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triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway
Department of Immunology and Oncology, Centro Nacional de Biotecnología, CSIC-Universidad Autónoma de Madrid, Campus de Cantoblanco, E-28049 Madrid, Spain
1Correspondence: Department of Immunology and Oncology, Centro Nacional de Biotecnología, CSIC, Universidad Autónoma de Madrid, Campus de Cantoblanco, E-28049 Madrid, Spain. E-mail cmartineza{at}cnb.uam.es
The chemokine stromal cell-derived factor (SDF-1
), the ligand for the
CXCR4 receptor, induces a wide variety of effects that include calcium
mobilization, chemotactic responses, bone marrow myelopoiesis, neuronal
patterning, and prevention of HIV-1 infection. Nonetheless, little is
known of the biochemical pathways required to achieve this variety of
responses triggered after receptor–chemokine interaction. We developed
a set of monoclonal antibodies that specifically recognize the CXCR4
receptor and used them to identify the signaling pathway activated
after SDF-1 binding in human T cell lines. Here we demonstrate that
SDF-1 activation promotes the physical association of
Gi with the CXCR4. Furthermore, within seconds of
SDF-1 activation, the CXCR4 receptor becomes tyrosine phosphorylated
through the activation and association with the receptor of JAK2 and
JAK3 kinases. After SDF-1 binding, JAK2 and JAK3 associate with
CXCR4 and are activated, probably by transphosphorylation, in a
Gi-independent manner. This activation enables the
recruitment and tyrosine phosphorylation of several members of the STAT
family of transcription factors. Finally, we have also observed
SDF-1-induced activation and association of the tyrosine phosphatase
Shp1 with the CXCR4 in a Gi-dependent manner. As occurs
with the cytokine receptors in response to cytokines, the CXCR4
undergoes receptor dimerization after SDF-1 binding and is a
critical step in triggering biological responses. We present compelling
evidence that the chemokines signal through mechanisms similar to those
activated by cytokines.—Vila-Coro, A. J.,
Rodríguez-Frade, J. M., Martín de Ana, A.,
Moreno-Ortíz, M. C., Martínez-A., C., Mellado, M.
The chemokine SDF-1 triggers CXCR4 receptor dimerization and
activates the JAK/STAT pathway.
Key Words: chemotactic response • tyrosine phosphorylation • Shp1 • G-proteins
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 S. F. Soriano, P. Hernanz-Falcon, J. M. Rodriguez-Frade, A. M. de Ana, R. Garzon, C. Carvalho-Pinto, A. J. Vila-Coro, A. Zaballos, D. Balomenos, C. Martinez-A., et al. Functional Inactivation of CXC Chemokine Receptor 4-mediated Responses through SOCS3 Up-regulation J. Exp. Med., August 5, 2002; 196(3): 311 - 321. [Abstract] [Full Text] [PDF]
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T. Netelenbos, S. Zuijderduijn, J. van den Born, F. L. Kessler, S. Zweegman, P. C. Huijgens, and A. M. Drager Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells J. Leukoc. Biol., August 1, 2002; 72(2): 353 - 362. [Abstract] [Full Text] [PDF]
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J. A. Fox, K. Ung, S. G. Tanlimco, and F. R. Jirik Disruption of a Single Pten Allele Augments the Chemotactic Response of B Lymphocytes to Stromal Cell-Derived Factor-1 J. Immunol., July 1, 2002; 169(1): 49 - 54. [Abstract] [Full Text] [PDF]
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V. Grabovsky, O. Dwir, and R. Alon Endothelial Chemokines Destabilize L-selectin-mediated Lymphocyte Rolling without Inducing Selectin Shedding J. Biol. Chem., May 31, 2002; 277(23): 20640 - 20650. [Abstract] [Full Text] [PDF]
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N. Wright, A. Hidalgo, J. M. Rodriguez-Frade, S. F. Soriano, M. Mellado, M. Parmo-Cabanas, M. J. Briskin, and J. Teixido The Chemokine Stromal Cell-Derived Factor-1{alpha} Modulates {alpha}4{beta}7 Integrin-Mediated Lymphocyte Adhesion to Mucosal Addressin Cell Adhesion Molecule-1 and Fibronectin J. Immunol., May 15, 2002; 168(10): 5268 - 5277. [Abstract] [Full Text] [PDF]
