Res. 2004, 64, 4010-4017.
Monteagudo, C.; Martin, J.M.; Jorda, E.; Llombart-Bosch, A. CXCR3 chemokine receptor immunoreactivity in primary cutaneous malignant melanoma: Correlation with clinicopathological prognostic factors. J. Clin. Pathol. 2007, 60, 596-599.
Magro, C.M.; Momtahen, S.; Lee, B.A.; Swanson, D.L.; Pavlovic, M.D. Epidermotropic B-cell lymphoma: A unique subset of CXCR3-positive marginal zone lymphoma. Am. J. Dermatopathol. 2016, 38, 105-112.
Trentin, L.; Agostini, C.; Facco, M.; Piazza, F.; Perin, A.; Siviero, M.; Gurrieri, C.; Galvan, S.; Adami, F.; Zambello, R. The chemokine receptor CXCR3 is expressed on malignant B cells and mediates chemotaxis. J. Clin. Investig. 1999, 104, 115-121.
Pu, Y.; Li, S.; Zhang, C.; Bao, Z.; Yang, Z.; Sun, L. High expression of CXCR3 is an independent prognostic factor in glioblastoma patients that promotes an invasive phenotype. J. Neuro-Oncol. 2015, 122, 43-51.
Murakami, T.; Kawada, K.; Iwamoto, M.; Akagami, M.; Hida, K.; Nakanishi, Y.; Kanda, K.; Kawada, M.; Seno, H.; Taketo, M.M. The role of CXCR3 and CXCR4 in colorectal cancer metastasis. Int. J. Cancer 2013, 132, 276-287.
Kawada, K.; Hosogi, H.; Sonoshita, M.; Sakashita, H.; Manabe, T.; Shimahara, Y.; Sakai, Y.; Takabayashi, A.; Oshima, M.; Taketo, M. Chemokine receptor CXCR3 promotes colon cancer metastasis to lymph nodes. Oncogene 2007, 26, 4679-4688.
Windmüller, C.; Zech, D.; Avril, S.; Boxberg, M.; Dawidek, T.; Schmalfeldt, B.; Schmitt, M.; Kiechle, M.; Bronger, H. CXCR3 mediates ascites-directed tumor cell migration and predicts poor outcome in ovarian cancer patients. Oncogenesis 2017, 6, e331.
Duruisseaux, M.; Rabbe, N.; Antoine, M.; Vieira, T.; Poulot, V.; Cadranel, J.; Wislez, M. Pro-tumoural CXCL10/CXCR3-A autocrine loop in invasive mucinous lung adenocarcinoma. ERJ Open Res. 2017, 3.
Ma, X.; Norsworthy, K.; Kundu, N.; Rodgers, W.H.; Gimotty, P.A.; Goloubeva, O.; Lipsky, M.; Li, Y.; Holt, D.; Fulton, A. CXCR3 expression is associated with poor survival in breast cancer and promotes metastasis in a murine model. Mol. Cancer Ther. 2009, 8, 490-498.
Zhu, G.; Yan, H.H.; Pang, Y.; Jian, J.; Achyut, B.R.; Liang, X.; Weiss, J.M.; Wiltrout, R.H.; Hollander, M.C.; Yang, L. CXCR3 as a molecular target in breast cancer metastasis: Inhibition of tumor cell migration and promotion of host anti-tumor immunity. Oncotarget 2015, 6, 43408-43419.
Romagnani, P.; Maggi, L.; Mazzinghi, B.; Cosmi, L.; Lasagni, L.; Liotta, F.; Lazzeri, E.; Angeli, R.; Rotondi, M.; Filì, L. CXCR3-mediated opposite effects of CXCL10 and CXCL4 on TH1 or TH2 cytokine production. J. Allergy Clin. Immunol. 2005, 116, 1372-1379.
Kelsen, S.G.; Aksoy, M.O.; Yang, Y.; Shahabuddin, S.; Litvin, J.; Safadi, F.; Rogers, T.J. The chemokine receptor CXCR3 and its splice variant are expressed in human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004, 287, L584-L591.
