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Cell surface expression of 27C7 by neonatal rat olfactory ensheathing cells in situ and in vitro is independent of axonal contact

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Abstract

Olfactory ensheathing cells (OECs) are Schwann cell-like glial cells of the olfactory system that promote neural regeneration after transplantation into the injured central nervous system. Compared to the closely related Schwann cells, however, the biological characterization of OECs has remained fragmentary. This is due to the fact that the expression of OEC-specific markers is subject to complex regulation and that intricate ultrastructural analysis is essential to determine their localization. The p75 neurotrophin receptor (p75NTR) as the prototype OEC marker, for example, is only expressed by a minor population of neonatal rat OECs in situ. The major population carries O4-positive axonal fragments on their surface after dissociation and up-regulates p75NTR during culturing (Wewetzer et al. in Glia 49:577–587, 2005). In the present study, we investigated whether the cell surface determinant 27C7, defined by a monoclonal antibody to Schwann cells, is also expressed by neonatal rat OECs in situ and in vitro. Primary cell suspensions of the olfactory bulb displayed 27C7 expression of both p75NTR-negative and p75NTR-positive OECs, while immature oligodendrocytes and astrocytes were devoid of any 27C7 labeling. This together with the finding that the intrafascicular OECs of the olfactory nerves in the mucosa expressed 27C7 but not p75NTR, suggests that 27C7 was expressed by the entire OEC population in situ. Maintenance of OECs in the absence of olfactory neurons in organotypic slice culture up-regulated p75NTR but did not alter 27C7 expression. It is concluded that 27C7 unlike p75NTR is constitutively expressed by OECs and may, therefore, be a useful marker for characterization of neonatal OECs in situ and in vitro.

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References

  • Alexander CL, Fitzgerald UF, Barnett SC (2002) Identification of growth factors that promote long-term proliferation of olfactory ensheathing cells and modulate their antigenic phenotype. Glia 37:349–364

    Article  PubMed  Google Scholar 

  • Asan E, Langenhan T, Holtmann B, Bock H, Sendtner M, Carroll P (2003) Ciliary neurotrophic factor in the olfactory bulb of rats and mice. Neuroscience 120:99–112

    Article  PubMed  CAS  Google Scholar 

  • Au WW, Treolar HB, Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68–80

    Article  PubMed  Google Scholar 

  • Barnett SC, Hutchins AM, Noble M (1993) Purification of olfactory nerve ensheathing cells from the olfactory bulb. Dev Biol 55:337–350

    Article  Google Scholar 

  • Barnett SC, Chang L (2004) Olfactory ensheathing cells and CNS repair: going solo or in need of a friend? Trends Neurosci 1:54–60

    Article  Google Scholar 

  • Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ, Baker CV (2010) Neural crest origin of olfactory ensheathing glia. Proc Natl Acad Sci USA 107:21040–21045

    Article  PubMed  CAS  Google Scholar 

  • Bock P, Beineke A, Techangamsuwan S, Baumgärtner W, Wewetzer K (2007) Differential expression of HNK-1 and p75(NTR) in adult canine Schwann cells and olfactory ensheathing cells in situ but not in vitro. J Comp Neurol 505:572–585

    Article  PubMed  Google Scholar 

  • Bock P, Beineke A, Baumgärtner W, Wewetzer K (2009) Site-specific population dynamics and variable olfactory marker protein expression in the adult canine olfactory epithelium. J Anat 215:522–535

    Article  PubMed  CAS  Google Scholar 

  • Boyd JG, Jahed A, McDonald TG, Krol KM, VanEyk JE, Doucette R, Kawaja MD (2006) Proteomic evaluation reveals that olfactory ensheathing cells but not Schwann cells express calponin. Glia 53:434–440

    Article  PubMed  Google Scholar 

  • Brandes G, Reale E (1990) The reaction of acridine orange with proteoglycans in the articular cartilage of the rat. Histochem J 22:106–112

    Article  PubMed  CAS  Google Scholar 

  • Chandler CE, Parsons LM, Hosang M, Shooter EM (1984) A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J Biol Chem 259:6882–6889

    PubMed  CAS  Google Scholar 

  • Field P, Li Y, Raisman G (2003) Ensheathment of the olfactory nerves in the adult rat. J Neurocytol 32:317–324

    Article  PubMed  Google Scholar 

  • Fortun J, Hill CE, Bunge MB (2009) Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci Lett 4563:124–132

    Article  Google Scholar 

  • Franceschini IA, Barnett SC (1996) Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 173:327–343

    Article  PubMed  CAS  Google Scholar 

  • Franklin RJ, Barnett SC (1997) Do olfactory glia have advantages over Schwann cells for CNS repair? J Neurosci Res 50:665–672