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T. Hideshima, D. Chauhan, T. Hayashi, K. Podar, M. Akiyama, D. Gupta, P. Richardson, N. Munshi, and K. C. Anderson The Biological Sequelae of Stromal Cell-derived Factor-1{alpha} in Multiple Myeloma Mol. Cancer Ther., May 1, 2002; 1(7): 539 - 544. [Abstract] [Full Text] [PDF]
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R. C. Patel, U. Kumar, D. C. Lamb, J. S. Eid, M. Rocheville, M. Grant, A. Rani, T. Hazlett, S. C. Patel, E. Gratton, et al. Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells PNAS, March 5, 2002; 99(5): 3294 - 3299. [Abstract] [Full Text] [PDF]
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S. Fruehauf, K. Srbic, R. Seggewiss, J. Topaly, and A. D. Ho Functional characterization of podia formation in normal and malignant hematopoietic cells J. Leukoc. Biol., March 1, 2002; 71(3): 425 - 432. [Abstract] [Full Text] [PDF]
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M. Nishita, H. Aizawa, and K. Mizuno Stromal Cell-Derived Factor 1{alpha} Activates LIM Kinase 1 and Induces Cofilin Phosphorylation for T-Cell Chemotaxis Mol. Cell. Biol., February 1, 2002; 22(3): 774 - 783. [Abstract] [Full Text] [PDF]
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M. Vicente-Manzanares, J. R. Cabrero, M. Rey, M. Perez-Martinez, A. Ursa, K. Itoh, and F. Sanchez-Madrid A Role for the Rho-p160 Rho Coiled-Coil Kinase Axis in the Chemokine Stromal Cell-Derived Factor-1{alpha}-Induced Lymphocyte Actomyosin and Microtubular Organization and Chemotaxis J. Immunol., January 1, 2002; 168(1): 400 - 410. [Abstract] [Full Text] [PDF]
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H. Geminder, O. Sagi-Assif, L. Goldberg, T. Meshel, G. Rechavi, I. P. Witz, and A. Ben-Baruch A Possible Role for CXCR4 and Its Ligand, the CXC Chemokine Stromal Cell-Derived Factor-1, in the Development of Bone Marrow Metastases in Neuroblastoma J. Immunol., October 15, 2001; 167(8): 4747 - 4757. [Abstract] [Full Text] [PDF]
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N. C. Ottoson, J. T. Pribila, A. S. H. Chan, and Y. Shimizu Cutting Edge: T Cell Migration Regulated by CXCR4 Chemokine Receptor Signaling to ZAP-70 Tyrosine Kinase J. Immunol., August 15, 2001; 167(4): 1857 - 1861. [Abstract] [Full Text] [PDF]
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B.-S. Youn, Y. J. Kim, C. Mantel, K.-Y. Yu, and H. E. Broxmeyer Blocking of c-FLIPL-independent cycloheximide-induced apoptosis or Fas-mediated apoptosis by the CC chemokine receptor 9/TECK interaction Blood, August 15, 2001; 98(4): 925 - 933. [Abstract] [Full Text] [PDF]
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N. Heveker, M. Tissot, A. Thuret, J. Schneider-Mergener, M. Alizon, M. Roch, and S. Marullo Pharmacological Properties of Peptides Derived from Stromal Cell-Derived Factor 1: Study on Human Polymorphonuclear Cells Mol. Pharmacol., June 1, 2001; 59(6): 1418 - 1425. [Abstract] [Full Text]
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X.-F. Zhang, J.-F. Wang, E. Matczak, J. Proper, and J. E. Groopman Janus kinase 2 is involved in stromal cell-derived factor-1{alpha}-induced tyrosine phosphorylation of focal adhesion proteins and migration of hematopoietic progenitor cells Blood, June 1, 2001; 97(11): 3342 - 3348. [Abstract] [Full Text] [PDF]
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R. Guerriero, G. Mattia, U. Testa, C. Chelucci, G. Macioce, I. Casella, P. Samoggia, C. Peschle, and H. J. Hassan Stromal cell-derived factor 1{alpha} increases polyploidization of megakaryocytes generated by human hematopoietic progenitor cells Blood, May 1, 2001; 97(9): 2587 - 2595. [Abstract] [Full Text] [PDF]
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R. P. Cherla and R. K. Ganju Stromal Cell-Derived Factor 1{{alpha}}-Induced Chemotaxis in T Cells Is Mediated by Nitric Oxide Signaling Pathways J. Immunol., March 1, 2001; 166(5): 3067 - 3074. [Abstract] [Full Text] [PDF]