Bodnar, R.J.; Wells, A. Differential regulation of pericyte function by the CXC receptor 3. Wound Repair Regen. 2015, 23, 785-796.
Murdoch, C.; Monk, P.N.; Finn, A. Cxc chemokine receptor expression on human endothelial cells. Cytokine 1999, 11, 704-712.
Datta, D.; Contreras, A.G.; Grimm, M.; Waaga-Gasser, A.M.; Briscoe, D.M.; Pal, S. Calcineurin inhibitors modulate CXCR3 splice variant expression and mediate renal cancer progression. J. Am. Soc. Nephrol. 2008, 19, 2437-2446.
Datta, D.; Banerjee, P.; Gasser, M.; Waaga-Gasser, A.M.; Pal, S. CXCR3-B can mediate growth-inhibitory signals in human renal cancer cells by down-regulating the expression of heme oxygenase-1. J. Biol. Chem. 2010, 285, 36842-36848.
Furuya, M.; Yoneyama, T.; Miyagi, E.; Tanaka, R.; Nagahama, K.; Miyagi, Y.; Nagashima, Y.; Hirahara, F.; Inayama, Y.; Aoki, I. Differential expression patterns of CXCR3 variants and corresponding CXC chemokines in clear cell ovarian cancers and endometriosis. Gynecol. Oncol. 2011, 122, 648-655.
Balan, M.; Pal, S. A novel CXCR3-B chemokine receptor-induced growth-inhibitory signal in cancer cells is mediated through the regulation of Bach-1 protein and Nrf2 protein nuclear translocation. J. Biol. Chem. 2014, 289, 3126-3137.
Datta, D.; Flaxenburg, J.A.; Laxmanan, S.; Geehan, C.; Grimm, M.; Waaga-Gasser, A.M.; Briscoe, D.M.; 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.
Gacci, M.; Serni, S.; Lapini, A.; Vittori, G.; Alessandrini, M.; Nesi, G.; Palli, D.; Carini, M. CXCR3-B expression correlates with tumor necrosis extension in renal cell carcinoma. J. Urol. 2009, 181, 843-848.
Li, Y.; Reader, J.C.; Ma, X.; Kundu, N.; Kochel, T.; Fulton, A.M. Divergent roles of CXCR3 isoforms in promoting cancer stem-like cell survival and metastasis. Breast Cancer Res. Treat. 2015, 149, 403-415.
De Palma, M.; Biziato, D.; Petrova, T.V. Microenvironmental regulation of tumour angiogenesis. Nat. Rev. Cancer 2017, 17, 457-474.
Bergers, G.; Benjamin, L.E. Angiogenesis: Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 2003, 3, 401-410.
Maione, T.E.; Gray, G.S.; Petro, J.; Hunt, A.J.; Donner, A.L.; Bauer, S.I.; Carson, H.F.; Sharpe, R.J. Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science 1990, 247, 77-79.
Luster, A.D.; Greenberg, S.M.; Leder, P. The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J. Exp. Med. 1995, 182, 219-231.
Strieter, R.M.; Polverini, P.J.; Kunkel, S.L.; Arenberg, D.A.; Burdick, M.D.; Kasper, J.; Dzuiba, J.; Van Damme, J.; Walz, A.; Marriott, D. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 1995, 270, 27348-27357.
Angiolillo, A.L.; Sgadari, C.; Taub, D.D.; Liao, F.; Farber, J.M.; Maheshwari, S.; Kleinman, H.K.; Reaman, G.H.; Tosato, G. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med. 1995, 182, 155-162.
Arenberg, D.A.; Kunkel, S.L.; Polverini, P.J.; Morris, S.B.; Burdick, M.D.; Glass, M.C.; Taub, D.T.; Iannettoni, M.D.; Whyte, R.I.; Strieter, R.M. Interferon-gamma-inducible protein 10 (IP-10) is an angiostatic factor that inhibits human non-small cell lung cancer (NSCLC) tumorigenesis and spontaneous metastases. J. Exp. Med. 1996, 184, 981-992.
