From the ECM to the Cytoskeleton and Back: How Integrins Orchestrate T Cell Action

T lymphocytes constitute a highly dynamic tissue type. During the course of their lives, they travel through a variety of physiological environments and experience a multitude of interactions with extracellular matrix components and other cells. In order to do this, they must receive many environmental cues, and translate these signals into the appropriate biological actions. Particularly dramatic are the cytoskeletal shape changes a T cell must undergo during the processes of leaving the bloodstream, migrating through tissues, and encountering antigen. In this review, we highlight the role of integrins in providing a link between the extracellular environment and cytoskeletal regulation and how these receptors help to orchestrate T cell migration and antigen recognition.

[1]  Ch'en Yl,et al.  [Focal adhesion kinase]. , 1999, Sheng li ke xue jin zhan [Progress in physiology].

[2]  Y. Shimizu,et al.  Stimulation of beta1-integrin function by epidermal growth factor and heregulin-beta has distinct requirements for erbB2 but a similar dependence on phosphoinositide 3-OH kinase. , 1999, Molecular biology of the cell.

[3]  J. Seavitt,et al.  Regulation of integrin-mediated T cell adhesion by the transmembrane protein tyrosine phosphatase CD45. , 1999, Journal of immunology.

[4]  F. Sánchez‐Madrid,et al.  Cytoskeletal rearrangement during migration and activation of T lymphocytes. , 1999, Trends in cell biology.

[5]  M. Crow,et al.  A Molecular Mechanism of Integrin Crosstalk: αvβ3 Suppression of Calcium/Calmodulin-dependent Protein Kinase II Regulates α5β1 Function , 1999, The Journal of cell biology.

[6]  N. Hogg,et al.  Lymphocyte Migration in Lymphocyte Function-associated Antigen (LFA)-1–deficient Mice , 1999, The Journal of experimental medicine.

[7]  R. Pardi,et al.  Anchorage dependence of mitogen-induced G1 to S transition in primary T lymphocytes. , 1999, Journal of Immunology.

[8]  C. Abraham,et al.  The dependence for leukocyte function-associated antigen-1/ICAM-1 interactions in T cell activation cannot be overcome by expression of high density TCR ligand. , 1999, Journal of immunology.

[9]  D. Schlaepfer,et al.  Signaling through focal adhesion kinase. , 1999, Progress in biophysics and molecular biology.

[10]  J. Bonnet,et al.  IL-2-dependent expression of genes involved in cytoskeleton organization, oncogene regulation, and transcriptional control. , 1999, Journal of immunology.

[11]  S. Zigmond,et al.  Actin polymerization: Where the WASP stings , 1999, Current Biology.

[12]  T. Mak,et al.  Genetic evidence for functional redundancy of Platelet/Endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. , 1999, Journal of immunology.

[13]  J. Miller,et al.  TCR, LFA-1, and CD28 play unique and complementary roles in signaling T cell cytoskeletal reorganization. , 1999, Journal of immunology.

[14]  L. Williams,et al.  Mice Lacking Expression of Secondary Lymphoid Organ Chemokine Have Defects in Lymphocyte Homing and Dendritic Cell Localization , 1999, The Journal of experimental medicine.

[15]  T. Harder,et al.  Clusters of glycolipid and glycosylphosphatidylinositol‐anchored proteins in lymphoid cells : accumulation of actin regulated by local tyrosine phosphorylation , 1999, European journal of immunology.

[16]  A. Lanzavecchia,et al.  T lymphocyte costimulation mediated by reorganization of membrane microdomains. , 1999, Science.

[17]  M. Hemler,et al.  Interaction of the Integrin β1 Cytoplasmic Domain with ICAP-1 Protein* , 1999, The Journal of Biological Chemistry.

[18]  H. Broxmeyer,et al.  Chemokines: signal lamps for trafficking of T and B cells for development and effector function , 1999, Journal of leukocyte biology.

