Increased p75 neurotrophin receptor expression in the canine distemper virus model of multiple sclerosis identifies aldynoglial schwann cells that emerge in response to axonal damage

GLIA

Volumn 60, Issue 3, 2012, Pages 358-371

  Imbschweiler, Ilka ^a   Seehusen, Frauke ^a   Peck, Claas Tido ^a   Omar, Mohamed ^b   Baumgärtner, Wolfgang ^a,c   Wewetzer, Konstantin ^a,b,c  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Axonal pathology; Demyelination; Differentiation; Precursor; Remyelination; Schwann cells

Indexed keywords

AMYLOID PRECURSOR PROTEIN; NEUROFILAMENT PROTEIN; NEUROTROPHIN RECEPTOR P75;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANINE DISTEMPER MORBILLIVIRUS; CELL DIFFERENTIATION; DEMYELINATION; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC INFILTRATION; MULTIPLE SCLEROSIS; NERVE FIBER GROWTH; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; WHITE MATTER;

ANIMALS; ANTIGENS, CD; DISEASE MODELS, ANIMAL; DISTEMPER; DISTEMPER VIRUS, CANINE; DOGS; ETHANOL; GENE EXPRESSION REGULATION, VIRAL; MULTIPLE SCLEROSIS; OLFACTORY BULB; OLIGODENDROGLIA; ORGAN CULTURE TECHNIQUES; RECEPTOR, NERVE GROWTH FACTOR; SCHWANN CELLS; SULFIDES; VIRAL PROTEINS;

EID: 84856235468     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22270     Document Type: Article

References (85)

