Semaphorins and their receptors in immune cell interactions

Semaphorins are newcomers to the growing panoply of immunoregulatory proteins. Members of this family were originally identified as proteins that provide axonal guidance cues during neuronal development. However, accumulating evidence indicates that several semaphorins, called 'immune semaphorins', are crucial to various phases of the immune response, from initiation to terminal inflammatory processes. Extensive studies of immune semaphorins have shown not only differences but also parallels in semaphorin functions among physiologically distinct systems, providing unexpected but meaningful insights into the biological activities of this protein family. Here we review the present knowledge of the function of semaphorins and their receptors in the immune system, including the most recent advances in this field.

[1]  M. Tessier-Lavigne,et al.  Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function , 2003, Nature.

[2]  D. Fearon,et al.  A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. , 1995, Science.

[3]  C. Tse,et al.  Human Semaphorin 3B (SEMA3B) located at chromosome 3p21.3 suppresses tumor formation in an adenocarcinoma cell line. , 2002, Cancer research.

[4]  G. Freeman,et al.  Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  H. Niiro,et al.  Decision making in the immune system: Regulation of B-cell fate by antigen-receptor signals , 2002, Nature Reviews Immunology.

[6]  Kazuhiro Suzuki,et al.  Requirement for the Lymphocyte Semaphorin, CD100, in the Induction of Antigen-Specific T Cells and the Maturation of Dendritic Cells1 , 2002, The Journal of Immunology.

[7]  T. Kurosaki Regulation of B cell fates by BCR signaling components. , 2002, Current opinion in immunology.

[8]  P. Circosta,et al.  CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes. , 2003, Blood.

[9]  N. Baumgarth,et al.  CD72-deficient mice reveal nonredundant roles of CD72 in B cell development and activation. , 1999, Immunity.

[10]  T. Pawson,et al.  The B-cell transmembrane protein CD72 binds to and is an in vivo substrate of the protein tyrosine phosphatase SHP-1 , 1998, Current Biology.

[11]  C. Tse,et al.  Semaphorin 3F gene from human 3p21.3 suppresses tumor formation in nude mice. , 2002, Cancer research.

[12]  J. Minna,et al.  Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Elhabazi,et al.  CD100 is a leukocyte semaphorin , 1998, Cellular and Molecular Life Sciences CMLS.

[14]  Jeffrey A. Golden,et al.  Semaphorin III is needed for normal patterning and growth of nerves, bones and heart , 1996, Nature.

[15]  Kazuhiro Suzuki,et al.  Involvement of CD100, a lymphocyte semaphorin, in the activation of the human immune system via CD72: implications for the regulation of immune and inflammatory responses. , 2003, International immunology.

[16]  K. Siminovitch,et al.  The SH2 Domain Containing Tyrosine Phosphatase-1 Down-regulates Activation of Lyn and Lyn-induced Tyrosine Phosphorylation of the CD19 Receptor in B Cells* , 2001, The Journal of Biological Chemistry.

[17]  S. Akira,et al.  Nonredundant roles of Sema4A in the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. , 2005, Immunity.

[18]  T. Walzer,et al.  Plexin C1 Engagement on Mouse Dendritic Cells by Viral Semaphorin A39R Induces Actin Cytoskeleton Rearrangement and Inhibits Integrin-Mediated Adhesion and Chemokine-Induced Migration , 2005, The Journal of Immunology.

[19]  Kazuhiro Suzuki,et al.  Immune semaphorins: increasing members and their diverse roles. , 2007, Advances in immunology.

[20]  A. Ebens,et al.  Human Semaphorin K1 Is Glycosylphosphatidylinositol-linked and Defines a New Subfamily of Viral-related Semaphorins* , 1998, The Journal of Biological Chemistry.

[21]  A. Fosberry,et al.  Sema7A is a Potent Monocyte Stimulator , 2002, Scandinavian journal of immunology.

[22]  D. Billadeau,et al.  Regulation of T-cell activation by the cytoskeleton , 2007, Nature Reviews Immunology.

[23]  丸川 聡子 Class IV semaphorin Sema4A enhances T-cell activation and interacts with Tim-2 , 2005 .

[24]  W. Fanslow,et al.  CD 40 Expression by Human Monocytes : Regulation by Cytokines and Activation of Monocytes by the Ligand for CD 40 , 2003 .

[25]  D. Dudley,et al.  The immune system in health and disease. , 1992, Bailliere's clinical obstetrics and gynaecology.

[26]  Richard O Hynes,et al.  Integrins Bidirectional, Allosteric Signaling Machines , 2002, Cell.