    Article  PubMed  CAS  Google Scholar 

  • Franssen EH, De Bree FM, Essing AH, Ramón-Cueto A, Verhaagen J (2008) Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 56:1285–1298

    Article  PubMed  Google Scholar 

  • Frosch M, Görgen I, Boulnois GJ, Timmis KN, Bitter-Suermann D (1985) NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc Natl Acad Sci USA 82:1194–1198

    Article  PubMed  CAS  Google Scholar 

  • Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT (1994) Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. J Comp Neurol 344:336–348

    Article  PubMed  CAS  Google Scholar 

  • Graziadei PP, Monti Graziadei GA (1985) Neurogenesis and plasticity of the olfactory sensory neurons. Ann N Y Acad Sci 457:127–142

    Article  PubMed  CAS  Google Scholar 

  • Heimrich B, Frotscher M (1993) Slice cultures as a model to study entorhinal–hippocampal interaction. Hippocampus 3 Spec No:11–17

  • Jessen KR, Morgan L, Stewart HJ, Mirsky R (1990) Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109:91–103

    PubMed  CAS  Google Scholar 

  • Jessen KR, Mirsky R (1999) Developmental regulation in the Schwann cell lineage. Adv Exp Med Biol 468:3–12

    PubMed  CAS  Google Scholar 

  • Jessen KR, Mirsky R (2002) Signals that determine Schwann cell identity. J Anat 200:367–376

    Article  PubMed  CAS  Google Scholar 

  • Jones LL, Sajed D, Tuszynski MH (2003) Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 23:9276–9288

    PubMed  CAS  Google Scholar 

  • Josephson EM, Yilma S, Vodyanov V, Morrison EE (2004) Structure and function of long-lived olfactory organotypic cultures from postnatal mice. J Neurosci Res 75:642–653

    Article  PubMed  CAS  Google Scholar 

  • Klinge PM, Vafa MA, Brinker T, Brandis A, Walter GF, Stieglitz T, Samii M, Wewetzer K (2001) Immunohistochemical characterization of axonal sprouting and reactive tissue changes after long-term implantation of a polyimide sieve electrode to the transected adult rat sciatic nerve. Biomaterials 22:2333–2343

    Article  PubMed  CAS  Google Scholar 

  • Krudewig C, Deschl U, Wewetzer K (2006) Purification and in vitro characterization of adult canine olfactory ensheathing cells. Cell Tissue Res 326:687–696

    Article  PubMed  CAS  Google Scholar 

  • Lavdas AA, Papastefanaki F, Thomaidou D, Matsas R (2008) Schwann cell transplantation for CNS repair. Curr Med Chem 15:151–160

    Article  PubMed  CAS  Google Scholar 

  • Lim JH, Brunjes PC (1999) Activity-dependent regulation of interleukin-1 beta immunoreactivity in the developing rat olfactory bulb. Neuroscience 93:371–374

    Article  PubMed  CAS  Google Scholar 

  • Lu P, Jones LL, Tuszynski MH (2005) BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp Neurol 191:344–360

    Article  PubMed  CAS  Google Scholar 

  • Lu P, Yang H, Culbertson M, Graham L, Roskams AJ, Tuszynski MH (2006) Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci 26:1120–1130

    Google Scholar 

  • Lu P, Jones LL, Tuszynski MH (2007) Axon regeneration through scars and into sites of chronic spinal cord injury. Exp Neurol 203:8–21

    Article  PubMed  CAS  Google Scholar 

  • Mirsky R, Jessen KR, Brennan A, Parkinson D, Dong Z, Meier C, Parmantier E, Lawson D (2002) Schwann cells as regulators of nerve development. J Physiol Paris 96:17–24

    Article  PubMed  CAS  Google Scholar 

  • Mirsky M, Jessen KR (2005) Molecular signaling in Schwann cell development. In: Dyck PJ, Thomas PK (eds) Peripheral neuropathy, 4th edn. Elsevier, Saunders, pp 341–376

    Google Scholar 

  • Radtke C, Wewetzer K (2009) Translating basic research into clinical practice: what else do we have to learn about olfactory ensheathing cells? Neurosci Lett 456:133–136

    Article  PubMed  CAS  Google Scholar 

  • Raisman G (1985) Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237–254

    Article  PubMed  CAS  Google Scholar 

  • Ramón-Cueto A, Avila J (1998) Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175–187

    Article  PubMed  Google Scholar 

  • Santos-Benito FF, Ramón-Cueto A (2003) Olfactory ensheathing glia transplantation: a therapy to promote repair in the mammalian central nervous system. Anat Rec 271B:77–85

    Article  Google Scholar 

  • Sommer I, Schachner M (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:311–327

