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Markers of Central Nervous System Glia and Neurons In Vivo During Normal and Pathological Conditions

  • J. M. Redwine
  • C. F. Evans
Chapter
  • 99 Downloads
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 265)

Abstract

Cell markers are valuable tools for examining the function of cells in normal conditions as well as during disease and repair processes. In fact, our understanding of the cell types that make up the central nervous system (CNS) is very much shaped by the markers available to identify them. CNS cell types were originally identified by morphology. The discovery of various proteins specific to certain cells led to the production of cell-type-specific antibodies that have been used to identify cells in situ. An ideal marker is specific to a given cell type in normal conditions and/or during conditions involving injury or disease. As simple as these criteria sound, they are not easy to fulfill. Markers can be expressed on more that one cell type. Astrocytes and olfactory-tract-ensheathing glia both express glial fibrillary acidic protein (GFAP), even though they have clear phe-notypic, anatomical, and functional differences (Ramon-Cueto and Valverde 1995). Also, a marker that is specific for a given cell type in normal conditions can be induced or up-regulated on other cell types during conditions such as inflammation, disease, or injury. Therefore cell type markers alone do not always conclusively identify a cell type.

Keywords

Myelin Sheath Adult Central Nervous System Central Nervous System Inflammation Oligodendrocyte Progenitor Mature Oligodendrocyte 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Acarin L, Vela JM, Gonzales B, Castallano B (1994) Demonstration of poly-JV-acetyl lactosamine residues in amoeboid and ramified microglial cells in rat bfain by tomato lectin binding. J Histochem Cytochem 42:1033–1041PubMedCrossRefGoogle Scholar
  2. Adams CW, Poston RN (1990) Macrophage histology in paraffin-embedded multiple sclerosis plaques is demonstrated by the monoclonal pan-macrophage marker HAM-56: correlation with chronicity of the lesion. Acta Neuropathol (Berl 80:208–11CrossRefGoogle Scholar
  3. al-Ali SY, al-Hussain SM (1996) An ultrastructural study of the phagocytic activity of astrocytes in adult rat brain. J Anat 188:257–62Google Scholar
  4. Andjelkovic AV, Nikolic B, Pachter JS, Zecevic N (1998) Macrophages/microglial cells in human central nervous system during development: an immunohistochemical study. Brain Res 814:13–25PubMedCrossRefGoogle Scholar
  5. Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11:805–15PubMedCrossRefGoogle Scholar
  6. Bar-Or A, Oliveira EM, Anderson DE, Hafler DA (1999) Molecular pathogenesis of multiple sclerosis. J Neuroimmunol 100:252–259PubMedCrossRefGoogle Scholar
  7. Barnett SC, Franceschini IA (1999) Adhesion molecule expression and phenotype of glial cells in the olfactory tract. Adv Exp Med Biol 468:297–307PubMedCrossRefGoogle Scholar
  8. Bechmann I, Nitsch R (1997) Astrocytes and microglial cells incorporate degenerating fibers following entorhinal lesion: a light, confocal, and electron microscopical study using a phagocytosis-dependent labeling technique. Glia 20:145–54PubMedCrossRefGoogle Scholar
  9. Beller DI, Springer TA, Schreiber RD (1982) Anti mac-1 selectively inhibits the mouse and human type three complement receptor. J Exp Med 156:1000–1009PubMedCrossRefGoogle Scholar
  10. Benkovic SA, Connor JR (1993) Ferritin, transferrin, and iron in selected regions of the adult and aged rat brain. J Comp Neurol 338:97–113PubMedCrossRefGoogle Scholar
  11. Bezzi P, Vesce S, Panzarasa P, Volterra A (1999) Astrocytes as active participants of glutamatergic function and regulators of its homeostasis. Adv Exp Med Biol 468:69–80PubMedCrossRefGoogle Scholar
  12. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in Oligodendroglia. Glia 17:169–74PubMedCrossRefGoogle Scholar
