Astrocyte-Secreted Matricellular Proteins in CNS Remodelling during Development and Disease

Matricellular proteins are secreted, nonstructural proteins that regulate the extracellular matrix (ECM) and interactions between cells through modulation of growth factor signaling, cell adhesion, migration, and proliferation. Despite being well described in the context of nonneuronal tissues, recent studies have revealed that these molecules may also play instrumental roles in central nervous system (CNS) development and diseases. In this minireview, we discuss the matricellular protein families SPARC (secreted protein acidic and rich in cysteine), Hevin/SC1 (SPARC-like 1), TN-C (Tenascin C), TSP (Thrombospondin), and CCN (CYR61/CTGF/NOV), which are secreted by astrocytes during development. These proteins exhibit a reduced expression in adult CNS but are upregulated in reactive astrocytes following injury or disease, where they are well placed to modulate the repair processes such as tissue remodeling, axon regeneration, glial scar formation, angiogenesis, and rewiring of neural circuitry. Conversely, their reexpression in reactive astrocytes may also lead to detrimental effects and promote the progression of neurodegenerative diseases.

[1]  N. J. Allen Role of glia in developmental synapse formation , 2013, Current Opinion in Neurobiology.

[2]  B. Penke,et al.  Tenascin-C deficiency ameliorates Alzheimer's disease-related pathology in mice , 2013, Neurobiology of Aging.

[3]  M. Kubista,et al.  Heterogeneity of Astrocytes: From Development to Injury – Single Cell Gene Expression , 2013, PloS one.

[4]  B. Song,et al.  Glial Scar Borders Are Formed by Newly Proliferated, Elongated Astrocytes That Interact to Corral Inflammatory and Fibrotic Cells via STAT3-Dependent Mechanisms after Spinal Cord Injury , 2013, The Journal of Neuroscience.

[5]  Ben A. Barres,et al.  Emerging roles of astrocytes in neural circuit development , 2013, Nature Reviews Neuroscience.

[6]  L. Tsai,et al.  Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [corrected]. , 2013, Cell stem cell.

[7]  Fabian J Theis,et al.  Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation , 2013, Nature Neuroscience.

[8]  E. York,et al.  SPARC Regulates Microgliosis and Functional Recovery following Cortical Ischemia , 2013, The Journal of Neuroscience.

[9]  J. Sweedler,et al.  Storage and Uptake of d-Serine into Astrocytic Synaptic-Like Vesicles Specify Gliotransmission , 2013, The Journal of Neuroscience.

[10]  Lesley S. Chaboub,et al.  Developmental Origins of Astrocyte Heterogeneity: The Final Frontier of CNS Development , 2012, Developmental Neuroscience.

[11]  Walter J Koroshetz,et al.  Plasma biomarkers associated with the apolipoprotein E genotype and Alzheimer disease. , 2012, Archives of neurology.

[12]  A. Volterra,et al.  TNFα in synaptic function: switching gears , 2012, Trends in Neurosciences.

[13]  G. Mazzucchelli,et al.  Sparc-like protein 1 is a new marker of human glioma progression. , 2012, Journal of proteome research.

[14]  O. Podhajcer,et al.  Hippocampal SPARC regulates depression‐related behavior , 2012, Genes, brain, and behavior.

[15]  Minh D. Tran,et al.  Trauma-induced expression of astrocytic thrombospondin-1 is regulated by P2 receptors coupled to protein kinase cascades , 2012, Neuroreport.

[16]  A. Roskams,et al.  SPARC‐like 1 (SC1) is a diversely expressed and developmentally regulated matricellular protein that does not compensate for the absence of SPARC in the CNS , 2012, The Journal of comparative neurology.

[17]  O. Steward,et al.  Thrombospondin-4 Contributes to Spinal Sensitization and Neuropathic Pain States , 2012, The Journal of Neuroscience.

[18]  S. Wiese,et al.  Astrocytes as a Source for Extracellular Matrix Molecules and Cytokines , 2012, Front. Pharmacol..