Rupertus, K.; Sinistra, J.; Scheuer, C.; Nickels, R.M.; Schilling, M.K.; Menger, M.D.; Kollmar, O. Interaction of the chemokines I-TAC (CXCL11) and SDF-1 (CXCL12) in the regulation of tumor angiogenesis of colorectal cancer. Clin. Exp. Metastasis 2014, 31, 447-459.
Campanella, G.S.; Colvin, R.A.; Luster, A.D. CXCL10 can inhibit endothelial cell proliferation independently of CXCR3. PLoS ONE 2010, 5, e12700.
Nagarsheth, N.; Peng, D.; Kryczek, I.; Wu, K.; Li, W.; Zhao, E.; Zhao, L.; Wei, S.; Frankel, T.; Vatan, L. PRC2 epigenetically silences Th1-type chemokines to suppress effector T-cell trafficking in colon cancer. Cancer Res. 2016, 76, 275-282.
Bronger, H.; Singer, J.; Windmüller, C.; Reuning, U.; Zech, D.; Delbridge, C.; Dorn, J.; Kiechle, M.; Schmalfeldt, B.; Schmitt, M., et al. CXCL9 and CXCL10 predict survival and are regulated by cyclooxygenase inhibition in advanced serous ovarian cancer. Br. J. Cancer 2016, 115, 553-563.
Bronger, H.; Kraeft, S.; Schwarz-Boeger, U.; Cerny, C.; Stöckel, A.; Avril, S.; Kiechle, M.; Schmitt, M. Modulation of CXCR3 ligand secretion by prostaglandin E2 and cyclooxygenase inhibitors in human breast cancer. Breast Cancer Res. 2012, 14, R30.
Havre, P.A.; Abe, M.; Urasaki, Y.; Ohnuma, K.; Morimoto, C.; Dang, N.H. The role of CD26/dipeptidyl peptidase IV in cancer. Front. Biosci. 2008, 13, 1634-1645.
Mortier, A.; Van Damme, J.; Proost, P. Overview of the mechanisms regulating chemokine activity and availability. Immunol. Lett. 2012, 145, 2-9.
Proost, P.; Schutyser, E.; Menten, P.; Struyf, S.; Wuyts, A.; Opdenakker, G.; Detheux, M.; Parmentier, M.; Durinx, C.; Lambeir, A.-M. Amino-terminal truncation of CXCR3 agonists impairs receptor signaling and lymphocyte chemotaxis, while preserving antiangiogenic properties. Blood 2001, 98, 3554-3561.
Karin, N.; Wildbaum, G.; Thelen, M. Biased signaling pathways via CXCR3 control the development and function of CD4+ T cell subsets. J. Leukoc. Biol. 2016, 99, 857-862.
Zhang, C.; Li, Z.; Xu, L.; Che, X.; Wen, T.; Fan, Y.; Li, C.; Wang, S.; Cheng, Y.; Wang, X. CXCL9/10/11, a regulator of PD-L1 expression in gastric cancer. BMC Cancer 2018, 18, 462.
Szpakowska, M.; Nevins, A.M.; Meyrath, M.; Rhainds, D.; D’huys, T.; Guité-Vinet, F.; Dupuis, N.; Gauthier, P.A.; Counson, M.; Kleist, A. Different contributions of chemokine N-terminal features attest to a different ligand binding mode and a bias towards activation of ACKR3/CXCR7 compared with CXCR4 and CXCR3. Br. J. Pharmacol. 2018, 175, 1419-1438.
Sierro, F.; Biben, C.; Martínez-Muñoz, L.; Mellado, M.; Ransohoff, R.M.; Li, M.; Woehl, B.; Leung, H.; Groom, J.; Batten, M. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA 2007, 104, 14759-14764.
Zohar, Y.; Wildbaum, G.; Novak, R.; Salzman, A.L.; Thelen, M.; Alon, R.; Barsheshet, Y.; Karp, C.L.; Karin, N. CXCL11-dependent induction of FOXP3-negative regulatory T cells suppresses autoimmune encephalomyelitis. J. Clin. Investig. 2014, 124, 2009-2022.