  13. Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429–435PubMedCrossRefGoogle Scholar
  14. Birling MC, Roussel G, Nussbaum F, Nussbaum JL (1993) Biochemical and immunohistochemical studies with specific polyclonal antibodies directed against bovine myelin/oligodendrocyte glycoprotein. Neurochem Res 18:937–45PubMedCrossRefGoogle Scholar
  15. Black JA, Waxman SG (1988) The perinodal astrocyte. Glia 1:169–83PubMedCrossRefGoogle Scholar
  16. Carson MJ, Reilly CR, Sutcliffe JG, Lo D (1998) Mature microglia resemble immature antigen-presenting cells. Glia 22:72–85PubMedCrossRefGoogle Scholar
  17. Carson MJ, Reilly CR, Sutcliffe JG, Lo D (1999) Disproportionate recruitment of CD8 + T cells into the central nervous system by professional antigen-presenting cells. Am J Pathol 154:481–94PubMedCrossRefGoogle Scholar
  18. Carson MJ, Sutcliffe JG, Campbell IL (1999) Microglia stimulate naive T-cell differentiation without stimulating T-cell proliferation. J Neurosci Res 55:127–134PubMedCrossRefGoogle Scholar
  19. Chanas-Sacre G, Rogister B, Moonen G, Leprince P (2000) Radial glia phenotype: origin, regulation, and transdifferentiation. J Neurosci Res 61:357–63PubMedCrossRefGoogle Scholar
  20. 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 20:6404–12PubMedGoogle Scholar
  21. Conner JR, Fine RE (1986) The distribution of transferrin immunoreactivity in the rat central nervous system. Brain Res 368:319–328CrossRefGoogle Scholar
  22. Dangond F, Windhagen A, Groves CJ, Hafler DA (1997) Constitutive expression of costimulatory molecules by human microglia and its relevance to CNS autoimmunity. J Neuroimmunol 76:132–138PubMedCrossRefGoogle Scholar
  23. Dawson MR, Levine JM, Reynolds R (2000) NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J Neurosci Res 61:471–479PubMedCrossRefGoogle Scholar
  24. De Simone R, Giampaolo A, Giometto B, Gallo P, Levi G, Peschle C, Aloisi F (1995) The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J Neuropath Exp Neurol 54:175–187PubMedCrossRefGoogle Scholar
  25. Dijkstra CD, Dopp EA, Joling P, Kraal G (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies EDI, ED2 and ED3. Immunology 54:589–99PubMedGoogle Scholar
  26. Dobersen MJ, Hammer JA, Noronha AB, Macintosh TD, Trapp BD, Brady RO, Quarles RH (1985) Generation and characterization of mouse monoclonal antibodies to the myelin-associated glycoprotein (MAG). Neurochem Res 10:499–513PubMedCrossRefGoogle Scholar
  27. Eddleston M, de la Torre JC, Oldstone MBA, LoskutofT DJ, Edgington TS, Mackman N (1993) Astrocytes are the primary source of tissue factor in the murine central nervous system; a role for astrocytes in cerebral hemostasis. J Clin Invest 92:349–358PubMedCrossRefGoogle Scholar
  28. Eglitis MA, Mezey E (1997) Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci USA 94:4080–5PubMedCrossRefGoogle Scholar
  29. Elkabes S, Di Cicco-Bloom EM, Black IB (1996) Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16:2508–21PubMedGoogle Scholar
  30. Evans CF, Horwitz MS, Hobbs MV, Oldstone MB (1996) Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease. J Exp Med 184:2371–84PubMedCrossRefGoogle Scholar
  31. Fedoroff S, Zhai R, Novak JP (1997) Microglia and astroglia have a common progenitor cell. J Neurosci Res 50:477–4186PubMedCrossRefGoogle Scholar
  32. Ffrench-Constant C, Raff MC (1986) Proliferating bipotential glial progenitor cells in adult rat optic nerve. Nature 319:499–502PubMedCrossRefGoogle Scholar
  33. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD (1995) Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. Phenotypic differences defined and direct ex vivo antigen presentation to myelin basic protein-reactive CD4+ T cells compared. J Immunol 154:4309–21PubMedGoogle Scholar
  34. Forss-Petter S, Danielson P, Sutcliffe JG (1986) Neuron-specific enolase: complete structure of rat mRNA, multiple transcriptional start sites, and evidence suggesting post-transcriptional control. J Neurosci Res 16:141–56PubMedCrossRefGoogle Scholar