[19]  L. Schlichter,et al.  SC1/Hevin Identifies Early White Matter Injury After Ischemia and Intracerebral Hemorrhage in Young and Aged Rats , 2012, Journal of neuropathology and experimental neurology.

[20]  Stephen J. Smith,et al.  Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors , 2012, Nature.

[21]  J. Lawler,et al.  Molecular basis for the regulation of angiogenesis by thrombospondin-1 and -2. , 2012, Cold Spring Harbor perspectives in medicine.

[22]  E. Hol,et al.  Differential cell proliferation in the cortex of the appsweps1de9 alzheimer's disease mouse model , 2012, Glia.

[23]  C. Eroglu,et al.  Thrombospondins as key regulators of synaptogenesis in the central nervous system. , 2012, Matrix biology : journal of the International Society for Matrix Biology.

[24]  R. Iozzo,et al.  Thrombospondins in physiology and disease: new tricks for old dogs. , 2012, Matrix biology : journal of the International Society for Matrix Biology.

[25]  N. Frangogiannis Matricellular proteins in cardiac adaptation and disease. , 2012, Physiological reviews.

[26]  T. Owens,et al.  Microglia are required for astroglial toll‐like receptor 4 response and for optimal TLR2 and TLR3 response , 2012, Glia.

[27]  A. Bradshaw Diverse biological functions of the SPARC family of proteins. , 2012, The international journal of biochemistry & cell biology.

[28]  C. ffrench-Constant,et al.  The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification , 2011, Development.

[29]  Lester F. Lau,et al.  Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets , 2011, Nature Reviews Drug Discovery.

[30]  E. Sage,et al.  Proteolysis of the matricellular protein hevin by matrix metalloproteinase‐3 produces a SPARC‐like fragment (SLF) associated with neovasculature in a murine glioma model , 2011, Journal of cellular biochemistry.

[31]  Khaleel Bhaukaurally,et al.  Local Ca2+ detection and modulation of synaptic release by astrocytes , 2011, Nature Neuroscience.

[32]  Andrea Volterra,et al.  SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: A comparative analysis , 2011, Glia.

[33]  J. Lacaille,et al.  Astrocytes Are Endogenous Regulators of Basal Transmission at Central Synapses , 2011, Cell.

[34]  R. Vandenbroucke,et al.  Matrix metalloproteinases as drug targets in ischemia/reperfusion injury. , 2011, Drug discovery today.

[35]  R. Brekken,et al.  The regulatory function of SPARC in vascular biology , 2011, Cellular and Molecular Life Sciences.

[36]  E. Holland,et al.  Connective tissue growth factor and the parallels between brain injury and brain tumors. , 2011, Journal of the National Cancer Institute.

[37]  W. Poewe,et al.  Toll-like receptor 4 promotes α-synuclein clearance and survival of nigral dopaminergic neurons. , 2011, The American journal of pathology.

[38]  B. Barres,et al.  Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC , 2011, Proceedings of the National Academy of Sciences.

[39]  W. Bowers,et al.  Tumor Necrosis Factor-alpha and the Roles it Plays in Homeostatic and Degenerative Processes Within the Central Nervous System , 2011, Journal of Neuroimmune Pharmacology.

[40]  K. Murai,et al.  Astrocytes Control Glutamate Receptor Levels at Developing Synapses through SPARC–β-Integrin Interactions , 2011, The Journal of Neuroscience.

[41]  L. Kular,et al.  The CCN family: a new class of inflammation modulators? , 2011, Biochimie.

[42]  A. Planas,et al.  Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88‐dependent NFκB signaling, MAPK, and Jak1/Stat1 pathways , 2011, Glia.

[43]  Magdalena Götz,et al.  The stem cell potential of glia: lessons from reactive gliosis , 2011, Nature Reviews Neuroscience.

[44]  J. Busciglio,et al.  A Role for Thrombospondin-1 Deficits in Astrocyte-Mediated Spine and Synaptic Pathology in Down's Syndrome , 2010, PloS one.