Heise, C.E.; Pahuja, A.; Hudson, S.C.; Mistry, M.S.; Putnam, A.L.; Gross, M.M.; Gottlieb, P.A.; Wade, W.S.; Kiankarimi, M.; Schwarz, D. Pharmacological characterization of CXC chemokine receptor 3 ligands and a small molecule antagonist. J. Pharmacol. Exp. Ther. 2005, 313, 1263-1271.
Proost, P.; Verpoest, S.; Van de Borne, K.; Schutyser, E.; Struyf, S.; Put, W.; Ronsse, I.; Grillet, B.; Opdenakker, G.; Van Damme, J. Synergistic induction of CXCL9 and CXCL11 by Toll-like receptor ligands and interferon-γ in fibroblasts correlates with elevated levels of CXCR3 ligands in septic arthritis synovial fluids. J. Leukoc. Biol. 2004, 75, 777-784.
Sauty, A.; Colvin, R.A.; Wagner, L.; Rochat, S.; Spertini, F.; Luster, A.D. CXCR3 internalization following T cell-endothelial cell contact: Preferential role of IFN-inducible T cell α chemoattractant (CXCL11). J. Immunol. 2001, 167, 7084-7093.
Szpakowska, M.; Meyrath, M.; Reynders, N.; Counson, M.; Hanson, J.; Steyaert, J.; Chevigné, A. Mutational analysis of the extracellular disulphide bridges of the atypical chemokine receptor ACKR3/CXCR7 uncovers multiple binding and activation modes for its chemokine and endogenous non-chemokine agonists. Biochem. Pharmacol. 2018, 153, 299-309.
Burns, J.M.; Summers, B.C.; Wang, Y.; Melikian, A.; Berahovich, R.; Miao, Z.; Penfold, M.E.; Sunshine, M.J.; Littman, D.R.; Kuo, C.J. 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.
Massara, M.; Bonavita, O.; Mantovani, A.; Locati, M.; Bonecchi, R. Atypical chemokine receptors in cancer: Friends or foes? J. Leukoc. Biol. 2016, 99, 927-933.
Freitas, C.; Desnoyer, A.; Meuris, F.; Bachelerie, F.; Balabanian, K.; Machelon, V. The relevance of the chemokine receptor ACKR3/CXCR7 on CXCL12-mediated effects in cancers with a focus on virus-related cancers. Cytokine Growth Factor Rev. 2014, 25, 307-316.
Gao, Y.J.; De Lin Liu, S.L.; Yuan, G.F.; Li, L.; Zhu, H.Y.; Cao, G.Y. Down-regulation of cXcl11 inhibits colorectal cancer cell growth and epithelial-mesenchymal transition. Oncotargets Ther. 2018, 11, 7333-7343.
Zhang, Y.; Zhao, W.; Li, S.; Lv, M.; Yang, X.; Li, M.; Zhang, Z. CXCL11 promotes self-renewal and tumorigenicity of α2δ1+ liver tumor-initiating cells through CXCR3/ERK1/2 signaling. Cancer Lett. 2019, 449, 163-171.
Mulligan, A.M.; Raitman, I.; Feeley, L.; Pinnaduwage, D.; Nguyen, L.T.; O’Malley, F.P.; Ohashi, P.S.; Andrulis, I.L. Tumoral lymphocytic infiltration and expression of the chemokine CXCL10 in breast cancers from the Ontario Familial Breast Cancer Registry. Clin. Cancer Res. 2013, 19, 336-346.
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.
Zipin-Roitman, A.; Meshel, T.; Sagi-Assif, O.; Shalmon, B.; Avivi, C.; Pfeffer, R.M.; Witz, I.P.; Ben-Baruch, A. CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res. 2007, 67, 3396-3405.
Zumwalt, T.J.; Arnold, M.; Goel, A.; Boland, C.R. Active secretion of CXCL10 and CCL5 from colorectal cancer microenvironments associates with GranzymeB+ CD8+ T-cell infiltration. Oncotarget 2014, 6, 2981-2991.