  35. Fox RJ, Levin MC, Jacobson S (1996) Tumor necrosis factor alpha expression in the spinal cord of human T-cell lymphotrophic virus type I associated myelopathy/tropical spastic paraparesis patients. J Neurovirol 2:323–9PubMedCrossRefGoogle Scholar
  36. Franke H, Krugel U, Illes P (1999) P2 receptor-mediated proliferative effects on astrocytes in vivo. Glia 28:190–200PubMedCrossRefGoogle Scholar
  37. Friedman B, Hockfield S, Black JA, Woodruff KA, Waxman SG(1989) In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, Rip. Glia 2:380–390CrossRefGoogle Scholar
  38. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB (2000) Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259–74PubMedCrossRefGoogle Scholar
  39. Gardinier MV, Matthieu JM (1993) Cloning and cDNA sequence analysis of myelin/oligodendrocyte glycoprotein: a novel member of the immunoglobulin gene superfamily. Schweiz Arch Neurol Psychiatr 144:201–7PubMedGoogle Scholar
  40. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immunoeffector cell of the brain. Brain Res Rev 20:269–287PubMedCrossRefGoogle Scholar
  41. Gogate N, Verva L, Zhou J, Milward E, Rusten R, O’Conner M, Kufta C, Kim J, Hudson L, Dubois-Dalq M (1994) Plasticity in the adult human oligodendrocyte lineage. J Neurosci 14:4571–4587PubMedGoogle Scholar
  42. Goldman JE, Reynolds R (1996) A reappraisal of ganglioside GD3 expression in the CNS. Glia 16:291–5PubMedCrossRefGoogle Scholar
  43. Goto S, Korematsu K, Nagahiro S, Ushio Y (1993) Distinct neuronal subset reveals perikaryal imrau-nostaining for synaptophysin (protein p38) in the striatum of rats. Acta Neuropathol (Berl 86:302–5CrossRefGoogle Scholar
  44. Graeber MB, Streit W, Kreutzberg GW (1989) Identity of ED2-positive perivascular cells in rat brain. J Neurosci Res 22:103–106PubMedCrossRefGoogle Scholar
  45. Greer JM, Dyer CA, Pakaski M, Symonowicz C, Lees MB (1996) Orientation of myelin proteolipid protein in the oligodendrocyte cell membrane. Neurochem Res 21:431–40PubMedCrossRefGoogle Scholar
  46. Haan EA, Boss BD, Cowan WM (1982) Production and characterization of monoclonal antibodies against the “brain-specific” proteins 14–3–2 and S-100. Proc Natl Acad Sci USA 79:7585–7589PubMedCrossRefGoogle Scholar
  47. Hart IK, Richardson WD, Heldin CH, Westermark B, Raff MC (1989) PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O 2 A) cell lineage. Development 105:595–603PubMedGoogle Scholar
  48. Harvey AR, Symons NA, Pollett MA, Brooker GJ, Bartlett PF (1997) Fate of adult neural precursors grafted to adult cortex monitored with a Y-chromosome marker. Neuroreport 8:3939–43PubMedCrossRefGoogle Scholar
  49. Hauke C, Korr H (1993) RCA-I lectin histochemistry after trypsinisation enables the identification of microglial cells in thin paraffin sections of the mouse brain. J Neurosci Methods 50:273–7PubMedCrossRefGoogle Scholar
  50. Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin CH, Westermark, Nister M (1992) Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52:3213–3219PubMedGoogle Scholar
  51. Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow derived and present antigen in vivo. Science 239:290–292PubMedCrossRefGoogle Scholar
  52. Hickey WF, Vass K, Lassman H (1992) Bone marrow-derived elements in the central nervous system: an immunohistochemical and ultrastructural survey of rat chimeras. J Neuropathol Exp Neurol 51: 246–256PubMedCrossRefGoogle Scholar
  53. Ho MK, Springer, TA (1982) Mac-1 antigen: quantitative expression in macrophage populations and tissues, and immunofluorescent localization in spleen. J Immunol 128:2281–2286PubMedGoogle Scholar
  54. Holz A, Schaeren-Wiemers N, Schaefer C, Pott U, Colello RJ, Schwab ME (1996) Molecular and developmental characterization of novel cDNAs of the myelin-associated/oligodendrocytic basic protein. J Neurosci 16:467–77PubMedGoogle Scholar