[45]  J. Kipnis,et al.  Thrombospondin 1—a key astrocyte‐derived neurogenic factor , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[46]  E. Diamandis,et al.  Amniotic fluid proteome analysis from Down syndrome pregnancies for biomarker discovery. , 2010, Journal of proteome research.

[47]  S. Hattori,et al.  Type IV collagen induces expression of thrombospondin‐1 that is mediated by integrin α1β1 in astrocytes , 2010, Glia.

[48]  D. Attwell,et al.  Do astrocytes really exocytose neurotransmitters? , 2010, Nature Reviews Neuroscience.

[49]  W. Arap,et al.  Processing of the Matricellular Protein Hevin in Mouse Brain Is Dependent on ADAMTS4* , 2009, The Journal of Biological Chemistry.

[50]  M. Sofroniew,et al.  Astrocytes: biology and pathology , 2009, Acta Neuropathologica.

[51]  M. Sofroniew Molecular dissection of reactive astrogliosis and glial scar formation , 2009, Trends in Neurosciences.

[52]  S. Oliet,et al.  Long term potentiation depends on release of D-serine from astrocytes , 2009, Nature.

[53]  C. Eroglu The role of astrocyte-secreted matricellular proteins in central nervous system development and function , 2009, Journal of Cell Communication and Signaling.

[54]  Stephen J. Smith,et al.  Gabapentin Receptor α2δ-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis , 2009, Cell.

[55]  B. Song,et al.  Reactive Astrocytes Form Scar-Like Perivascular Barriers to Leukocytes during Adaptive Immune Inflammation of the CNS , 2009, The Journal of Neuroscience.

[56]  M. Kashiwagi,et al.  Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease , 2009, Nature Medicine.

[57]  J. Fawcett,et al.  α9 Integrin Promotes Neurite Outgrowth on Tenascin-C and Enhances Sensory Axon Regeneration , 2009, The Journal of Neuroscience.

[58]  E. Sage,et al.  The Copper Binding Domain of SPARC Mediates Cell Survival in Vitro via Interaction with Integrin β1 and Activation of Integrin-linked Kinase* , 2008, Journal of Biological Chemistry.

[59]  S. Akira,et al.  STAT3 is a Critical Regulator of Astrogliosis and Scar Formation after Spinal Cord Injury , 2008, The Journal of Neuroscience.

[60]  B. Barres,et al.  Thrombospondins 1 and 2 are Necessary for Synaptic Plasticity and Functional Recovery after Stroke , 2008, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[61]  Y. Eto,et al.  Alteration of inflammatory cytokine production in the injured central nervous system of tenascin-deficient mice. , 2008, In vivo.

[62]  Hong-Duck Kim,et al.  Toll-like receptor 4-dependent upregulation of cytokines in a transgenic mouse model of Alzheimer's disease , 2008, Journal of Neuroinflammation.

[63]  A. Roskams,et al.  SPARC is expressed by macroglia and microglia in the developing and mature nervous system , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[64]  J. Noth,et al.  TGF-β1 and TGF-β2 expression after traumatic human spinal cord injury , 2008, Spinal Cord.

[65]  S. Love,et al.  Abeta-degrading enzymes in Alzheimer's disease. , 2008, Brain pathology.

[66]  I. Brown,et al.  Localization of the Extracellular Matrix Protein SC1 Coincides with Synaptogenesis During Rat Postnatal Development , 2008, Neurochemical Research.

[67]  Y. Xing,et al.  A Transcriptome Database for Astrocytes, Neurons, and Oligodendrocytes: A New Resource for Understanding Brain Development and Function , 2008, The Journal of Neuroscience.

[68]  M. Freire,et al.  Cajal's contributions to glia research , 2007, Trends in Neurosciences.

[69]  I. Brown,et al.  Analysis of the extracellular matrix protein SC1 during reactive gliosis in the rat lithium–pilocarpine seizure model , 2007, Brain Research.

