Presentation of chemokine SDF-1α by fibronectin mediates directed migration of T cells

The role of chemokine–matrix interactions in integrin-dependent T-cell migration was examined to address the critical question of how chemokines provide directional information. The chemokine SDF-1α binds fibronectin (Fn) with a low nanomolar K d(equilibrium dissociation constant). SDF-1α presented by Fn induced directed migration. Spatial concentration gradients of chemokine were not required to maintain directed migration. Fn-presented chemokine induced the polarization of cells, including the redistribution of the SDF-1α receptor, to the basal surface and leading edge of the cell. A new model for directed migration is proposed in which the co-presentation of an adhesive matrix and chemokine provides the necessary positional information independent of a soluble spatial gradient.

[1]  M. Baggiolini,et al.  Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[2]  S. Miron,et al.  TNF-alpha associated with fibronectin enhances phorbol myristate acetate- or antigen-mediated integrin-dependent adhesion of CD4+ T cells via protein tyrosine phosphorylation. , 1994, Journal of immunology.

[3]  David A. Williams,et al.  Fibronectin improves transduction of reconstituting hematopoietic stem cells by retroviral vectors: evidence of direct viral binding to chymotryptic carboxy-terminal fragments. , 1996, Blood.

[4]  C. Power,et al.  Glycosaminoglycans mediate cell surface oligomerization of chemokines. , 1997, Biochemistry.

[5]  C. Martínez-A,et al.  Membrane raft microdomains mediate front–rear polarity in migrating cells , 1999, The EMBO journal.

[6]  A. Gotoh,et al.  SDF‐1 suppresses cytokine‐induced adhesion of human haemopoietic progenitor cells to immobilized fibronectin , 1999, British journal of haematology.

[7]  David A. Williams,et al.  Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells , 1996, Nature Medicine.

[8]  J. Coligan,et al.  Constitutive activation of integrin alpha 4 beta 1 defines a unique stage of human thymocyte development , 1994, The Journal of experimental medicine.

[9]  Colin R. F. Monks,et al.  Three-dimensional segregation of supramolecular activation clusters in T cells , 1998, Nature.

[10]  F. Sánchez‐Madrid,et al.  Polarization of Chemokine Receptors to the Leading Edge during Lymphocyte Chemotaxis , 1997, The Journal of experimental medicine.

[11]  Masahiko Kuroda,et al.  Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development , 1998, Nature.

[12]  K. Campbell,et al.  Role of α-Dystroglycan as a Schwann Cell Receptor for Mycobacterium leprae , 1998 .

[13]  C. Martínez-A,et al.  The chemokine SDF‐lα triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[14]  A. Calof,et al.  Domain-specific activation of neuronal migration and neurite outgrowth-promoting activities of laminin , 1994, Neuron.

[15]  K. Horgan,et al.  Costimulation of proliferative responses of resting CD4+ T cells by the interaction of VLA-4 and VLA-5 with fibronectin or VLA-6 with laminin. , 1990, Journal of immunology.

[16]  D. Taylor,et al.  Correlated distribution of actin, myosin, and microtubules at the leading edge of migrating Swiss 3T3 fibroblasts. , 1989, Cell motility and the cytoskeleton.

[17]  David A. Williams,et al.  Optimization of fibronectin-assisted retroviral gene transfer into human CD34+ hematopoietic cells. , 1997, Human gene therapy.

[18]  T. Schall,et al.  Chemokine Class Differences in Binding to the Duffy Antigen-Erythrocyte Chemokine Receptor (*) , 1995, The Journal of Biological Chemistry.

[19]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[20]  H. Petty,et al.  Cellular memory: neutrophil orientation reverses during temporally decreasing chemoattractant concentrations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Adams,et al.  Proteoglycans on endothelial cells present adhesion-inducing cytokines to leukocytes. , 1993, Immunology today.

[22]  R. Bronson,et al.  Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. G. Vicker.  Gradient and temporal signal perception in chemotaxis. , 1989, Journal of cell science.

[24]  L. Visai,et al.  Heparin‐binding domain of human fibronectin binds HIV‐1 gp120/160 and reduces virus infectivity , 1998, Journal of medical virology.

[25]  R. Alon,et al.  TNF-alpha binds to the N-terminal domain of fibronectin and augments the beta 1-integrin-mediated adhesion of CD4+ T lymphocytes to the glycoprotein. , 1994, Journal of immunology.

[26]  V. Quaranta,et al.  Activation of the Integrin Involves a Discrete Cation-binding Site That Regulates Conformation (*) , 1996, The Journal of Biological Chemistry.

[27]  W. Gong,et al.  Chemically Synthesized SDF-1α Analogue, N33A, Is a Potent Chemotactic Agent for CXCR4/Fusin/LESTR-expressing Human Leukocytes* , 1997, The Journal of Biological Chemistry.

[28]  C. Martínez-A,et al.  The chemokine monocyte chemoattractant protein-1 induces functional responses through dimerization of its receptor CCR2. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Scadden,et al.  Active movement of T cells away from a chemokine , 2000, Nature Medicine.

[30]  E. Ohlstein,et al.  Chemokine Receptors in Human Endothelial Cells , 1998, The Journal of Biological Chemistry.

[31]  A. Lander,et al.  Differential binding of chemokines to glycosaminoglycan subpopulations , 1994, Current Biology.

[32]  Paul E. Kennedy,et al.  HIV-1 Entry Cofactor: Functional cDNA Cloning of a Seven-Transmembrane, G Protein-Coupled Receptor , 1996, Science.

[33]  Bernhard Moser,et al.  The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1 , 1996, Nature.

[34]  K. Campbell,et al.  Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. , 1998, Science.

[35]  Kouji Matsushima,et al.  The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract , 1998, Nature.

[36]  D. Lauffenburger,et al.  Gradient perception by neutrophil leucocytes, continued. , 1987, Journal of cell science.

[37]  R. Hershkoviz,et al.  Regulation of adhesion of CD4+ T lymphocytes to intact or heparinase-treated subendothelial extracellular matrix by diffusible or anchored RANTES and MIP-1 beta. , 1994, Journal of immunology.

[38]  B O Palsson,et al.  Effective intercellular communication distances are determined by the relative time constants for cyto/chemokine secretion and diffusion. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Baggiolini.  Chemokines and leukocyte traffic , 1998, Nature.

[40]  F. Sánchez‐Madrid,et al.  Cellular polarization induced by chemokines: a mechanism for leukocyte recruitment? , 1996, Immunology today.

[41]  B. Dewald,et al.  N-terminal Peptides of Stromal Cell-derived Factor-1 with CXC Chemokine Receptor 4 Agonist and Antagonist Activities* , 1998, The Journal of Biological Chemistry.

[42]  A. Lander,et al.  Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti- adhesive , 1991, The Journal of cell biology.