  55. Holz A, Schwab ME (1997) Developmental expression of the myelin gene MOBP in the rat nervous system. J Neurocytol 26:467–477PubMedCrossRefGoogle Scholar
  56. Horwitz MA (1992) Interactions between macrophages and legionella pneumophila. In: Russel SW, Gordon S (eds) Current topics in microbiology and immunology. Springer-Verlag, BerlinGoogle Scholar
  57. Horwitz MS, Evans CF, Klier FG, Oldstone MB (1999) Detailed in vivo analysis of interferon-gamma induced major histocompatibility complex expression in the central nervous system: astrocytes fail to express major histocompatibility complex class I and II molecules. Lab Invest 79:235–42PubMedGoogle Scholar
  58. Horwitz MS, Evans CF, McGavern DB, Rodriguez M, Oldstone MBA (1997) Primary demyelination in transgenic mice expressing interferon-gamma. Nature Med 3:1037–1041PubMedCrossRefGoogle Scholar
  59. Huber G, Matus A (1984) Differences in the cellular distributions of two microtubule-associated proteins, MAPI and MAP2, in rat brain. J Neurosci 4:151–60PubMedGoogle Scholar
  60. Hulette CM, Downey BT, Burger PC (1992) Macrophage markers in diagnostic neuropathology [published erratum appears in Am J Surg Pathol 1992 Oct; 16(10):1029]. Am J Surg Pathol 16:493–9PubMedCrossRefGoogle Scholar
  61. Katz-Levy Y, Neville KL, Girvin AM, Vanderlugt CL, Pope JG, Tan LJ, Miller SD (1999) Endogenous presentation of self myelin epitopes by CNS-resident APCs in Theiler’s virus-infected mice. J Clin Invest 104:599–610PubMedCrossRefGoogle Scholar
  62. Keirstead HS, Levine JM, Blakemore WF (1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22:161–70PubMedCrossRefGoogle Scholar
  63. Krivit W, Sung JH, Shapiro EG, Lockman LA (1995) Microglia: the effector cell for reconstitution of the central nervous system following bone marrow transplantation for lysosomal and peroxisomal storage diseases. Cell Transplant 4:385–92PubMedCrossRefGoogle Scholar
  64. Lampson LA (1995) Interpreting MHC class I expression and class I/classII reciprocity in the CNS: Reconciling divergent findings. Microsc Res Tech 32:267–285PubMedCrossRefGoogle Scholar
  65. Lasser DM, DeVivo DC, Garvin J, Wilhemsen KC(1994) Turcot’s syndrome: evidence for linkage to the adenomatous polyposis coli (APC) locus. Neurology 44:1083–1086PubMedCrossRefGoogle Scholar
  66. Lee SJ, Benveniste EN (1999) Adhesion molecule expression and regulation on cells of the central nervous system. J Neuroimmunol 98:77–88PubMedCrossRefGoogle Scholar
  67. Levi G, Aloisi F, Wilkin GP (1987) Differentiation of cerebellar bipotential glial precursors into oligodendrocytes in primary culture: developmental profile of surface antigens and mitotic activity. J Neurosci Res 18:407–417PubMedCrossRefGoogle Scholar
  68. Levine JM (1994) Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J Neurosci 14:4716–4730PubMedGoogle Scholar
  69. Levine JM, Card JP (1987) Light and electron microscopic localization of a cell surface antigen (NG2) in the rat cerebellum: association with smooth protoplasmic astrocytes. J Neurosci 7:2711–2720PubMedGoogle Scholar
  70. Levine JM, Reynolds R, Fawcett JW (2000) The oligodendrocyte precursor cell in health and disease. TINS (in press)Google Scholar
  71. Levine JM, Stallcup WB (1987) Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci 7:2721–2731PubMedGoogle Scholar
  72. Levine JM, Stincone F, Lee YS (1993) Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7:307–21PubMedCrossRefGoogle Scholar
  73. Levison SW, Goldman JE (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201–212PubMedCrossRefGoogle Scholar
  74. Lewis SA, Lee G-S, Cowan NJ (1985) Five mouse tubulin isotypes and their regulated expression during development. J Cell Biol 101:852–860PubMedCrossRefGoogle Scholar
  75. Ling EA, Wong WC (1993) The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7:9–18PubMedCrossRefGoogle Scholar