[70]  C. Farina,et al.  Astrocytes are active players in cerebral innate immunity. , 2007, Trends in immunology.

[71]  J. C. Baayen,et al.  Serial analysis of gene expression in the hippocampus of patients with mesial temporal lobe epilepsy , 2006, Neuroscience.

[72]  Milos Pekny,et al.  Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury , 2006, Proceedings of the National Academy of Sciences.

[73]  Frauke Zipp,et al.  The brain as a target of inflammation: common pathways link inflammatory and neurodegenerative diseases , 2006, Trends in Neurosciences.

[74]  J. Neary,et al.  Purinergic signaling induces thrombospondin-1 expression in astrocytes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[75]  B. Rosen,et al.  Role of matrix metalloproteinases in delayed cortical responses after stroke , 2006, Nature Medicine.

[76]  Henrik Ahlenius,et al.  Persistent Production of Neurons from Adult Brain Stem Cells During Recovery after Stroke , 2006, Stem cells.

[77]  T. Nishio,et al.  Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay , 2005, Neuroscience.

[78]  M. Haber,et al.  Reshaping neuron-glial communication at hippocampal synapses. , 2005, Neuron glia biology.

[79]  Yan Wang,et al.  Entorhinal deafferentation induces upregulation of SPARC in the mouse hippocampus. , 2005, Brain research. Molecular brain research.

[80]  M. Sofroniew,et al.  Reactive Astrocytes in Neural Repair and Protection , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[81]  Melitta Schachner,et al.  Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. , 2005, Cerebral cortex.

[82]  G. Rosenberg,et al.  Multiple roles for MMPs and TIMPs in cerebral ischemia , 2005, Glia.

[83]  M. West,et al.  Gene expression profiling and genetic markers in glioblastoma survival. , 2005, Cancer research.

[84]  J. Hell,et al.  Thrombospondins Are Astrocyte-Secreted Proteins that Promote CNS Synaptogenesis , 2005, Cell.

[85]  B. Weston,et al.  Connective tissue growth factor CCN2 interacts with and activates the tyrosine kinase receptor TrkA. , 2005, Journal of the American Society of Nephrology : JASN.

[86]  E. Sage,et al.  SPARC and tumor growth: Where the seed meets the soil? , 2004, Journal of cellular biochemistry.

[87]  E Helene Sage,et al.  Hevin/SC1, a matricellular glycoprotein and potential tumor-suppressor of the SPARC/BM-40/Osteonectin family. , 2004, The international journal of biochemistry & cell biology.

[88]  V. Gundersen,et al.  Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate , 2004, Nature Neuroscience.

[89]  Josephine C. Adams,et al.  Functions of the conserved thrombospondin carboxy-terminal cassette in cell-extracellular matrix interactions and signaling. , 2004, The international journal of biochemistry & cell biology.

[90]  K. Nose,et al.  Structural Characterization of TSC-36/Flik , 2004, Journal of Biological Chemistry.

[91]  Jerry Silver,et al.  Regeneration beyond the glial scar , 2004, Nature Reviews Neuroscience.

[92]  P. Rakic,et al.  SPARC-like 1 Regulates the Terminal Phase of Radial Glia-Guided Migration in the Cerebral Cortex , 2004, Neuron.

[93]  T. Nishio,et al.  Secretion of tenascin-C by cultured astrocytes: regulation of cell proliferation and process elongation , 2003, Brain Research.

[94]  A. Zien,et al.  Correlated stage‐ and subfield‐associated hippocampal gene expression patterns in experimental and human temporal lobe epilepsy , 2003, The European journal of neuroscience.

[95]  M. Reed,et al.  Cleavage of the Matricellular Protein SPARC by Matrix Metalloproteinase 3 Produces Polypeptides That Influence Angiogenesis* , 2003, Journal of Biological Chemistry.