[19]  M. Miceli,et al.  Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. , 1998, Immunity.

[20]  J. Cambier,et al.  pp56Lck mediates TCR zeta-chain binding to the microfilament cytoskeleton. , 1998, Journal of immunology.

[21]  J. Cambier,et al.  pp56Lck Mediates TCR ζ-Chain Binding to the Microfilament Cytoskeleton , 1998, The Journal of Immunology.

[22]  E. Butcher,et al.  Evidence of ζ Protein Kinase C Involvement in Polymorphonuclear Neutrophil Integrin-dependent Adhesion and Chemotaxis* , 1998, The Journal of Biological Chemistry.

[23]  H. Stockinger,et al.  Polyunsaturated Fatty Acids Inhibit T Cell Signal Transduction by Modification of Detergent-insoluble Membrane Domains , 1998, The Journal of cell biology.

[24]  B. Mayer,et al.  Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. , 1998, Immunity.

[25]  J. Mendelsohn,et al.  Heregulin Regulates Cytoskeletal Reorganization and Cell Migration through the p21-activated Kinase-1 via Phosphatidylinositol-3 Kinase* , 1998, The Journal of Biological Chemistry.

[26]  N. Hogg,et al.  Integrins take partners: cross-talk between integrins and other membrane receptors. , 1998, Trends in cell biology.

[27]  T. Roach,et al.  The protein tyrosine phosphatase SHP-1 regulates integrin-mediated adhesion of macrophages , 1998, Current Biology.

[28]  Patricia L. Widder,et al.  A Novel Adaptor Protein Orchestrates Receptor Patterning and Cytoskeletal Polarity in T-Cell Contacts , 1998, Cell.

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

[30]  A. Ariel,et al.  IL-2 induces T cell adherence to extracellular matrix: inhibition of adherence and migration by IL-2 peptides generated by leukocyte elastase. , 1998, Journal of immunology.

[31]  B. Bierer,et al.  Identification of a Proline-Rich Sequence in the CD2 Cytoplasmic Domain Critical for Regulation of Integrin-Mediated Adhesion and Activation of Phosphoinositide 3-Kinase , 1998, Molecular and Cellular Biology.

[32]  L. Samelson,et al.  LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. , 1998, Immunity.

[33]  F. Ross,et al.  A Role for the αvβ3 Integrin in the Transmigration of Monocytes , 1998, The Journal of cell biology.

[34]  D. Cantrell Lymphocyte signalling: A coordinating role for Vav? , 1998, Current Biology.

[35]  J. Westwick,et al.  Chemokines and T lymphocytes: more than an attraction. , 1998, Immunity.

[36]  L. Van Aelst,et al.  Rac Regulates Integrin-Mediated Spreading and Increased Adhesion of T Lymphocytes , 1998, Molecular and Cellular Biology.

[37]  F. Sánchez‐Madrid,et al.  CD43 interacts with moesin and ezrin and regulates its redistribution to the uropods of T lymphocytes at the cell-cell contacts. , 1998, Blood.

[38]  W. Kolanus,et al.  Phosphoinositide 3-OH Kinase Activates the β2Integrin Adhesion Pathway and Induces Membrane Recruitment of Cytohesin-1* , 1998, The Journal of Biological Chemistry.

[39]  Kenneth M. Yamada,et al.  Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. , 1998, Science.

[40]  R. Xavier,et al.  Membrane compartmentation is required for efficient T cell activation. , 1998, Immunity.

[41]  A. Trautmann,et al.  Involvement of phosphoinositide 3‐kinase and Rac in membrane ruffling induced by IL‐2 in T cells , 1998, European journal of immunology.

[42]  M. Baggiolini,et al.  The chemokine SLC is expressed in T cell areas of lymph nodes and mucosal lymphoid tissues and attracts activated T cells via CCR7 , 1998, European journal of immunology.