1. Archelos JJ, Roggenbuck K, Schneider-Schaulies J, Linington C, Toyka KV, Hartung HP. 1993. Production and characterization of monoclonal antibodies to the extracellular domain of P0. J Neurosci Res 35: 46-53.
2. Beineke A, Puff C, Seehusen F, Baumgärtner W. 2009. Pathogenesis and immunopathology of systemic and nervous canine distemper. Vet Immunol Immunopathol 127: 1-18.
3. Blakemore WF. 2005. The case for a central nervous system (CNS) origin for the Schwann cells that remyelinate CNS axons following concurrent loss of oligodendrocytes and astrocytes. Neuropathol Appl Neurobiol 31: 1-10.
4. Blanchard AD, Sinanan A, Parmantier E, Zwart R, Broos L, Meijer D, Meier C, Jessen KR, Mirsky R. 1996. Oct-6 (SCIP/Tst-1) is expressed in Schwann cell precursors, embryonic Schwann cells, and postnatal myelinating Schwann cells: Comparison with Oct-1, Krox-20, and Pax-3. J Neurosci Res 46: 630-640.
5. NTR in adult canine Schwann cells and olfactory ensheathing cells in situ but not in vitro. J Comp Neurol 505: 572-585.
6. Boekhoff TM, Ensinger EM, Carlson RBock P, Baumgärtner W, Rohn K, Tipold A, Stein VM. 2011. Microglial contribution to secondary injury evaluated in a large animal model of human spinal cord trauma. J Neurotrauma [Epub ahead of print].
7. Brandes G, Khayami M, Peck C-T, Baumgärtner W, Bugday H, Wewetzer K. 2011. 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.
8. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. 2000. NG2-positive oligodendrocyte progenitor cells in adult human brain and Multiple Sclerosis lesions. J Neurosci 20: 6404-6412.
9. Chang A, Tourtellotte WW, Rudick R, Trapp BD. 2002. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 346: 199-200.
10. Copray S, Küst B, Emmer B, Lin MY, Liem R, Amor S, de Vries H, Floris S, Boddeke E. 2004. Deficient p75 low-affinity neurotrophin receptor expression exacerbates experimental allergic encephalomyelitis in C57/BL6 mice. J Neuroimmunol 148: 41-53.
11. Cotman CW, Head E. 2008. The canine (dog) model of human aging and disease: Dietary, environmental and immunotherapy approaches. J Alzheimers Dis 15: 685-707.
12. Crisan M, Chen CW, Corselli M, Andriolo G, Lazzari L, Péault B. 2009. Perivascular multipotent progenitor cells in human organs. Ann NY Acad Sci 1176: 118-123.
13. Crockett DP, Wang L, Zhang RX, Egger MD. 1999. Distribution of the low-affinity neurotrophin receptor (p75) in the developing trigeminal brainstem complex in the rat. Anat Rec 254: 549-565.
14. Cummings BJ, Head E, Ruehl W, Milgram NW, Cotman CW. 1996. The canine as an animal model of human aging and dementia. Neurobiol Aging 17: 259-268.
15. Czasch S, Paul S, Baumgärtner W. 2006. A comparison of immunohistochemical and silver staining methods for the detection of diffuse plaques in the aged canine brain. Neurobiol Aging 27: 293-305.
16. DalCanto MC, Lipton HL. 1980. Schwann-cell remyelination and recurrent demyelination in the central nervous-system of mice infected with attenuated Theiler's virus. Am J Pathol 98: 101-122.
17. DalCanto MC, Barbano RL. 1984. Remyelination during remission in Theiler's virus infection. Am J Pathol 116: 30-45.
18. Di Bello IC, Dawson MR, Levine JM, Reynold R. 1999. Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesions of the rat brain stem is associated with demyelination rather than inflammation. J Neurocytol 28: 365-381.
19. Donzel-Pérez E, Caballero-Chacón S, Nieto-Sampedro M. 2009. Neurosphere cell differentiation to aldynoglia promoted by olfactory ensheathing cell conditioned medium. Glia 57: 1393-1409.
20. Dore-Duffy P. 2008. Pericytes: pluripotent cells of the blood brain barrier. Curr Pharm Des 14: 1581-1593.
21. Fleming JC, Norenberg MD, Ramsay DA, Dekaban GA, Marcillo AE, Saenz AD, Pasquale-Styles M, Dietrich WD, Weaver LC. 2006. The cellular inflammatory response in human spinal cords after injury. Brain 129: 3249-3469.
22. Franklin RJ, Blakemore WF. 1993. Requirements for Schwann cell migration within CNS environments: A viewpoint. Int J Dev Neurosci 11: 641-649.
23. Gerhart DZ, Drewes LR. 1987. Butyrylcholinesterase in pericytes associated with canine brain capillaries. Cell Tissue Res 247: 533-536.
24. 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.
25. Gudiño-Cabrera G, Nieto-Sampedro M. 1999. Estrogen receptor immunoreactivity in Schwann-like brain macroglia. J Neurobiol 40: 458-470.
26. Gudiño-Cabrera G, Nieto-Sampedro M. 2000. Schwann-like macroglia in adult rat brain. Glia 30: 49-63.
27. Hafler DA, Slavik JM, Anderson DE, O'Connor KC, De Jager P, Baecher-Allan C. 2005. Multiple sclerosis. Immunol Rev 204: 208-231.
28. Hanbury R, Charles V, Chen EY, Leventhal L, Rosenstein JM, Mufson EJ, Kordower JH. 2002. Excitotoxic and metabolic damage to the rodent striatum: Role of the p75 Neurotrophin receptor and glial progenitors. J Comp Neurol 444: 291-305.
29. Heimrich B, Frotscher M. 1993. Slice cultures as a model to study entorhinal-hippocampal interaction. Hippocampus 3 Spec No: 11-17.
30. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Evercooren AB, Chambon P, Ffrench-Constant C, Franklin RJ. 2011. Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14: 45-53.