Sato, Y.; Motoyama, S.; Nanjo, H.; Wakita, A.; Yoshino, K.; Sasaki, T.; Nagaki, Y.; Liu, J.; Imai, K.; Saito, H. CXCL10 expression status is prognostic in patients with advanced thoracic esophageal squamous cell carcinoma. Ann. Surg. Oncol. 2016, 23, 936-942.
Wightman, S.; Uppal, A.; Pitroda, S.; Ganai, S.; Burnette, B.; Stack, M.; Oshima, G.; Khan, S.; Huang, X.; Posner, M. Oncogenic CXCL10 signalling drives metastasis development and poor clinical outcome. Br. J. Cancer 2015, 113, 327-335.
Wu, Z.; Huang, X.; Han, X.; Li, Z.; Zhu, Q.; Yan, J.; Yu, S.; Jin, Z.; Wang, Z.; Zheng, Q. The chemokine CXCL9 expression is associated with better prognosis for colorectal carcinoma patients. Biomed. Pharmacother. 2016, 78, 8-13.
Cao, Y.; Huang, H.; Wang, Z.; Zhang, G. The Inflammatory CXC Chemokines, GROαhigh, IP-10low, and MIGlow, in Tumor Microenvironment Can Be Used as New Indicators for Non-small Cell Lung Cancer Progression. Immunol. Investig. 2017, 46, 361-374.
Gorbachev, A.V.; Kobayashi, H.; Kudo, D.; Tannenbaum, C.S.; Finke, J.H.; Shu, S.; Farber, J.M.; Fairchild, R.L. CXC chemokine ligand 9/monokine induced by IFN-γ production by tumor cells is critical for T cell-mediated suppression of cutaneous tumors. J. Immunol. 2007, 178, 2278-2286.
Ohtani, H.; Jin, Z.; Takegawa, S.; Nakayama, T.; Yoshie, O. Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3+ T cells in lymphocyte-rich gastric carcinoma. J. Pathol. A J. Pathol. Soc. Great Br. Irel. 2009, 217, 21-31.
Sgadari, C.; Farber, J.M.; Angiolillo, A.L.; Liao, F.; Teruya-Feldstein, J.; Burd, P.R.; Yao, L.; Gupta, G.; Kanegane, C.; Tosato, G. Mig, the monokine induced by interferon-γ, promotes tumor necrosis in vivo. Blood 1997, 89, 2635-2643.
Amatschek, S.; Lucas, R.; Eger, A.; Pflueger, M.; Hundsberger, H.; Knoll, C.; Grosse-Kracht, S.; Schuett, W.; Koszik, F.; Maurer, D. CXCL9 induces chemotaxis, chemorepulsion and endothelial barrier disruption through CXCR3-mediated activation of melanoma cells. Br. J. Cancer 2011, 104, 469-479.
Li, Z.; Liu, J.; Li, L.; Shao, S.; Wu, J.; Bian, L.; He, Y. Epithelial mesenchymal transition induced by the CXCL9/CXCR3 axis through AKT activation promotes invasion and metastasis in tongue squamous cell carcinoma. Oncol. Rep. 2018, 39, 1356-1368.
Mir, M.A.; Maurer, M.J.; Ziesmer, S.C.; Slager, S.L.; Habermann, T.; Macon, W.R.; Link, B.K.; Syrbu, S.; Witzig, T.; Friedberg, J.W. Elevated serum levels of IL-2R, IL-1RA, and CXCL9 are associated with a poor prognosis in follicular lymphoma. Blood 2015, 125, 992-998.
Pucci, F.; Rickelt, S.; Newton, A.P.; Garris, C.; Nunes, E.; Evavold, C.; Pfirschke, C.; Engblom, C.; Mino-Kenudson, M.; Hynes, R.O. PF4 promotes platelet production and lung cancer growth. Cell Rep. 2016, 17, 1764-1772.
Deng, S.; Deng, Q.; Zhang, Y.; Ye, H.; Yu, X.; Zhang, Y.; Han, G.Y.; Luo, P.; Wu, M.; Yu, Y. Non-platelet-derived CXCL4 differentially regulates cytotoxic and regulatory T cells through CXCR3 to suppress the immune response to colon cancer. Cancer Lett. 2019, 443, 1-12.