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J.-W. Oh, K. Drabik, O. Kutsch, C. Choi, A. Tousson, and E. N. Benveniste CXC Chemokine Receptor 4 Expression and Function in Human Astroglioma Cells J. Immunol., February 15, 2001; 166(4): 2695 - 2704. [Abstract] [Full Text] [PDF]
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A. R. L. Gear, S. Suttitanamongkol, D. Viisoreanu, R. K. Polanowska-Grabowska, S. Raha, and D. Camerini Adenosine diphosphate strongly potentiates the ability of the chemokines MDC, TARC, and SDF-1 to stimulate platelet function Blood, February 15, 2001; 97(4): 937 - 945. [Abstract] [Full Text] [PDF]
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R. D. Chernock, R. P. Cherla, and R. K. Ganju SHP2 and cbl participate in {alpha}-chemokine receptor CXCR4-mediated signaling pathways Blood, February 1, 2001; 97(3): 608 - 615. [Abstract] [Full Text] [PDF]
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G Milligan Oligomerisation of G-protein-coupled receptors J. Cell Sci., January 4, 2001; 114(7): 1265 - 1271. [Abstract] [PDF]
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A. J. Pelletier, L. J. W. van der Laan, P. Hildbrand, M. A. Siani, D. A. Thompson, P. E. Dawson, B. E. Torbett, and D. R. Salomon Presentation of chemokine SDF-1alpha by fibronectin mediates directed migration of T cells Blood, October 15, 2000; 96(8): 2682 - 2690. [Abstract] [Full Text] [PDF]
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 J. B. Johnston, Y. Jiang, G. van Marle, M. B. Mayne, W. Ni, J. Holden, J. C. McArthur, and C. Power Lentivirus Infection in the Brain Induces Matrix Metalloproteinase Expression: Role of Envelope Diversity J. Virol., August 15, 2000; 74(16): 7211 - 7220. [Abstract] [Full Text]
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C. A. Haskell, M. D. Cleary, and I. F. Charo Unique Role of the Chemokine Domain of Fractalkine in Cell Capture. KINETICS OF RECEPTOR DISSOCIATION CORRELATE WITH CELL ADHESION J. Biol. Chem., October 27, 2000; 275(44): 34183 - 34189. [Abstract] [Full Text] [PDF]
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R. Sadir, F. Baleux, A. Grosdidier, A. Imberty, and H. Lortat-Jacob Characterization of the Stromal Cell-derived Factor-1alpha -Heparin Complex J. Biol. Chem., March 9, 2001; 276(11): 8288 - 8296. [Abstract] [Full Text] [PDF]
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M. McVey, D. Ramsay, E. Kellett, S. Rees, S. Wilson, A. J. Pope, and G. Milligan Monitoring Receptor Oligomerization Using Time-resolved Fluorescence Resonance Energy Transfer and Bioluminescence Resonance Energy Transfer. THE HUMAN delta -OPIOID RECEPTOR DISPLAYS CONSTITUTIVE OLIGOMERIZATION AT THE CELL SURFACE, WHICH IS NOT REGULATED BY RECEPTOR OCCUPANCY J. Biol. Chem., April 20, 2001; 276(17): 14092 - 14099. [Abstract] [Full Text] [PDF]
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V. Lukashova, C. Asselin, J. J. Krolewski, M. Rola-Pleszczynski, and J. Stankova G-protein-independent Activation of Tyk2 by the Platelet-activating Factor Receptor J. Biol. Chem., June 22, 2001; 276(26): 24113 - 24121. [Abstract] [Full Text] [PDF]
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J. Wang, E. Guan, G. Roderiquez, V. Calvert, R. Alvarez, and M. A. Norcross Role of Tyrosine Phosphorylation in Ligand-independent Sequestration of CXCR4 in Human Primary Monocytes-Macrophages J. Biol. Chem., December 21, 2001; 276(52): 49236 - 49243. [Abstract] [Full Text] [PDF]
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J. H. White, R. A. J. McIllhinney, A. Wise, F. Ciruela, W.-Y. Chan, P. C. Emson, A. Billinton, and F. H. Marshall The GABAB receptor interacts directly with the related transcription factors CREB2 and ATFx PNAS, December 5, 2000; 97(25): 13967 - 13972. [Abstract] [Full Text] [PDF]
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