[43]  F. Alt,et al.  Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction , 1998, Current Biology.

[44]  K. Tedford,et al.  Vav is a regulator of cytoskeletal reorganization mediated by the T-cell receptor , 1998, Current Biology.

[45]  K. Rogers,et al.  Activation of p21-CDC42/Rac-activated kinases by CD28 signaling: p21-activated kinase (PAK) and MEK kinase 1 (MEKK1) may mediate the interplay between CD3 and CD28 signals. , 1998, Journal of immunology.

[46]  G. Bokoch,et al.  Two Signaling Mechanisms for Activation of αMβ2 Avidity in Polymorphonuclear Neutrophils* , 1998, The Journal of Biological Chemistry.

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

[48]  D. Cantrell,et al.  Networking Rho family GTPases in lymphocytes. , 1998, Immunity.

[49]  K. Vuori,et al.  CAS/Crk Coupling Serves as a “Molecular Switch” for Induction of Cell Migration , 1998, The Journal of cell biology.

[50]  A. Weiss,et al.  Cytoskeletal Polarization of T Cells Is Regulated by an Immunoreceptor Tyrosine-based Activation Motif–dependent Mechanism , 1998, The Journal of cell biology.

[51]  A. Hall,et al.  Rho GTPases and the actin cytoskeleton. , 1998, Science.

[52]  E. Butcher,et al.  Chemokines and the arrest of lymphocytes rolling under flow conditions. , 1998, Science.

[53]  S. Hanks,et al.  Identification of p130Cas as a Mediator of Focal Adhesion Kinase–promoted Cell Migration , 1998, The Journal of cell biology.

[54]  J. Cyster,et al.  A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  K. Rogers,et al.  Stimulation of CD28 with B7-2 promotes focal adhesion-like cell contacts where Rho family small G proteins accumulate in T cells. , 1998, Journal of immunology.

[56]  Leslie M Shaw,et al.  Activation of Phosphoinositide 3-OH Kinase by the α6β4 Integrin Promotes Carcinoma Invasion , 1997, Cell.

[57]  Y. Shimizu,et al.  Alpha 4 beta 1 integrin-mediated tyrosine phosphorylation in human T cells: characterization of Crk- and Fyn-associated substrates (pp105, pp115, and human enhancer of filamentation-1) and integrin-dependent activation of p59fyn1. , 1997, Journal of immunology.

[58]  B. Groner,et al.  Phosphatidylinositol 3-kinase couples the interleukin-2 receptor to the cell cycle regulator E2F. , 1997, Immunity.

[59]  M. Auer,et al.  Transcytosis and Surface Presentation of IL-8 by Venular Endothelial Cells , 1997, Cell.

[60]  J. Guan,et al.  Focal adhesion kinase in integrin signaling. , 1997, Matrix biology : journal of the International Society for Matrix Biology.

[61]  F. Giancotti,et al.  Integrin signaling: specificity and control of cell survival and cell cycle progression. , 1997, Current opinion in cell biology.

[62]  S. Rosen,et al.  Ligation of L-selectin on T lymphocytes activates beta1 integrins and promotes adhesion to fibronectin. , 1997, Journal of immunology.

[63]  N. Hogg,et al.  Integrin Cross Talk: Activation of Lymphocyte Function-associated Antigen-1 on Human T Cells Alters α4β1- and α5β1-mediated Function , 1997, The Journal of cell biology.

[64]  D. Chang,et al.  ICAP-1, a Novel β1 Integrin Cytoplasmic Domain–associated Protein, Binds to a Conserved and Functionally Important NPXY Sequence Motif of β1 Integrin , 1997, The Journal of cell biology.

[65]  M. Sheetz,et al.  Ligation of L-selectin through conserved regions within the lectin domain activates signal transduction pathways and integrin function in human, mouse, and rat leukocytes. , 1997, Journal of immunology.