  76. Ludwin SK, Kosek JC, Eng LF (1976) The topographical distribution of S-100 and GFA proteins in the adult rat brain: an immunohistochemical study using horseradish peroxidase-labelled antibodies. J Comp Neurol 165:197–208PubMedCrossRefGoogle Scholar
  77. Luskin MB, McDermott K (1994) Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 3:211–226CrossRefGoogle Scholar
  78. Luskin MB, Parnavelas JG, Barfield JA (1993) Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J Neurosci 13:1730–1750PubMedGoogle Scholar
  79. Manoji H, Yeger H, Becher LE (1986) A specific histochemical marker (lectin ricinus communis agglutinin-1) for normal human microglia and application to routine histopathology. Acta Neuropathol 71:341–343CrossRefGoogle Scholar
  80. Marangos PJ, Schmechel D, Zis AP, Goodwin FK (1979) The existence and neurobiological significance of neuronal and glial forms of the glycolytic enzyme enolase. Biol Psychiatry 14:563–79PubMedGoogle Scholar
  81. Marangos PJ, Zis AP, Clark RL, Goodwin FK (1978) Neuronal, non-neuronal and hybrid forms of enolase in brain: structural, immunological and functional comparisons. Brain Res 150:117–33PubMedCrossRefGoogle Scholar
  82. Matsumoto Y, Ohmori K, Fujiwara M (1992) Immune regulation by brain cells in the central nervous system: microglia but not astrocytes present myelin basic protein to encephalitogenic T cells under in vivo-mimicking conditions. Immunol 76:209–216Google Scholar
  83. McFarland HI, Nahill SR, Maciaszek JW, Welsh RM (1992) CD11b (mac-1); a marker for CD8 + cytotoxic T cell activation and memory in virus infection. J Immunol 149:1326–1333PubMedGoogle Scholar
  84. McGarry RC, Helfand SL, Quarles RH, Roder JC (1983) Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1. Nature 306:376–8PubMedCrossRefGoogle Scholar
  85. Mercken M, Lubke U, Vandermeeren M, Gheuens J, Oestreicher AB (1992) Immunocytochemical detection of the growth-associated protein B-50 by newly characterized monoclonal antibodies in human brain and muscle. J Neurobiol 23:309–21PubMedCrossRefGoogle Scholar
  86. Mercken M, Vandermeeren M, Lubke U, Six J, Boons J, Vanmechelen E, Van de Voorde A, Gheuens J (1992) Affinity purification of human tau proteins and the construction of a sensitive sandwich enzyme-linked immunosorbent assay for human tau detection. J Neurochem 58:548–53PubMedCrossRefGoogle Scholar
  87. MesserSmith DJ, Murtie JC, Le TQ, Frost EE, Armstrong RC (2000) Fibroblast growth factor 2 (FGF2) and FGF receptor expression in an experimental demyelinating disease with extensive remyelination. J Neurosci Res 62:241–256CrossRefGoogle Scholar
  88. Miller RH, Zhang H, Fok-Seang J (1994) Glial cell heterogeneity in the mammalian spinal cord. Perspect Dev Neurobiol 2:225–231PubMedGoogle Scholar
  89. Miyake T, Okada M, Kitamura T (1992) Reactive proliferation of astrocytes studied by immunohisto-chemistry for proliferating cell nuclear antigen. Brain Res 590:300–2PubMedCrossRefGoogle Scholar
  90. Morris CS, Esiri MM, Sprinkle TJ, Gregson N (1994) Oligodendrocyte reactions and cell proliferation markers in human demyelinating diseases. Neuropathol Appl Neurobiol 20:272–81PubMedCrossRefGoogle Scholar
  91. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201–11PubMedGoogle Scholar
  92. Muller T, Kettenmann H (1995) Physiology of bergmann glial cells. Int Rev Neurobiol 38:341–359PubMedCrossRefGoogle Scholar
  93. Nagata K, Takei N, Nakajima K, Saito H, Kohsaka S (1993) Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 34:357–63PubMedCrossRefGoogle Scholar
  94. Nishiyama A, Chang A, Trapp BD (1999) NG2+ glial cells: a novel glial cell population in the adult brain. J Neuropathol Exp Neurol 58:1113–24PubMedCrossRefGoogle Scholar
  95. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Co-localization of NG2 proteoglycan and PDGF alpha-receptor on 02 A progenitor cells in the developing rat brain. J Neurosci Res 43:299–314PubMedCrossRefGoogle Scholar