[27]  K. Shirouzu,et al.  CDw108 expression during T-cell development. , 2000, Tissue antigens.

[28]  H. Katoh,et al.  The Semaphorin 4D Receptor Plexin-B1 Is a GTPase Activating Protein for R-Ras , 2004, Science.

[29]  A. Kolodkin,et al.  Semaphorin 7A initiates T-cell-mediated inflammatory responses through α1β1 integrin , 2007, Nature.

[30]  Bernd Fritzsch,et al.  Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. , 2003, Developmental cell.

[31]  Laurie H Glimcher,et al.  A Novel Transcription Factor, T-bet, Directs Th1 Lineage Commitment , 2000, Cell.

[32]  L. Boumsell,et al.  Increased surface expression of a newly identified 150-kDa dimer early after human T lymphocyte activation. , 1992, Journal of immunology.

[33]  K. Sugamura,et al.  Molecular cloning of a glycosylphosphatidylinositol-anchored molecule CDw108. , 1999, Journal of immunology.

[34]  Thomas M. Jessell,et al.  Semaphorin 3E and Plexin-D1 Control Vascular Pattern Independently of Neuropilins , 2005, Science.

[35]  J. Cyster,et al.  Germinal-center organization and cellular dynamics. , 2007, Immunity.

[36]  M. Hemler VLA proteins in the integrin family: structures, functions, and their role on leukocytes. , 1990, Annual review of immunology.

[37]  M. Hori,et al.  Dual roles of Sema6D in cardiac morphogenesis through region-specific association of its receptor, Plexin-A1, with off-track and vascular endothelial growth factor receptor type 2. , 2004, Genes & development.

[38]  S. Ben-Horin,et al.  The role of very late antigen-1 in immune-mediated inflammation. , 2004, Clinical immunology.

[39]  R. Kalb,et al.  Plexin-Neuropilin-1 Complexes Form Functional Semaphorin-3A Receptors , 1999, Cell.

[40]  M. Spriggs,et al.  Shared resources between the neural and immune systems: semaphorins join the ranks. , 1999, Current opinion in immunology.

[41]  J. Mora,et al.  In vivo imaging of leukocyte trafficking in blood vessels and tissues. , 2004, Current opinion in immunology.

[42]  J. Epstein,et al.  PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. , 2004, Developmental cell.

[43]  M. Faronato,et al.  Semaphorin-3A is expressed by tumor cells and alters T-cell signal transduction and function. , 2006, Blood.

[44]  R. Homer,et al.  Semaphorin 7A plays a critical role in TGF-β1–induced pulmonary fibrosis , 2007, The Journal of experimental medicine.

[45]  M. Colonna TREMs in the immune system and beyond , 2003, Nature Reviews Immunology.

[46]  M. Tamura,et al.  Requirement for CD100-CD72 interactions in fine-tuning of B-cell antigen receptor signaling and homeostatic maintenance of the B-cell compartment. , 2005, International immunology.

[47]  C. Janeway Immunobiology: The Immune System in Health and Disease , 1996 .

[48]  J. Christensen,et al.  Expression and Functional Importance of Collagen-Binding Integrins, α1β1 and α2β1, on Virus-Activated T Cells 1 , 2003, The Journal of Immunology.

[49]  L. Lanier,et al.  The ITAM-bearing transmembrane adaptor DAP12 in lymphoid and myeloid cell function. , 2000, Immunology today.

[50]  J. Bonventre,et al.  T Cell, Ig Domain, Mucin Domain-2 Gene-Deficient Mice Reveal a Novel Mechanism for the Regulation of Th2 Immune Responses and Airway Inflammation1 , 2006, The Journal of Immunology.

[51]  M. Hori,et al.  Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling , 2004, Nature Cell Biology.

[52]  M. Reth,et al.  SHP-1 Requires Inhibitory Co-receptors to Down-modulate B Cell Antigen Receptor-mediated Phosphorylation of Cellular Substrates* , 2001, The Journal of Biological Chemistry.

[53]  石田 勲 Involvement of CD100, a lymphocyte semaphorin, in the activation of the human immune system via CD72 : Implications for the regulation of immune and inflammatory responses , 2004 .

[54]  L. Fetler,et al.  Requirement of Rac1 and Rac2 Expression by Mature Dendritic Cells for T Cell Priming , 2004, Science.

[55]  M. Poo,et al.  Plexins Are a Large Family of Receptors for Transmembrane, Secreted, and GPI-Anchored Semaphorins in Vertebrates , 1999, Cell.

[56]  Michael L. Dustin,et al.  Dynamic imaging of the immune system: progress, pitfalls and promise , 2006, Nature Reviews Immunology.