[66]  G. Fields,et al.  CD7-mediated regulation of integrin adhesiveness on human T cells involves tyrosine phosphorylation-dependent activation of phosphatidylinositol 3-kinase. , 1997, Journal of immunology.

[67]  R. Hynes,et al.  Targeted Mutations in Integrins and their Ligands: Their Implications for Vascular Biology , 1997, Thrombosis and Haemostasis.

[68]  J. Madrenas,et al.  Generation of dendritic cell‐like antigen‐presenting cells in long‐term mixed leucocyte culture: phenotypic and functional studies , 1997, Immunology.

[69]  A. Ager,et al.  Regulation of lymphocyte migration into lymph nodes by high endothelial venules. , 1997, Biochemical Society transactions.

[70]  David A. Cheresh,et al.  Regulation of Cell Motility by Mitogen-activated Protein Kinase , 1997, The Journal of cell biology.

[71]  D A Peterson,et al.  Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[72]  C. Martínez-A,et al.  Intermediate Affinity Interleukin-2 Receptor Mediates Survival via a Phosphatidylinositol 3-Kinase-dependent Pathway* , 1997, The Journal of Biological Chemistry.

[73]  G. Bokoch,et al.  Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells , 1997, Current Biology.

[74]  M. Schwartz,et al.  Suppression of Integrin Activation: A Novel Function of a Ras/Raf-Initiated MAP Kinase Pathway , 1997, Cell.

[75]  Wei Wang,et al.  A new class of membrane-bound chemokine with a CX3C motif , 1997, Nature.

[76]  R. Hynes Targeted mutations in cell adhesion genes: what have we learned from them? , 1996, Developmental biology.

[77]  Y. Shimizu,et al.  Regulating integrin-mediated adhesion: one more function for PI 3-kinase? , 1996, Immunology today.

[78]  T. Ogata,et al.  Follicular dendritic cells adhere to fibronectin and laminin fibers via their respective receptors. , 1996, Blood.

[79]  S. Simon,et al.  GlyCAM-1, a physiologic ligand for L-selectin, activates beta 2 integrins on naive peripheral lymphocytes , 1996, The Journal of experimental medicine.

[80]  S. Iwata,et al.  Structure and function of Cas-L, a 105-kD Crk-associated substrate- related protein that is involved in beta 1 integrin-mediated signaling in lymphocytes , 1996, The Journal of experimental medicine.

[81]  T. Udagawa,et al.  Alpha 4 beta 1 (CD49d/CD29) integrin costimulation of human T cells enhances transcription factor and cytokine induction in the absence of altered sensitivity to anti-CD3 stimulation. , 1996, Journal of immunology.

[82]  B. Seed,et al.  αLβ2 Integrin/LFA-1 Binding to ICAM-1 Induced by Cytohesin-1, a Cytoplasmic Regulatory Molecule , 1996, Cell.

[83]  G. Bokoch,et al.  Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic. , 1996, Journal of immunology.

[84]  J. Guan,et al.  Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. , 1996, Journal of cell science.

[85]  W. Stetler-Stevenson,et al.  Localization of Matrix Metalloproteinase MMP-2 to the Surface of Invasive Cells by Interaction with Integrin αvβ3 , 1996, Cell.

[86]  R. Herrera,et al.  Adhesion through the Interaction of Lymphocyte Function-associated Antigen-1 with Intracellular Adhesion Molecule-1 Induces Tyrosine Phosphorylation of p130 and Its Association with c-CrkII (*) , 1996, The Journal of Biological Chemistry.

[87]  N. Hogg,et al.  T cell adhesion to intercellular adhesion molecule-1 (ICAM-1) is controlled by cell spreading and the activation of integrin LFA-1. , 1996, Journal of immunology.

[88]  E. Butcher,et al.  Role of Rho in Chemoattractant-Activated Leukocyte Adhesion Through Integrins , 1996, Science.