  96. Nishiyama A, Yu M, Drazba JA, Tuohy VK (1997) Normal and reactive NG2+ glial cells are distinct from resting and activated microglia. J Neurosci Res 48:299–312PubMedCrossRefGoogle Scholar
  97. Norton WT (1999) Cell reactions following acute brain injury: a review. Neurochem Res 24:213–8PubMedCrossRefGoogle Scholar
  98. Oumesmar BN, Vignais L, Baron-Van Evercooren A (1997) Developmental expression of platelet-derived growth factor alpha receptor in neurons and glial cells of the mouse CNS. J Neurosci 17:125–139Google Scholar
  99. Pawlinski R, Janeczko K (1997) An inhibitory effect of interferon gamma on the injury-induced astrocyte proliferation in the postmitotic rat brain. Brain Res 773:231–4PubMedCrossRefGoogle Scholar
  100. Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system. Oxford University Press, New YorkGoogle Scholar
  101. Pouly S, Becher B, Blain M, Antel JP (1999) Expression of a homologue of rat NG2 on human microglia. Glia 27:259–68PubMedCrossRefGoogle Scholar
  102. Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, Kinzler KW (1992) APC mutations occur early during colorectal tumorgenesis. Nature 359:235–237PubMedCrossRefGoogle Scholar
  103. Pringle N, Mudhar HS, Collarini EJ, Richardson WD(1992) PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha receptor appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115:535–551PubMedGoogle Scholar
  104. Pringle NP, Richardson WD (1993) A singularity of PDGF alpha receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 115:535–551Google Scholar
  105. Ramon-Cueto A, Valverde F (1995) Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 14:163–173PubMedCrossRefGoogle Scholar
  106. Redwine JM, Armstrong RC (1998) In vivo proliferation of oligodendrocyte progenitors expressing PDGF-alpha receptor during early remyelination. J Neurobiol 37:413–428PubMedCrossRefGoogle Scholar
  107. Redwine JM, Buchmeier MJ, Evans CF (2001) In vivo expression of MHC molecules on oligodendrocytes and neurons during viral infection. Am J Pathol 159:1219–1224PubMedCrossRefGoogle Scholar
  108. Reiser G, Kunzelmann U, Steinhilber G, Binmöller FJ (1994) Generation of a monoclonal antibody against the myelin protein CNP suitable for biochemical and for immunohistochemical investigations of CNP. Neurochem Res 19:1479–1485PubMedCrossRefGoogle Scholar
  109. Reynolds R, Hardy R (1997) Oligodendroglial progenitors labeled with the 04 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 47:455–470PubMedCrossRefGoogle Scholar
  110. Reynolds R, Wilkin GP(1988) Development of macroglial cells in the rat cerebellum II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 102:409–425PubMedGoogle Scholar
  111. Richardson A, Hao C, Fedoroff S (1993) Microglia progenitor cells: a subpopulation on cultures of mouse neopallial astroglia. Glia 7:25–33PubMedCrossRefGoogle Scholar
  112. Rickmann M, Wolff JR (1995) S100 protein expression in subpopulations of neurons of rat brain. Neuroscience 67:977–91PubMedCrossRefGoogle Scholar
  113. Robinson AP, White TM, Mason DW (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57:239–47PubMedGoogle Scholar
  114. Rodriguez M, Pierce ML, Howie EA (1987) Immune response gene products (Ia antigens) on glial and endothelial cells in virus-induced demyelination. J Immunol 138:3438–3442PubMedGoogle Scholar
  115. Schmechel D, Marangos PJ, Zis AP, Brightman M, Goodwin FK (1978) Brain endolases as specific markers of neuronal and glial cells. Science 199:313–5PubMedCrossRefGoogle Scholar
  116. Schumacher U, Adam E, Kretzschmar H, Pfuller U(1994) Binding patterns of mistletoe lectins I, II and III to microglia and Alzheimer plaque glycoproteins in human brains. Acta Histochem 96:399–403PubMedCrossRefGoogle Scholar
  117. Scolding N, Franklin R, Stevens S, Heldin CH, Compston A, Newcombe J (1998) Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 121:2221–8PubMedCrossRefGoogle Scholar
