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      Revisiting the matricellular concept

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          Abstract

          The concept of a matricellular protein was first proposed by Paul Bornstein in the mid-1990s to account for the non-lethal phenotypes of mice with inactivated genes encoding thrombospondin-1, tenascin-C, or SPARC. It was also recognized that these extracellular matrix proteins were primarily counter or de-adhesive. This review reappraises the matricellular concept after nearly two decades of continuous investigation. The expanded matricellular family as well as the diverse and often unexpected functions, cellular location, and interacting partners/receptors of matricellular proteins are considered. Development of therapeutic strategies that target matricellular proteins are discussed in the context of pathology and regenerative medicine.

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          Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis.

          Cagla Eroglu, Nicola J Allen, Michael W Susman … (2009)
          Synapses are asymmetric cellular adhesions that are critical for nervous system development and function, but the mechanisms that induce their formation are not well understood. We have previously identified thrombospondin as an astrocyte-secreted protein that promotes central nervous system (CNS) synaptogenesis. Here, we identify the neuronal thrombospondin receptor involved in CNS synapse formation as alpha2delta-1, the receptor for the anti-epileptic and analgesic drug gabapentin. We show that the VWF-A domain of alpha2delta-1 interacts with the epidermal growth factor-like repeats common to all thrombospondins. alpha2delta-1 overexpression increases synaptogenesis in vitro and in vivo and is required postsynaptically for thrombospondin- and astrocyte-induced synapse formation in vitro. Gabapentin antagonizes thrombospondin binding to alpha2delta-1 and powerfully inhibits excitatory synapse formation in vitro and in vivo. These findings identify alpha2delta-1 as a receptor involved in excitatory synapse formation and suggest that gabapentin may function therapeutically by blocking new synapse formation.
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            Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC.

            Hakan Kucukdereli, Nicola J Allen, Anthony Lee … (2011)
            Astrocytes regulate synaptic connectivity in the CNS through secreted signals. Here we identified two astrocyte-secreted proteins, hevin and SPARC, as regulators of excitatory synaptogenesis in vitro and in vivo. Hevin induces the formation of synapses between cultured rat retinal ganglion cells. SPARC is not synaptogenic, but specifically antagonizes synaptogenic function of hevin. Hevin and SPARC are expressed by astrocytes in the superior colliculus, the synaptic target of retinal ganglion cells, concurrent with the excitatory synaptogenesis. Hevin-null mice had fewer excitatory synapses; conversely, SPARC-null mice had increased synaptic connections in the superior colliculus. Furthermore, we found that hevin is required for the structural maturation of the retinocollicular synapses. These results identify hevin as a positive and SPARC as a negative regulator of synapse formation and signify that, through regulation of relative levels of hevin and SPARC, astrocytes might control the formation, maturation, and plasticity of synapses in vivo.
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              Osteopontin: role in immune regulation and stress responses.

              Kathryn X Wang, David T Denhardt (2008)
              Recent research has led to a better but as yet incomplete understanding of the complex roles osteopontin plays in mammalian physiology. A soluble protein found in all body fluids, it stimulates signal transduction pathways (via integrins and CD44 variants) similar to those stimulated by components of the extracellular matrix. This appears to promote the survival of cells exposed to potentially lethal insults such as ischemia/reperfusion or physical/chemical trauma. OPN is chemotactic for many cell types including macrophages, dendritic cells, and T cells; it enhances B lymphocyte immunoglobulin production and proliferation. In inflammatory situations it stimulates both pro- and anti-inflammatory processes, which on balance can be either beneficial or harmful depending on what other inputs the cell is receiving. OPN influences cell-mediated immunity and has been shown to have Th1-cytokine functions. OPN deficiency is linked to a reduced Th1 immune response in infectious diseases, autoimmunity and delayed type hypersensitivity. OPN's role in the central nervous system and in stress responses has also emerged as an important aspect related to its cytoprotective and immune functions. Evidence suggests that either OPN or anti-OPN monoclonal antibodies (depending on the circumstances) might be clinically useful in modulating OPN function. Manipulation of plasma OPN levels may be useful in the treatment of autoimmune disease, cancer metastasis, osteoporosis and some forms of stress.
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 9432592
                Journal ID (pubmed-jr-id): 8496
                Journal ID (nlm-ta): Matrix Biol
                Journal ID (iso-abbrev): Matrix Biol.
                Title: Matrix biology : journal of the International Society for Matrix Biology
                ISSN (Print): 0945-053X
                ISSN (Electronic): 1569-1802
                Publication date Nihms-submitted: 12 March 2015
                Publication date (Electronic): 24 July 2014
                Publication date (Print): July 2014
                Publication date PMC-release: 31 March 2015
                Volume: 37
                Pages: 1-14
                Affiliations
                [a ]Department of Pathology, University of Alabama at Birmingham, Birmingham, AL 35294-0019, United States
                Author notes
                [* ]Corresponding author at: Department of Pathology, University of Alabama at Birmingham, Volker Hall G001, Birmingham, AL 35294-0019, United States. Tel.: +1 205 934 0415; fax: +1 205 975 9927,. murphy@ 123456uab.edu (J.E. Murphy-Ullrich)
                Article
                Manuscript ID: NIHMS670769
                DOI: 10.1016/j.matbio.2014.07.005
                PMC ID: 4379989
                PubMed ID: 25064829
                SO-VID: 03ca92eb-7988-463c-89e9-1b6bea28470e
                Copyright © © 2014 Published by Elsevier B.V.
                License:

                This is an open access article under the CC BY-NC-ND license ( http://creativecommons.org/licenses/by-nc-nd/3.0/).

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                Subject: Article

                ScienceOpen disciplines: Molecular biology
                Keywords: matricellular,thrombospondins,sparc,hevin,tenascins,ccn,osteopontin,fibulin,periostin,r-spondin,extracellular matrix,cell adhesion,regenerative medicine
                Data availability:
                ScienceOpen disciplines: Molecular biology
                Keywords: matricellular, thrombospondins, sparc, hevin, tenascins, ccn, osteopontin, fibulin, periostin, r-spondin, extracellular matrix, cell adhesion, regenerative medicine

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