[89]  T. Springer,et al.  The C–C Chemokine MCP-1 Differentially Modulates the Avidity of β1 and β2 Integrins on T Lymphocytes , 1996 .

[90]  T. Zell,et al.  CD28-mediated up-regulation of beta 1-integrin adhesion involves phosphatidylinositol 3-kinase. , 1996, Journal of immunology.

[91]  S. Dedhar,et al.  Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase , 1996, Nature.

[92]  B. Wolff,et al.  Some aspects of IL‐8 pathophysiology III: chemokine interaction with endothelial cells , 1996, Journal of leukocyte biology.

[93]  Y. Shimizu,et al.  A role for phosphatidylinositol 3-kinase in the regulation of beta 1 integrin activity by the CD2 antigen , 1995, The Journal of cell biology.

[94]  S. Hanks,et al.  T cell receptor- and beta 1 integrin-mediated signals synergize to induce tyrosine phosphorylation of focal adhesion kinase (pp125FAK) in human T cells , 1995, The Journal of experimental medicine.

[95]  B. Malissen,et al.  Tyrosine-phosphorylated T cell receptor zeta chain associates with the actin cytoskeleton upon activation of mature T lymphocytes. , 1995, Immunity.

[96]  S. Aizawa,et al.  Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice , 1995, Nature.

[97]  E. Butcher,et al.  Distinct roles of L-selectin and integrins α4β7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: The multistep model confirmed and refined , 1995 .

[98]  Z. Werb,et al.  Cooperative signaling by alpha 5 beta 1 and alpha 4 beta 1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin , 1995, The Journal of cell biology.

[99]  J. Brugge,et al.  Integrins and signal transduction pathways: the road taken. , 1995, Science.

[100]  R. Brezinschek,et al.  Phenotypic characterization of CD4+ T cells that exhibit a transendothelial migratory capacity. , 1995, Journal of immunology.

[101]  E. Berg,et al.  Rolling of lymphocytes and neutrophils on peripheral node addressin and subsequent arrest on ICAM‐1 in shear flow , 1995, European journal of immunology.

[102]  T. Springer,et al.  The integrin VLA-4 supports tethering and rolling in flow on VCAM-1 , 1995, The Journal of cell biology.

[103]  C. Morimoto,et al.  Focal Adhesion Kinase (pp125FAK) Is Tyrosine Phosphorylated after Engagement of α4β1 and α5β1 Integrins on Human T-Lymphoblastic Cells , 1995 .

[104]  E. Berg,et al.  α4 integrins mediate lymphocyte attachment and rolling under physiologic flow , 1995, Cell.

[105]  T. Springer,et al.  Distinct cell surface ligands mediate T lymphocyte attachment and rolling on P and E selectin under physiological flow , 1994, The Journal of cell biology.

[106]  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.

[107]  E. Brown,et al.  Integrin alpha v beta 3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor alpha 5 beta 1 , 1994, The Journal of cell biology.

[108]  E. Butcher,et al.  L-selectin and very late antigen-4 integrin promote eosinophil rolling at physiological shear rates in vivo. , 1994, Journal of immunology.

[109]  Timothy A. Springer,et al.  The dynamic regulation of integrin adhesiveness , 1994, Current Biology.

[110]  A. M. Romanic,et al.  The induction of 72-kD gelatinase in T cells upon adhesion to endothelial cells is VCAM-1 dependent , 1994, The Journal of cell biology.

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

[112]  E. Berg,et al.  α4β7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1 , 1993, Cell.

[113]  E. Butcher,et al.  Rapid G protein-regulated activation event involved in lymphocyte binding to high endothelial venules , 1993, The Journal of experimental medicine.

[114]  D. Adams,et al.  T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-lβ , 1993, Nature.

[115]  S. Albelda,et al.  Platelet endothelial cell adhesion molecule, PECAM‐1, modulates cell migration , 1992, Journal of cellular physiology.

