Skip to main content

Advertisement

SpringerLink
Log in

Existence of Tenascin-C Isoforms in Rat that Contain the Alternatively Spliced AD1 Domain are Developmentally Regulated During Hippocampal Development

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Tenascin-C (TN-C) is a multimodular glycoprotein of the extracellular matrix which is important for the development of the nervous system and has a range of different functions which are mediated by the different protein domains present. TN-C contains eight constitutive fibronectin type III (FNIII) domains and a region of alternatively spliced FNIII domains. In the mouse and chick, six of these domains have been described and characterized, whereas in human there are nine of them. In this report, we show that seven alternatively spliced FNIII domains exist in rat and describe the differential expression pattern of the additional domain AD1 during embryonic and postnatal rat brain development. The AD1 domain of rat is homologous to the ones described in human and chick proteins but does not exist in mouse. Its expression can be located to the developing rat hippocampus and the lining of the lateral ventricle, regions where the TN-C protein may affect the behavior of stem and progenitor cells. During hippocampal development AD1 and the other alternatively spliced domains are differentially expressed as shown by RT-PCRs, immunocytochemistry and in situ hybridizations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

TN-C:

Tenascin-C

FNIII:

Fibronectin type III domain

RT-PCR:

Reverse transcription-polymerase chain reaction

ECM:

Extracellular matrix

CNS:

Central nervous system

EGF:

Epidermal growth factor

PDGF:

Platelet-derived growth factor

VZ:

Ventricular zone

CA:

Cornu ammonis

MMP:

Matrix metalloproteinase

TGF:

Transforming growth factor

References

  • Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M (1992) Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736–749

    PubMed  CAS  Google Scholar 

  • Berndt A, Anger K, Richter P, Borsi L, Brack S, Silacci M, Franz M, Wunderlich H, Gajda M, Zardi L et al (2006) Differential expression of tenascin-C splicing domains in urothelial carcinomas of the urinary bladder. J Cancer Res Clin Oncol 132:537–546

    Article  PubMed  CAS  Google Scholar 

  • Chiquet-Ehrismann R, Chiquet M (2003) Tenascins: regulation and putative functions during pathological stress. J Pathol 200:488–499

    Article  PubMed  CAS  Google Scholar 

  • Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47:131–139

    Article  PubMed  CAS  Google Scholar 

  • Crossin KL (1996) Tenascin: a multifunctional extracellular matrix protein with a restricted distribution in development and disease. J Cell Biochem 61:592–598

    Article  PubMed  CAS  Google Scholar 

  • Czopka T, von Holst A, Schmidt G, Ffrench-Constant C, Faissner A (2009) Tenascin C and tenascin R similarly prevent the formation of myelin membranes in a RhoA-dependent manner, but antagonistically regulate the expression of myelin basic protein via a separate pathway. Glia 57:1790–1801

    Article  PubMed  Google Scholar 

  • Czopka T, von Holst A, Ffrench-Constant C, Faissner A (2010) Regulatory mechanisms that mediate tenascin C-dependent inhibition of oligodendrocyte precursor differentiation. J Neurosci 30:12333–122310

    Article  Google Scholar 

  • Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M (1997) Up-regulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:829–846

    Article  PubMed  CAS  Google Scholar 

  • Derr LB, Chiquet-Ehrismann R, Gandour-Edwards R, Spence J, Tucker RP (1997) The expression of tenascin-C with the AD1 variable repeat in embryonic tissues, cell lines and tumors in various vertebrate species. Differentiation 62:71–82

    Article  PubMed  CAS  Google Scholar 

  • Dobbertin A, Czvitkovich S, Theocharidis U, Garwood J, Andrews MR, Properzi F, Lin R, Fawcett JW, Faissner A (2010) Analysis of combinatorial variability reveals selective accumulation of the fibronectin type III domains B and D of tenascin-C in injured brain. Exp Neurol 225:60–73

    Article  PubMed  CAS  Google Scholar 

  • Faissner A (1997) The tenascin gene family in axon growth and guidance. Cell Tissue Res 290:331–341

    Article  PubMed  CAS  Google Scholar 

  • Faissner A, Kruse J (1990) J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5:627–637

    Article  PubMed  CAS  Google Scholar 

  • Faissner A, Steindler D (1995) Boundaries and inhibitory molecules in developing neural tissues. Glia 13:233–254

    Article  PubMed  CAS  Google Scholar 

  • Faissner A, Kruse J, Kuhn K, Schachner M (1990) Binding of the J1 adhesion molecules to extracellular matrix constituents. J Neurochem 54:1004–1015

    Article  PubMed  CAS  Google Scholar 

  • Fischer D, Tucker RP, Chiquet-Ehrismann R, Adams JC (1997) Cell-adhesive responses to tenascin-C splice variants involve formation of fascin microspikes. Mol Biol Cell 8:2055–2075

    PubMed  CAS  Google Scholar 

  • Garcion E, Faissner A, Ffrench-Constant C (2001) Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128:2485–2496

    PubMed  CAS  Google Scholar 

  • Garcion E, Halilagic A, Faissner A, Ffrench-Constant C (2004) Generation of an environmental niche for neural stem cell development by the extracellular matrix molecule tenascin C. Development 131:3423–3432