Zhang, Y.; Gao, J.; Wang, X.; Deng, S.; Ye, H.; Guan, W.; Wu, M.; Zhu, S.; Yu, Y.; Han, W. CXCL4 mediates tumor regrowth after chemotherapy by suppression of antitumor immunity. Cancer Biol. Ther. 2015, 16, 1775-1783.
Struyf, S.; Salogni, L.; Burdick, M.D.; Vandercappellen, J.; Gouwy, M.; Noppen, S.; Proost, P.; Opdenakker, G.; Parmentier, M.; Gerard, C. Angiostatic and chemotactic activities of the CXC chemokine CXCL4L1 (platelet factor-4 variant) are mediated by CXCR3. Blood 2011, 117, 480-488.
Struyf, S.; Burdick, M.D.; Proost, P.; Van Damme, J.; Strieter, R.M. Platelets release CXCL4L1, a nonallelic variant of the chemokine platelet factor-4/CXCL4 and potent inhibitor of angiogenesis. Circ. Res. 2004, 95, 855-857.
Struyf, S.; Burdick, M.D.; Peeters, E.; Van den Broeck, K.; Dillen, C.; Proost, P.; Van Damme, J.; Strieter, R.M. Platelet factor-4 variant chemokine CXCL4L1 inhibits melanoma and lung carcinoma growth and metastasis by preventing angiogenesis. Cancer Res. 2007, 67, 5940-5948.
Quemener, C.; Baud, J.; Boyé, K.; Dubrac, A.; Billottet, C.; Soulet, F.; Darlot, F.; Dumartin, L.; Sire, M.; Grepin, R. Dual roles for CXCL4 chemokines and CXCR3 in angiogenesis and invasion of pancreatic cancer. Cancer Res. 2016, 76, 6507-6519.
Karjalainen, M.K.; Ojaniemi, M.; Haapalainen, A.M.; Mahlman, M.; Salminen, A.; Huusko, J.M.; Määttä, T.A.; Kaukola, T.; Anttonen, J.; Ulvila, J. CXCR3 polymorphism and expression associate with spontaneous preterm birth. J. Immunol. 2015, 195, 2187-2198.
Wu, Q.; Dhir, R.; Wells, A. Altered CXCR3 isoform expression regulates prostate cancer cell migration and invasion. Mol. Cancer 2012, 11, 3.
Baribaud, F.; Edwards, T.G.; Sharron, M.; Brelot, A.; Heveker, N.; Price, K.; Mortari, F.; Alizon, M.; Tsang, M.; Doms, R.W. Antigenically distinct conformations of CXCR4. J. Virol. 2001, 75, 8957-8967.
Blanpain, C.; Vanderwinden, J.-M.; Cihak, J.; Wittamer, V.; Le Poul, E.; Issafras, H.; Stangassinger, M.; Vassart, G.; Marullo, S.; Schlöndorff, D., et al. Multiple active states and oligomerization of CCR5 revealed by functional properties of monoclonal antibodies. Mol. Biol. Cell 2002, 13, 723-737.
Jopling, L.; Watt, G.; Fisher, S.; Birch, H.; Coggon, S.; Christie, M. Analysis of the pharmacokinetic/pharmacodynamic relationship of a small molecule CXCR3 antagonist, NBI-74330, using a murine CXCR3 internalization assay. Br. J. Pharmacol. 2007, 152, 1260-1271.
Scholten, D.; Canals, M.; Wijtmans, M.; De Munnik, S.; Nguyen, P.; Verzijl, D.; De Esch, I.; Vischer, H.; Smit, M.; Leurs, R. Pharmacological characterization of a small-molecule agonist for the chemokine receptor CXCR3. Br. J. Pharmacol. 2012, 166, 898-911.
Andrews, S.P.; Cox, R.J. Small molecule CXCR3 antagonists. J. Med. Chem. 2015, 59, 2894-2917.