[57]  R. Medzhitov,et al.  Semaphorin 7A is a negative regulator of T cell responses. , 2006, Immunity.

[58]  S. Akira,et al.  Plexin-A1 and its interaction with DAP12 in immune responses and bone homeostasis , 2006, Nature Cell Biology.

[59]  C. Goodman,et al.  The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules , 1993, Cell.

[60]  M. Tessier-Lavigne,et al.  Neuropilin Is a Receptor for the Axonal Chemorepellent Semaphorin III , 1997, Cell.

[61]  A. Kolodkin,et al.  Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. , 2007, Nature.

[62]  A. Barzilai,et al.  Immunosuppressive role of semaphorin‐3A on T cell proliferation is mediated by inhibition of actin cytoskeleton reorganization , 2006, European journal of immunology.

[63]  A. Kolodkin,et al.  Semaphorin junction: making tracks toward neural connectivity , 2003, Current Opinion in Neurobiology.

[64]  V. Kuchroo,et al.  TIM family of genes in immunity and tolerance. , 2006, Advances in immunology.

[65]  A. Miller,et al.  CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. , 1996, Immunity.

[66]  Alex L Kolodkin,et al.  Neuropilin Is a Semaphorin III Receptor , 1997, Cell.

[67]  A. Wong,et al.  CIITA-regulated plexin-A1 affects T-cell–dendritic cell interactions , 2003, Nature Immunology.

[68]  W. Fanslow,et al.  CD40 expression by human monocytes: regulation by cytokines and activation of monocytes by the ligand for CD40 , 1993, The Journal of experimental medicine.

[69]  A. Elhabazi,et al.  Biological Activity of Soluble CD100. II. Soluble CD100, Similarly to H-SemaIII, Inhibits Immune Cell Migration1 2 , 2001, The Journal of Immunology.

[70]  Miguel Vicente-Manzanares,et al.  Role of the cytoskeleton during leukocyte responses , 2004, Nature Reviews Immunology.

[71]  M. Matsumoto,et al.  Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. , 2000, Immunity.

[72]  M. Neuberger,et al.  Hyperresponsive B Cells in CD22-Deficient Mice , 1996, Science.

[73]  R. Pasterkamp,et al.  Soluble CD100 functions on human monocytes and immature dendritic cells require plexin C1 and plexin B1, respectively. , 2005, International immunology.

[74]  J. Minna,et al.  Human semaphorins A(V) and IV reside in the 3p21.3 small cell lung cancer deletion region and demonstrate distinct expression patterns. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  M. Okabe,et al.  Enhanced Immune Responses in Transgenic Mice Expressing a Truncated Form of the Lymphocyte Semaphorin CD1001 , 2001, The Journal of Immunology.

[76]  K. Guan,et al.  Semaphorins command cells to move , 2005, Nature Reviews Molecular Cell Biology.

[77]  M. Cybulsky,et al.  Getting to the site of inflammation: the leukocyte adhesion cascade updated , 2007, Nature Reviews Immunology.

[78]  M. Reth,et al.  The B cell surface protein CD72 recruits the tyrosine phosphatase SHP-1 upon tyrosine phosphorylation. , 1998, Journal of immunology.

[79]  M. Ikawa,et al.  The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. , 2000, Immunity.

[80]  Jacques J. Peschon,et al.  Semaphorin 7A promotes axon outgrowth through integrins and MAPKs , 2003, Nature.

[81]  M. Poo,et al.  Unified Nomenclature for the Semaphorins/Collapsins , 1999, Cell.

[82]  R. Dubose,et al.  A poxvirus-encoded semaphorin induces cytokine production from monocytes and binds to a novel cellular semaphorin receptor, VESPR. , 1998, Immunity.

[83]  S. Offermanns,et al.  Plexin-B1 Directly Interacts with PDZ-RhoGEF/LARG to Regulate RhoA and Growth Cone Morphology , 2002, Neuron.

[84]  P. Doherty,et al.  The Collagen Binding α1β1 Integrin VLA-1 Regulates CD8 T Cell-Mediated Immune Protection against Heterologous Influenza Infection , 2004 .

[85]  Junko Kamei,et al.  Semaphorin‐4A, an activator for T‐cell‐mediated immunity, suppresses angiogenesis via Plexin‐D1 , 2007, The EMBO journal.

[86]  V. Kuchroo,et al.  Tim-2 regulates T helper type 2 responses and autoimmunity , 2005, The Journal of experimental medicine.

[87]  B. Neel,et al.  From Form to Function: Signaling by Protein Tyrosine Phosphatases , 1996, Cell.