    Article  PubMed  CAS  Google Scholar 

  • Garwood J, Heck N, Rigato F, Faissner A (eds) (2001a) The extracellular matrix in neural development, plasticity, and regeneration. Humana Press Inc., Totowa

    Google Scholar 

  • Garwood J, Rigato F, Heck N, Faissner A (2001b) Tenascin glycoproteins and the complementary ligand DSD-1-PG/phosphacan-structuring the neural extracellular matrix during development and repair. Restor Neurol Neurosci 19:51–64

    PubMed  CAS  Google Scholar 

  • Garwood J, Garcion E, Dobbertin A, Heck N, Calco V, Ffrench-Constant C, Faissner A (2004) The extracellular matrix glycoprotein tenascin-C is expressed by oligodendrocyte precursor cells and required for the regulation of maturation rate, survival and responsiveness to platelet-derived growth factor. Eur J Neurosci 20:2524–2540

    Article  PubMed  Google Scholar 

  • Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Gotz B, Silver J, Steindler DA (1995) Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol 361:249–266

    Article  PubMed  CAS  Google Scholar 

  • Husmann K, Faissner A, Schachner M (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J Cell Biol 116:1475–1486

    Article  PubMed  CAS  Google Scholar 

  • Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 371:376–396

    Article  PubMed  CAS  Google Scholar 

  • Joester A, Faissner A (1999) Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J Biol Chem 274:17144–17151

    Article  PubMed  CAS  Google Scholar 

  • Joester A, Faissner A (2001) The structure and function of tenascins in the nervous system. Matrix Biol 20:13–22

    Article  PubMed  CAS  Google Scholar 

  • Jones FS, Jones PL (2000a) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259

    Article  PubMed  CAS  Google Scholar 

  • Jones PL, Jones FS (2000b) Tenascin-C in development and disease: gene regulation and cell function. Matrix Biol 19:581–596

    Article  PubMed  CAS  Google Scholar 

  • Laywell ED, Steindler DA (1991) Boundaries and wounds, glia and glycoconjugates. Cellular and molecular analyses of developmental partitions and adult brain lesions. Ann N Y Acad Sci 633:122–141

    Article  PubMed  CAS  Google Scholar 

  • Miragall F, Kadmon G, Faissner A, Antonicek H, Schachner M (1990) Retention of J1/tenascin and the polysialylated form of the neural cell adhesion molecule (N-CAM) in the adult olfactory bulb. J Neurocytol 19:899–914

    Article  PubMed  CAS  Google Scholar 

  • Moritz S, Lehmann S, Faissner A, von Holst A (2008) An induction gene trap screen in neural stem cells reveals an instructive function of the niche and identifies the splicing regulator sam68 as a tenascin-C-regulated target gene. Stem Cells 26:2321–2331

    Article  PubMed  CAS  Google Scholar 

  • Rigato F, Garwood J, Calco V, Heck N, Faivre-Sarrailh C, Faissner A (2002) 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. J Neurosci 22:6596–6609

    PubMed  CAS  Google Scholar 

  • Taylor J, Pesheva P, Schachner M (1993) Influence of janusin and tenascin on growth cone behavior in vitro. J Neurosci Res 35:347–362

    Article  PubMed  CAS  Google Scholar 

  • Theodosis DT, Pierre K, Cadoret MA, Allard M, Faissner A, Poulain DA (1997) Expression of high levels of the extracellular matrix glycoprotein, tenascin-C, in the normal adult hypothalamoneurohypophysial system. J Comp Neurol 379:386–398

    Article  PubMed  CAS  Google Scholar 

  • von Holst A, Egbers U, Prochiantz A, Faissner A (2007) Neural stem/progenitor cells express 20 tenascin C isoforms that are differentially regulated by Pax6. J Biol Chem 282:9172–9181

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Tim Czopka for the TN-C riboprobe, Anke Mommsen for excellent technical assistance, and Corinna Zimmermann for her help. This study was supported by the CNRS, German Research Council (DFG SPP, Molecular and Cellular Basis of CNS Repair Fa 159/11-1,2,3), the Association pour la Recherche contre le Cancer (ARC), and the International Spinal Research Trust (ISRT).

Author information

Authors and Affiliations

  1. Department of Cell Morphology and Molecular Neurobiology, Ruhr University, NDEF 05/593, Universitätsstraße 150, 44780, Bochum, Germany

    J. Garwood, U. Theocharidis & A. Faissner

  2. Département Neurotransmission et Sécrétion Neuroendocrine, Institut des Neurosciences Cellulaires et Intégratives (UPR 3212), Centre National de la Recherche Scientifique et Université de Strasbourg, 5 rue Blaise Pascal, 67084, Strasbourg, France

    V. Calco

  3. Université Paris Descartes, INSERM U686, Centre universitaire des Saints-Pères, 75006, Paris, France

    A. Dobbertin

Authors
  1. J. Garwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. U. Theocharidis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Calco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Dobbertin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Faissner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to J. Garwood or A. Faissner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garwood, J., Theocharidis, U., Calco, V. et al. Existence of Tenascin-C Isoforms in Rat that Contain the Alternatively Spliced AD1 Domain are Developmentally Regulated During Hippocampal Development. Cell Mol Neurobiol 32, 279–287 (2012). https://doi.org/10.1007/s10571-011-9759-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-011-9759-1

Keywords

Search

Navigation