[116]  Simon C Watkins,et al.  Association of murine CD31 with transmigrating lymphocytes following antigenic stimulation. , 1992, The American journal of pathology.

[117]  Y. Tanaka,et al.  CD31 expressed on distinctive T cell subsets is a preferential amplifier of beta 1 integrin-mediated adhesion , 1992, The Journal of experimental medicine.

[118]  K. Horgan,et al.  Crosslinking of the T cell-specific accessory molecules CD7 and CD28 modulates T cell adhesion , 1992, The Journal of experimental medicine.

[119]  E. Butcher Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity , 1991, Cell.

[120]  D. T. Bogue,et al.  Differential utilization of ICAM-1 and VCAM-1 during the adhesion and transendothelial migration of human T lymphocytes. , 1991, Journal of immunology.

[121]  T. Springer,et al.  Regulation of adhesion of ICAM-1 by the cytoplasmic domain of LFA-1 integrin beta subunit. , 1991, Science.

[122]  L. Davis,et al.  Human T lymphocyte adhesion to endothelial cells and transendothelial migration. Alteration of receptor use relates to the activation status of both the T cell and the endothelial cell. , 1990, Journal of immunology.

[123]  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.

[124]  K. Horgan,et al.  The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. , 1990, Journal of immunology.

[125]  K. Horgan,et al.  Regulated expression and binding of three VLA (β1) integrin receptors on T cells , 1990, Nature.

[126]  C. Figdor,et al.  Enhancement of LFA-1-mediated cell adhesion by triggering through CD2 or CD3 on T lymphocytes , 1989, Nature.

[127]  Michael L. Dustin,et al.  T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1 , 1989, Nature.

[128]  L. Daniel,et al.  Evidence of protein kinase C involvement in phorbol diester-stimulated arachidonic acid release and prostaglandin synthesis. , 1987, The Journal of biological chemistry.

[129]  T. Springer,et al.  Two antigen-independent adhesion pathways used by human cytotoxic T-cell clones , 1986, Nature.

[130]  Z. Werb,et al.  Cooperative Signaling by and a4/ l Integrins Regulates Metalloproteinase Gene Expression in Fibroblasts Adhering to Fibronectin , 2002 .

[131]  E. Butcher,et al.  Lymphocyte trafficking and regional immunity. , 1999, Advances in immunology.

[132]  M. Ginsberg,et al.  Integrins in the immune system. , 1999, Advances in immunology.

[133]  J. Bonnet,et al.  IL-2-Dependent Expression of Genes Involved , 1999 .

[134]  G. Bazzoni,et al.  Are changes in integrin affinity and conformation overemphasized? , 1998, Trends in biochemical sciences.

[135]  E. Kaldjian,et al.  Orchestrated information transfer underlying leukocyte endothelial interactions. , 1996, Annual review of immunology.

[136]  R. Hershkoviz,et al.  Interplay of T cells and cytokines in the context of enzymatically modified extracellular matrix. , 1996, Immunology today.

[137]  尾形 隆 Follicular dendritic cells adhere to fibronectin and laminin fibers via their respective receptors , 1996 .

[138]  T. Springer,et al.  The C-C chemokine MCP-1 differentially modulates the avidity of beta 1 and beta 2 integrins on T lymphocytes. , 1996, Immunity.

[139]  R. Hershkoviz,et al.  Interactions of migrating T lymphocytes, inflammatory mediators, and the extracellular matrix. , 1995, Critical reviews in immunology.

[140]  T. Springer,et al.  Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. , 1995, Annual review of physiology.

[141]  M. Schwartz,et al.  Integrins: emerging paradigms of signal transduction. , 1995, Annual review of cell and developmental biology.

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

[143]  A. Fischer T cell adhesion. , 1990, Nouvelle revue francaise d'hematologie.

[144]  J. Hay,et al.  Lymphocyte migration. , 1986, Immunology today.