31. Jeffery ND, Lakatos A, Franklin RJ. 2005. Autologous olfactory glial cell transplantation is reliable and safe in naturally occurring canine spinal cord injury. J Neurotrauma 22: 1282-1293.
32. Jeffery ND, Smith PM, Lakatos A, Ibanez C, Ito D, Franklin RJM. 2006. Clinical canine spinal cord injury provides an opportunity to examine the issues in translating laboratory techniques into practical therapy. Spinal Cord 44: 584-593.
33. Jessen KR, Mirsky R. 2002. Signals that determine Schwann cell identity. J Anat 200: 367-376.
34. Kawaja MD, Gage FH. 1991. Nerve growth factor receptor immunoreactivity in the rat septohippocampal pathway: A light and electron microscope investigation. J Comp Neurol 307: 517-529.
35. Krueger M, Bechmann I. 2010. CNS pericytes: Concepts, misconceptions, and a way out. Glia 58: 1-10.
36. Küst B, Mantingh-Otter I, Boddeke E, Copray S. 2006. Deficient p75 low-affinity neurotrophin receptor expression does alter the composition of cellular infiltrate in experimental autoimmune encephalomyelitis in C57BL/6 mice. J Neuroimmunol 174: 92-100.
37. Lambertsen KL, Clausen BH, Fenger C, Wulf H, Owens T, Dagnaes-Hansen F, Meldgaard M, Finsen B. 2007. Microglia and macrophages express tumor necrosis factor receptor p75 following middle cerebral artery occlusion in mice. Neuroscience 144: 934-949.
38. Lassmann H. 1983. Comparative neuropathology of chronic experimental autoimmune encephalomyelitis and multiple sclerosis. Schriftenreihe Neurologie, 1st ed, Berlin, Deutschland: Springer, 25. pp 1-135.
39. Lassmann H, Brück W, Lucchinetti C. 2007. The immunopathology of multiple sclerosis: an overview. Brain Pathol 17: 210-218.
40. Liu Y, Rao MS. 2004. Glial progenitors in the CNS and possible lineage relationships among them. Biol Cell 96: 279-290.
41. Louis JC, Magal E, Muir D, Manthorpe M, Varon S. 1992. CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J Neurosci Res 31: 193-204.
42. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26: 7907-7918.
43. Meinecke DL, Rakic P. 1993. Low-affinity p75 nerve growth factor receptor expression in the embryonic monkey telencephalon: Timing and localization in diverse cellular elements. Neuroscience 54: 105-116.
44. Mrzljak L, Goldman-Rakic PS. 1993. Low-affinity nerve growth factor receptor (p75NGFR)-and choline acetyltransferase (ChAT)-immunoreactive axons in the cerebral cortex and hippocampus of adult macaque monkeys and humans. Cereb Cortex 3: 133-147.
45. Mirsky M, Jessen KR. 2005. Molecular signaling in Schwann cell development. In: Dyck PJ, Thomas PK, editors. Peripheral neuropathy, 4th ed. Saunders: Elsevier. pp 341-376.
46. Nataf S, Naveilhan P, Sindji L. Darcy F, Brachet P, Montero-Menei CN. 1998. Low affinity NGF receptor expression in the central nervous system during experimental allergic encephalomyelitis. J Neurosci Res 52: 83-92.
47. Naumann T, Deller T, Bender R, Frotscher M. 1997. 192 IgG-saporin-induced loss of cholinergic neurons in the septum abolishes cholinergic sprouting after unilateral entorhinal lesion in the rat. Eur J Neurosci 9: 1304-1313.
48. Neumann H, Kotter MR, Franklin RJM. 2009. Debris clearance by microglia: An essential link between degeneration and regeneration. Brain 132: 288-295.
49. Nieto-Sampedro M. 2002. CNS Schwann-like glia and functional restoration of damaged spinal cord. Prog Brain Res 136: 303-318.
50. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB. 1996. Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. J Neurosci Res 43: 315-330.
51. Oderfeld-Nowak B, Zaremba M, Micera A, Aloe L. 2001. The upregulation of nerve growth factor receptors in reactive astrocytes of rat spinal cord during experimental autoimmune encephalomyelitis. Neurosci Lett 308: 165-168.
52. Oderfeld-Nowak B, Orzylowska-Sliwinska O, Soltys Z, Zaremba M, Januszewski S, Janeczko K, Mossakowski M. 2003. Concomitant up-regulation of astroglial high and low affinity nerve growth factor receptors in the CA1 hippocampal area following global transient cerebral ischemia in rat. Neuroscience 120: 31-40.
53. Omar M, Bock P, Kreutzer R, Ziege S, Imbschweiler I, Hansmann F, Peck CT, Baumgärtner W, Wewetzer K. 2011. Defining the morphological phenotype: 2'-3'-cyclic nucleotide 3'-phopshodiesterase (CNPase) is a novel marker for in situ detection of canine but not olfactory ensheathing cells. Cell Tissue Res 344: 391-405.
54. Orlando EA, Imbschweiler I, Gerhauser Baumgärtner W, Wewetzer K. 2008. In vitro characterization and preferential infection by canine distemper virus of glial precursors with Schwann cell characteristics from adult canine brain. Neuropathol Appl Neurobiol 34: 621-637.
55. Petratos S, Gonzales MF, Azari MF, Marriott M, Minichiello RA, Shipham KA, Profyris C, Nicolaou A, Boyle K, Cheema SS, Kilpatrick TJ. 2004. Expression of the low-affinity neurotrophin receptor, p75(NTR), is upregulated by oligodendroglial progenitors adjacent to the subventricular zone in response to demyelination. Glia 48: 64-75.
56. Popovich PG, Stokes BT, Whitacre CC. 1996. Concept of autoimmunity following spinal cord injury: Possible roles for T lymphocytes in the traumatized central nervous system. J Neurosci Res 45: 349-363.