[96]  R. Ravid,et al.  Cytokine, chemokine and growth factor gene profiling of cultured human astrocytes after exposure to proinflammatory stimuli , 2003, Glia.

[97]  Dirk Troost,et al.  Increased expression of connective tissue growth factor in amyotrophic lateral sclerosis human spinal cord , 2003, Acta Neuropathologica.

[98]  Pamela L. Follett,et al.  Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[99]  D. Bigner,et al.  Bone-related Genes Expressed in Advanced Malignancies Induce Invasion and Metastasis in a Genetically Defined Human Cancer Model* , 2003, The Journal of Biological Chemistry.

[100]  T. Arendt,et al.  Connective tissue growth factor in Alzheimer’s disease , 2003, Neuroscience.

[101]  Yong Y. He,et al.  Differential Regulation of Thrombospondin-1 and Thrombospondin-2 After Focal Cerebral Ischemia/Reperfusion , 2003, Stroke.

[102]  P. Bornstein,et al.  Matricellular proteins: extracellular modulators of cell function. , 2002, Current opinion in cell biology.

[103]  P. Gass,et al.  Fibronectin Domains of Extracellular Matrix Molecule Tenascin-C Modulate Hippocampal Learning and Synaptic Plasticity , 2002, Molecular and Cellular Neuroscience.

[104]  M. Schachner,et al.  Impairment of L-type Ca2+ Channel-Dependent Forms of Hippocampal Synaptic Plasticity in Mice Deficient in the Extracellular Matrix Glycoprotein Tenascin-C , 2002, The Journal of Neuroscience.

[105]  C. Faivre-Sarrailh,et al.  Tenascin-C Promotes Neurite Outgrowth of Embryonic Hippocampal Neurons through the Alternatively Spliced Fibronectin Type III BD Domains via Activation of the Cell Adhesion Molecule F3/Contactin , 2002, The Journal of Neuroscience.

[106]  Tony Wyss-Coray,et al.  Inflammation in Neurodegenerative Disease—A Double-Edged Sword , 2002, Neuron.

[107]  D Gveric,et al.  Astrocyte characterization in the multiple sclerosis glial scar , 2002, Neuropathology and applied neurobiology.

[108]  P. Bornstein,et al.  Thrombospondins as matricellular modulators of cell function. , 2001, The Journal of clinical investigation.

[109]  J. Murphy-Ullrich The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? , 2001, The Journal of clinical investigation.

[110]  J. Schwab,et al.  Differential cellular accumulation of connective tissue growth factor defines a subset of reactive astrocytes, invading fibroblasts, and endothelial cells following central nervous system injury in rats and humans. , 2001, Journal of neurotrauma.

[111]  M. Kurrer,et al.  Gene expression profiling of low-grade diffuse astrocytomas by cDNA arrays. , 2000, Cancer research.

[112]  G. Ivy,et al.  Induction of SC1 mRNA Encoding a Brain Extracellular Matrix Glycoprotein Related to SPARC following Lesioning of the Adult Rat Forebrain , 2000, Neurochemical Research.

[113]  R. Savani,et al.  Bleomycin-induced pulmonary injury in mice deficient in SPARC. , 2000, American journal of physiology. Lung cellular and molecular physiology.

[114]  J. Schwab,et al.  Connective tissue growth factor is expressed by a subset of reactive astrocytes in human cerebral infarction , 2000, Neuropathology and applied neurobiology.

[115]  S. Werner,et al.  Connective tissue growth factor: a novel player in tissue reorganization after brain injury? , 2000, The European journal of neuroscience.

[116]  T. Sasaki,et al.  Immunochemical and tissue analysis of protease generated neoepitopes of BM-40 (osteonectin, SPARC) which are correlated to a higher affinity binding to collagens. , 1999, Matrix biology : journal of the International Society for Matrix Biology.

[117]  M. Takigawa,et al.  Immunohistochemical localization of connective tissue growth factor in the rat central nervous system , 1999, Brain Research.