  118. Shaw G, Osborn M, Weber K (1981) An immunofluorescence microscopical study of the neurofilament triplet proteins, vimentin and glial fibrillary acidic protein within the adult rat brain. Eur J Cell Biol 26:68–82PubMedGoogle Scholar
  119. Sheedlo HJ, Sprinkle TJ (1983) The localization of 2’,3’-cyclic nucleotide 3’-phosphodiesterase in bovine cerebrum by immunofluorescence. Brain Res 288:330–333PubMedCrossRefGoogle Scholar
  120. Shine HD, Readhead C, Popko B, Hood L, Sidman RL (1992) Morphometric analysis of normal, mutant, and transgenic CNS: correlation of myelin basic protein expression to myelinogenesis. J Neurochem 58:342–9PubMedCrossRefGoogle Scholar
  121. Sillevis Smitt PA, van der Loos C, Vianney de Jong JM, Troost D (1993) Tissue fixation methods alter the immunohistochemical demonstrability of neurofilament proteins, synaptophysin, and glial fibrillary acidic protein in human cerebellum. Acta Histochem 95:13–21CrossRefGoogle Scholar
  122. Smith KJ, Johnson KA, Bryan TM, Hill DE, Markowitz S, Willson JK, Paraskeva C, Petersen GM, Hamilton SR, Vogelstein B, et al. (1993) The APC gene product in normal and tumor cells. Proc Natl Acad Sci U S A 90:2846–50PubMedCrossRefGoogle Scholar
  123. Sobel RA, Greer JM, Isaac J, Fondren G, Lees MB (1994) Immunolocalization of proteolipid protein peptide 103–116 in myelin. J Neurosci Res 37:36–43PubMedCrossRefGoogle Scholar
  124. Sommer I, Schachner M (1981) Monoclonal antibodies (Ol and 04) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:328–228CrossRefGoogle Scholar
  125. Sorensen T, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM (1999) Expression of specific chemokines and chemo-kine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 103:807–815PubMedCrossRefGoogle Scholar
  126. Stallcup WB (1981) The NG2 antigen, a putative lineage marker: immunofluorescent localization in primary cultures of rat brain. Dev Biol 83:154–165PubMedCrossRefGoogle Scholar
  127. Stallcup WB, Beasley L (1987) Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci 7:2737–2744PubMedGoogle Scholar
  128. Stallcup WB, Beasley L, Levine J (1983) Cell-surface molecules that characterize different stages in the development of cerebellar interneurons. Cold Spr Harbor Symp Quant Biol 48:761–774CrossRefGoogle Scholar
  129. Starkey PM, Turley L, Gordon S (1987) The mouse macrophage-specific glycoprotein defined by monoclonal antibody F4/80: characterization, biosynthesis and demonstration of a rat analogue. Immunology 60:117–22PubMedGoogle Scholar
  130. Sternberger NH, Itoyama Y, Kies MW, deF Webster H (1978) Myelin basic protein demonstrated immunocytochemically in Oligodendroglia prior to myelin sheath formation. Proc Natl Acad Sci USA 75:2521–2524PubMedCrossRefGoogle Scholar
  131. Sternberger NH, Quarles RH, Itoyama Y, deF Webster H (1979) Myelin associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rats. Proc Natl Acad Sci USA 76:1510–1514PubMedCrossRefGoogle Scholar
  132. Streit WJ, Graeber MB, Kreutzberg GW (1988) Functional plasticity of microglia: a review. Glia 1:301–7PubMedCrossRefGoogle Scholar
  133. Streit WJ, Kreitzberg GW (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248–263PubMedCrossRefGoogle Scholar
  134. Streit WJ, Kreutzberg GW (1987) Lectin binding by resting and reactive microglia. J Neurocytol 16: 249–60PubMedCrossRefGoogle Scholar
  135. Stridsberg M, Lundqvist G, Engstrom U, Wilander E, Su H, Gobl A, Oberg K (1994) Development of polyclonal antibodies and evaluation of a sensitive radioimmunoassay for detection and measurement of synaptophysin. Acta Neuropathol (Berl) 87:635–41CrossRefGoogle Scholar
  136. Sun N, Grzybicki D, Castro RF, Murphy S, Perlman S (1995) Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic Coronavirus. Virology 213:482–93PubMedCrossRefGoogle Scholar
  137. Sutcliffe JG, Foye PE, Erlander MG, Hilbush BS, Bodzin LJ, Durham JT, Hasel KW (2000) TOGA: an automated parsing technology for analyzing expression of nearly all genes. Proc Natl Acad Sci USA 97:1976–81PubMedCrossRefGoogle Scholar