57. Pringle NP, Mudhar HS, Collarini EJ, Richardson WD. 1992. PDGF receptors in the rat CNS: During late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115: 535-551.
58. Pringproa K;Kumnok J;Ulrich R, Baumgärtner W, Wewetzer K. 2008. In vitro characterization of a murine oligodendrocyte precursor cell line (BO-1) following spontaneous immortalization. Int J Dev Neurosci 26: 283-291.
59. Risling M, Fried K, Lindå H, Cullheim S, Meier M. 1992. Changes in nerve growth factor receptor-like immunoreactivity in the spinal cord after ventral funiculus lesion in adult cats. J Neurocytol 21: 79-93.
60. Schmitt AB, Buss A, Breuer S, Brook GA, Pech K, Martin D, Schoenen J, Noth J, Love S, Schröder JM, Kreutzberg GW, Nacimiento W. 2000. Major histocompatibility complex class II expression by activated microglia caudal to lesions of descending tracts in the human spinal cord is not associated with a T cell response. Acta Neuropathol 100: 528-536.
61. Shields SA, Blakemore WF, Franklin RJ. 2000. Schwann cell remyelination is restricted to astrocyte-deficient areas after transplantation into demyelinated adult rat brain. J Neurosci Res 60: 571-578.
62. Seehusen F, Orlando EA, Wewetzer K, Baumgärtner W. 2007. Vimentin-positive astrocytes in canine distemper: A target for canine distemper virus especially in chronic demyelinating lesions? Acta Neuropathol 114: 597-608.
63. Seehusen F, Baumgärtner W. 2010. Axonal pathology and loss precede demyelination and accompany chronic lesions in a spontaneously occurring animal model of multiple sclerosis. Brain Pathol 20: 551-559.
64. Smith PM, Sim FJ, Barnett SC, Franklin RJ. 2001. SCIP/Oct-6, Krox-20, and desert hedgehog mRNA expression during CNS remyelination by transplanted olfactory ensheathing cells. Glia 36: 342-353.
65. Smith PM, Lakatos A, Barnett SC, Jeffery ND, Franklin RJ. 2002. Cryopreserved cells isolated from the adult canine olfactory bulb are capable of extensive remyelination following transplantation into the adult rat CNS. Exp Neurol 176: 402-406.
66. Spitzbarth I, Bock P, Haist V, Stein VM, Tipold A, Wewetzer K, Baumgärtner W, Beineke A. 2011. Prominent microglial activation in the early proinflammatory immune response in naturally-occurring canine spinal cord injury. J Neuropathol Exp Neurol 70: 703-714.
67. Soltys Z, Janeczko K, Orzylowska-Sliwinska O, Zaremba M, Januszewski S, Oderfeld-Nowak B. 2003. Morphological transformations of cells immuno-positive for GFAP, TrkA or p75 in the CA1 hippocampal area following transient global ischemia in the rat. A quantitative study. Brain Res 987: 186-193.
68. Stemple DL, Anderson DJ. 1991. A Schwann cell antigen recognized by monoclonal antibody 217c is the rat low-affinity nerve growth factor receptor. Neurosci Lett 124: 57-60.
69. Talbott JF, Cao Q, Enzmann GU, Benton RL, Achim V, Cheng XX, Mills MD, Rao MS, Whittemore SR. 2006. Schwann cell-like differentiation by adult oligodendrocyte precursor cells following engraftment into the demyelinated spinal cord is BMP-dependent. Glia 54: 147-159.
70. 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 enheathing cells in long-term culture. Brain Res 1240: 31-38.
71. Thomas WE. 1999. Brain macrophages: On the role of pericytes and perivascular cells. Brain Res Rev 31: 42-57.
72. Tremere LA, Pinaud R, Grosche J, et al. 2000. Antibody for human p75 LNTR identifies cholinergic basal forebrain of non-primate species. Neuroreport 11: 2177-2183.
73. Turner CP, Perez-Polo JR. 1993. Expression of p75NGFR in the olfactory system following peripheral deafferentation. Neuroreport 4: 1023-1026.
74. 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.
75. Vandevelde M, Zurbriggen A. 2005. Demyelination in canine distemper virus infection: A review. Acta Neuropathol 109: 56-68.
76. 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.
77. Wewetzer K, Verdu E, Angelov DN, Navarro X. 2002. Olfactory ensheathing glia and Schwann cells: Tow of a kind? Cell Tissue Res 309: 337-345.
78. 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.
79. Wewetzer K, Radtke C, Kocsis J, Baumgärtner W. 2011. 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 229: 80-87.
80. Wiggins RC, Benjamins JA, Morell P. 1975. Appearance of myelin proteins in rat sciatic nerve during development. Brain Res 89: 99-106.
81. Woodhoo A, Sommer L. 2008. Development of the Schwann cell lineage: From the neural crest to the myelinated nerve. Glia 56: 1481-1490.
82. Wünschmann A, Alldinger S, Kremmer E, Baumgärtner W. 1999. Identification of CD4+ and CD8+ T cell subsets and B cells in the brain of dogs with spontaneous acute, subacute-, and chronic-demyelinating distemper encephalitis. Vet Immunol Immunopathol 67: 101-116.
83. Young KM, Merson TD, Sotthibundhu A, Coulson EJ, Bartlett PF. 2007. p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells. J Neurosci 27: 5146-5155.
84. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ. 2010. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6: 578-590.
85. Zhu L, Lu J, Tay SS, Jiang H, He BP. 2010. Induced NG2 expressing microglia in the facial motor nucleus after facial nerve axotomy. Neuroscience 166: 842-851.