[118]  Clive N Svendsen,et al.  Leukocyte Infiltration, Neuronal Degeneration, and Neurite Outgrowth after Ablation of Scar-Forming, Reactive Astrocytes in Adult Transgenic Mice , 1999, Neuron.

[119]  E. Powell,et al.  Dissection of astrocyte‐mediated cues in neuronal guidance and process extension , 1999, Glia.

[120]  K. S. O'Shea,et al.  Thrombospondin expression in nerve regeneration II. comparison of optic nerve crush in the mouse and goldfish , 1999, Brain Research Bulletin.

[121]  H. M. Geller,et al.  Neurite outgrowth promotion by the alternatively spliced region of tenascin-C is influenced by cell-type specific binding. , 1999, Matrix biology : journal of the International Society for Matrix Biology.

[122]  T. Mikkelsen,et al.  SPARC: a signal of astrocytic neoplastic transformation and reactive response in human primary and xenograft gliomas. , 1998, Journal of neuropathology and experimental neurology.

[123]  M. Götz,et al.  Pax6 Controls Radial Glia Differentiation in the Cerebral Cortex , 1998, Neuron.

[124]  George M. Smith,et al.  Macrophage/Microglia Regulation of Astrocytic Tenascin: Synergistic Action of Transforming Growth Factor-β and Basic Fibroblast Growth Factor , 1997, The Journal of Neuroscience.

[125]  S. K. Malhotra,et al.  Reactive astrocytes: cellular and molecular cues to biological function , 1997, Trends in Neurosciences.

[126]  C. ffrench-Constant,et al.  Expression and function of thrombospondin‐1 in myelinating glial cells of the central nervous system , 1997, Journal of neuroscience research.

[127]  H. Beck,et al.  Hippocampal loss of tenascin boundaries in Ammon's horn sclerosis , 1997, Glia.

[128]  G. Ivy,et al.  SC1, a brain extracellular matrix glycoprotein related to SPARC and follistatin, is expressed by rat cerebellar astrocytes following injury and during development , 1996, Brain Research.

[129]  G. Kreutzberg,et al.  Regulation of thrombospondin in the regenerating mouse facial motor nucleus , 1996, Glia.

[130]  R. Margolskee,et al.  SC1: a marker for astrocytes in the adult rodent brain is upregulated during reactive astrocytosis , 1996, Brain Research.

[131]  S. Meiners,et al.  A distinct subset of tenascin/CS-6-PG-rich astrocytes restricts neuronal growth in vitro , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[132]  P. Caroni,et al.  Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth , 1995, The Journal of cell biology.

[133]  R. Timpl,et al.  The C-terminal portion of BM-40 (SPARC/osteonectin) is an autonomously folding and crystallisable domain that binds calcium and collagen IV. , 1995, Journal of molecular biology.

[134]  Y. Ben-Ari,et al.  Gliosis and axonal sprouting in the hippocampus of epileptic rats are associated with an increase of tenascin-C immunoreactivity , 1995, Journal of neurocytology.

[135]  D. Mendrick,et al.  Identification of integrin α 3 β 1 as a neuronal thrombospondin receptor mediating neurite outgrowth , 1995, Neuron.

[136]  L. Malaval,et al.  SPARC, an extracellular matrix glycoprotein containing the follistatin module, is expressed by astrocytes in synaptic enriched regions of the adult brain , 1995, Brain Research.

[137]  M. Iruela-Arispe,et al.  SPARC is a source of copper-binding peptides that stimulate angiogenesis , 1994, The Journal of cell biology.

[138]  M. Berry,et al.  Effects of Transforming Growth Factor β1, on Scar Production in the Injured Central Nervous System of the Rat , 1994, The European journal of neuroscience.

[139]  V. Dixit,et al.  Expression of thrombospondin in the adult nervous system , 1994, The Journal of comparative neurology.

[140]  H. Erickson Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. , 1993, Current opinion in cell biology.