    Article  PubMed  CAS  Google Scholar 

  • Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:172–182

    Article  Google Scholar 

  • Techangamsuwan S, Imbschweiler I, Kreutzer R, Kreutzer M, Baumgärtner W, Wewetzer K (2008) Similar behaviour and primate-like properties of adult canine Schwann cells and olfactory ensheathing cells in long-term culture. Brain Res 1240:31–38

    Article  PubMed  CAS  Google Scholar 

  • Turner CP, Perez-Polo JR (1993) Expression of p75NGFR in the olfactory system following peripheral deafferentation. Neuroreport 4:1023–1026

    Article  PubMed  CAS  Google Scholar 

  • Turner CP, Perez-Polo JR (1994) Changes in expression of the low affinity receptor for neurotrophins, p75NGFR, in the regenerating olfactory system. Int J Dev Neurosci 12:767–773

    Article  PubMed  CAS  Google Scholar 

  • Vickland H, Westrum LE, Kott JN, Patterson SL, Bothwell MA (1991) Nerve growth factor receptor expression in the young and adult rat olfactory system. Brain Res 565:269–279

    Article  PubMed  CAS  Google Scholar 

  • Vincent AJ, Taylor JM, Choi-Lundberg DL, West AK, Chuah MI (2005) Genetic expression profile of olfactory ensheathing cells is distinct from that of Schwann cells and astrocytes. Glia 51:132–147

    Article  PubMed  Google Scholar 

  • Vroemen M, Weidner N (2003) Purification of Schwann cells by selection of p75 low affinity nerve growth factor receptor expressing cells from adult peripheral nerve. J Neurosci Methods 124:135–143

    Article  PubMed  CAS  Google Scholar 

  • Weidner N, Blesch A, Grill RJ, Tuszynski MH (1999) Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J Comp Neurol 413:495–506

    Article  PubMed  CAS  Google Scholar 

  • Wewetzer K, Brandes G (2006) Axonal signalling and the making of olfactory ensheathing cells: a hypothesis. Neuron Glia Biol 2:217–224

    Article  PubMed  Google Scholar 

  • Wewetzer K, Grothe C, Christ B, Seilheimer B (1997) Identification and characterization of differentiation-dependent Schwann cell surface antigens by novel monoclonal antibodies: introduction of a marker common to the non-myelin-forming phenotype. Glia 19:213–226

    Article  PubMed  CAS  Google Scholar 

  • Wewetzer K, Heiniger C, Seilheimer B (1996) An improved cell ELISA for the differential screening of antibodies against cell surface molecules of viable adherent Schwann cells. J Immunol Methods 191:171–178

    Article  PubMed  CAS  Google Scholar 

  • Wewetzer K, Kern N, Ebel C, Radtke C, Brandes G (2005) Phagocytosis of O4+ axonal fragments in vitro by p75- neonatal rat olfactory ensheathing cells. Glia 49:577–587

    Article  PubMed  Google Scholar 

  • Wewetzer K, Radtke C, Kocsis J, Baumgärtner W (2010) Species-specific control of cellular proliferation and the impact of large animal models for the use of olfactory ensheathing cells and Schwann cells in spinal cord repair. Exp Neurol (Epub ahead of print)

  • Wewetzer K, Verdú E, Angelov DN, Navarro X (2002) Olfactory ensheathing glia and Schwann cells: two of a kind? Cell Tissue Res 309:337–345

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank H. Schneider for excellent technical assistance and Drs. E. Shooter, S. Barnett, and R. Gerardy-Schahn for providing anti-p75NTR, anti-O4, and anti-PSA antibodies, respectively. This study was supported by a grant from the German Research Foundation to K.W. and W.B. (BA815/10-1).

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Authors and Affiliations

  1. Department of Cell Biology, Hannover Medical School, 30625, Hannover, Germany

    Gudrun Brandes

  2. Department of Functional and Applied Anatomy, Center of Anatomy, Hannover Medical School, 30625, Hannover, Germany

    Massoud Khayami, Hatice Bugday & Konstantin Wewetzer

  3. Department of Pathology, University of Veterinary Medicine Hannover, Bünteweg 17, 30559, Hannover, Germany

    Claas-Tido Peck, Wolfgang Baumgärtner & Konstantin Wewetzer

  4. Center of Systems Neuroscience, Hannover, Germany

    Wolfgang Baumgärtner & Konstantin Wewetzer

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  1. Gudrun Brandes
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  2. Massoud Khayami
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  4. Wolfgang Baumgärtner
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  6. Konstantin Wewetzer
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Correspondence to Konstantin Wewetzer.

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Brandes, G., Khayami, M., Peck, CT. et al. Cell surface expression of 27C7 by neonatal rat olfactory ensheathing cells in situ and in vitro is independent of axonal contact. Histochem Cell Biol 135, 397–408 (2011). https://doi.org/10.1007/s00418-011-0796-0

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  • DOI: https://doi.org/10.1007/s00418-011-0796-0

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