  138. Suzuki H, Franz H, Yamamato Y, Iwasaki H, Konno H (1988) Identification of normal microglia population in human and rodent nervous tissue using lectin-histochemistry. J Neuropathol Appl Neurobiol 14:221–227CrossRefGoogle Scholar
  139. Todd AJ, Spike RC, Polgar E (1998) A quantitative study of neurons which express neurokinin-1 or somatostatin sst2a receptor in rat spinal dorsal horn. Neuroscience 85:459–73PubMedCrossRefGoogle Scholar
  140. Trapp BD, Andrews SB, Cootauco C, Quarles R (1989) The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J Cell Biol 109:2417–26PubMedCrossRefGoogle Scholar
  141. Tucker RP, Binder LI, Matus AI (1988) Neuronal microtubule-associated proteins in the embryonic avian spinal cord. J Comp Neurol 271:44–55PubMedCrossRefGoogle Scholar
  142. Ulvestad E, Williams K, Mork S, Antel J, Nyland H (1994) Phenotypic differences between human monocytes/macrophages and microglial cells studied in situ and in vitro. J Neuropathol Exp Neurol 53:492–502PubMedCrossRefGoogle Scholar
  143. Vijayan VK, Lee YL, Eng LF (1990) Increase in glial fibrillary acidic protein following neural trauma. Mol Chem Neuropathol 13:107–18PubMedCrossRefGoogle Scholar
  144. Warschkau H, Kiderlen AF (1999) A monoclonal antibody directed against the nurine macrophage surface molecule F4/80 modulates natural immune response to listeria monocytogenes. J Immunol 163:3409–3416PubMedGoogle Scholar
  145. Wenzel J, Lammert G, Meyer U, Krug M (1991) The influence of long-term potentiation on the spatial relationship between astrocyte processes and potentiated synapses in the dentate gyrus neuropil of rat brain. Brain Res 560:122–31PubMedCrossRefGoogle Scholar
  146. Westergaard N, Sonnewald U, Schousboe A (1995) Metabolic trafficking between neurons and astrocytes: the glutamate/glutamine cycle revisited. Dev Neurosci 17:203–11PubMedCrossRefGoogle Scholar
  147. Whitton JL, Tishon A, Lewicki H, Gebhard J, Cook T, Salvato M, Joly E, Oldstone MB (1989) Molecular analyses of a five-amino-acid cytotoxic T-lymphocyte (CTL) epitope: an immunodominant region which induces nonreciprocal CTL cross-reactivity. J Virol 63:4303–10PubMedGoogle Scholar
  148. Wiedenmann B, Franke WW (1985) Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41:1017–28PubMedCrossRefGoogle Scholar
  149. Williams K, Ulvestad E, Antel JP (1994) B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur J Immunol 24:3031–7PubMedCrossRefGoogle Scholar
  150. Wilson S-S, Baetge EE, Stallcup WB (1980) Antisera specific for cell lines with mixed neuronal and glial properties. Dev Biol 83:146–153CrossRefGoogle Scholar
  151. Wilson S-S, Baetge EE, Stallcup WB (1981) Antisera specific for cell lines with mixed neuronal and glial properties. Dev Biol 83:146–153PubMedCrossRefGoogle Scholar
  152. Wolswijk G, Noble M (1989) Identification of an adult-specific glial progenitor cell. Development 105:387–400PubMedGoogle Scholar
  153. Yamashita N, Ilg EC, Schafer BW, Heizmann CW, Kosaka T (1999) Distribution of a specific calcium-binding protein of the S100 protein family, S100A6 (calcyclin), in subpopulations of neurons and glial cells of the adult rat nervous system. J Comp Neurol 404:235–57PubMedCrossRefGoogle Scholar
  154. Yong VW, Moumdjian R, Yong FP, Ruijs TC, Freedman MS, Cashman N, Antel JP (1991) Gamma-interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo. Proc Natl Acad Sci USA 88:7016–20PubMedCrossRefGoogle Scholar
  155. Zheng-Fischhofer Q, Biernat J, Mandelkow EM, Illenberger S, Godemann R, Mandelkow E (1998) Sequential phosphorylation of Tau by glycogen synthase kinase-3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody ATIOO and requires a paired-helical-filament-like conformation. Eur J Biochem 252:542–52PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • J. M. Redwine
    • 1
  • C. F. Evans
    • 1
  1. 1.Dept. of NeuropharmacologyThe Scripps Research InstituteLa JollaUSA

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