[141]  Z. Werb,et al.  SPARC, a secreted protein associated with morphogenesis and tissue remodeling, induces expression of metalloproteinases in fibroblasts through a novel extracellular matrix-dependent pathway , 1993, The Journal of cell biology.

[142]  M. Iruela-Arispe,et al.  Differential expression of thrombospondin 1, 2, and 3 during murine development , 1993, Developmental dynamics : an official publication of the American Association of Anatomists.

[143]  E. Castrén,et al.  Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation , 1992, The Journal of cell biology.

[144]  D. Steindler,et al.  Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[145]  D. Higgins,et al.  Thrombospondin promotes process outgrowth in neurons from the peripheral and central nervous systems. , 1992, Developmental biology.

[146]  M. Schachner,et al.  Expression of tenascin in the developing and adult cerebellar cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[147]  K. S. O'Shea,et al.  Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 cells , 1991, Neuron.

[148]  L. Reichardt,et al.  Vitronectin and thrombospondin promote retinal neurite outgrowth: Developmental regulation and role of integrins , 1991, Neuron.

[149]  J. Kruse,et al.  J1/tenascin is a repulsive substrate for central nervous system neurons , 1990, Neuron.

[150]  J. Gurd,et al.  Molecular cloning of SC1: A putative brain extracellular matrix glycoprotein showing partial similarity to osteonectin/BM40/SPARC , 1990, Neuron.

[151]  B. Hogan,et al.  Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell ‘culture shock’ glycoprotein of Mr 43,000. , 1986, The EMBO journal.

[152]  R. Nachman,et al.  Human brain glial cells synthesize thrombospondin. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[153]  M. Schachner,et al.  Differential inhibition of neurone–neurone, neurone–astrocyte and astrocyte–astrocyte adhesion by L1, L2 and N-CAM antibodies , 1985, Nature.

[154]  R. Timpl,et al.  The J1 glycoprotein—a novel nervous system cell adhesion molecule of the L2/HNK-1 family , 1985, Nature.

[155]  D. Luciano,et al.  Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. , 2016 .

[156]  W. Schneider,et al.  Thrombospondin-1 binds to ApoER 2 and VLDL receptor and functions in postnatal neuronal migration , 2013 .

[157]  S. O'Bryant,et al.  Biomarkers of basic activities of daily living in Alzheimer's disease. , 2012, Journal of Alzheimer's disease : JAD.

[158]  T. Wyss-Coray,et al.  Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. , 2012, Cold Spring Harbor perspectives in medicine.

[159]  Ulrich Müller,et al.  Extracellular matrix: functions in the nervous system. , 2011, Cold Spring Harbor perspectives in biology.

[160]  Josephine C. Adams,et al.  The thrombospondins. , 2011, Cold Spring Harbor perspectives in biology.

[161]  Jun Xia,et al.  Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1 , 2010, Nature Neuroscience.

[162]  Stephen J. Smith,et al.  Gabapentin Receptor alpha 2 delta-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis , 2009 .

[163]  Peter Schirmacher,et al.  Tumor-suppressor function of SPARC-like protein 1/Hevin in pancreatic cancer. , 2007, Neoplasia.

[164]  M. Takigawa,et al.  CCN family proteins and angiogenesis: from embryo to adulthood , 2006, Angiogenesis.

[165]  R. Brekken,et al.  SPARC, a matricellular protein: at the crossroads of cell-matrix communication. , 2001, Matrix biology : journal of the International Society for Matrix Biology.

[166]  R. Probstmeier,et al.  Tenascin-C inhibits beta1 integrin-dependent cell adhesion and neurite outgrowth on fibronectin by a disialoganglioside-mediated signaling mechanism. , 1999, Glycobiology.

[167]  Y. Ben-Ari,et al.  Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression , 1996, Journal of neurocytology.

[168]  D. Steindler,et al.  Boundaries defined by adhesion molecules during development of the cerebral cortex: the J1/tenascin glycoprotein in the mouse somatosensory cortical barrel field. , 1989, Developmental biology.