Journal of Neuroimmunology
Volume 227, Issue 1 , Pages 144-152 , 8 October 2010

Regional topographical differences of canine microglial immunophenotype and function in the healthy spinal cord

  • Eva-Maria Ensinger

      Affiliations

    • Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Bünteweg 9, D-30559 Hannover, Germany
    • These authors contributed equally to the publication.
  • ,
  • Theda M.A. Boekhoff

      Affiliations

    • Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Bünteweg 9, D-30559 Hannover, Germany
    • These authors contributed equally to the publication.
  • ,
  • Regina Carlson

      Affiliations

    • Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Bünteweg 9, D-30559 Hannover, Germany
  • ,
  • Andreas Beineke

      Affiliations

    • Department of Pathology, University of Veterinary Medicine Hannover, Bünteweg 17, D-30559 Hannover, Germany
  • ,
  • Karl Rohn

      Affiliations

    • Institute of Biometry, Epidemiology, and Information Processing, University of Veterinary Medicine Hannover, Bünteweg 2, D-30559 Hannover, Germany
  • ,
  • Andrea Tipold

      Affiliations

    • Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Bünteweg 9, D-30559 Hannover, Germany
  • ,
  • Veronika M. Stein

      Affiliations

    • Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Bünteweg 9, D-30559 Hannover, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 511 953 6202; fax: +49 511 953 6204.

Received 22 April 2010 ,Revised 7 July 2010 ,Accepted 20 July 2010.

References 

  1. Akiyama H, McGeer PL. Brain microglia constitutively express beta-2 integrins. J. Neuroimmunol. 1990;30:81–93
  2. Alldinger S, Wünschmann A, Baumgärtner W, Voss C, Kremmer E. Up-regulation of major histocompatibility complex class II antigen expression in the central nervous system of dogs with spontaneous canine distemper virus encephalitis. Acta Neuropathol. 1996;92(3):273–280
  3. Aloisi F. Immune function of microglia. Glia. 2001;36:165–179
  4. Aloisi F, De Simone R, Columba-Cabezas S, Penna G, Adorini L. Functional maturation of adult mouse resting microglia into APC is promoted by granulocyte macrophage colony-stimulating factor and interaction with Th1 cells. J. Immunol. 2000;164(4):1705–1712
  5. Banati RB, Gehrmann J, Schubert P, Kreutzberg GW. Cytotoxicity of microglia. Glia. 1993;7:111–118
  6. Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunology. 1998;93(2):139–148
  7. Bußhoff U, Hein A, Iglesias A, Dörries R, Régnier-Vigouroux A. CD1c expression is differentially regulated by microglia, macrophages and T-cells in the central nervous system upon inflammation and demyelination. J. Neuroimmunol. 2001;113:220–230
  8. Carson MJ, Reilly CR, Sutcliffe JG, Lo D. Mature microglia resemble immature antigen-presenting-cells. Glia. 1998;22:72–85
  9. Colton CA, Gilbert DL. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett. 1987;223(2):284–288
  10. De Haas AH, Boddeke HWGM, Brouwer N, Biber K. Optimized isolation enables ex vivo analysis of microglia from various central nervous system regions. Glia. 2007;55:1374–1384
  11. De Haas AH, Boddeke HWGM, Biber K. Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia. 2008;56(8):888–894
  12. Del Rio-Hortega P. Microglia. In:  Penfield EW editors. Cytology and Cellular Pathology of the Nervous System. New York: Hoeber; 1932;p. 481–534
  13. Emmendörffer A, Hecht M, Lohmann-Matthes M-L, Roesler J. A fast and easy method to determine the production of reactive oxygen intermediates by human and murine phagocytes using dihydrorhodamine 123. J. Immunol. Meth. 1990;131:269–275
  14. Falcioni T, Manti A, Boi P, Canonico B, Balsamo M, Papa S. Comparison of disruption procedures for enumeration of activated sludge floc bacteria by flow cytometry. Cytom. B Clin. Cytom. 2006;70B:149–153
  15. Ford AL, Goodsall AL, Hickey WF, Sedgwick JD. Normal adult ramified microglia separated from other central nervous system macrophages by flow cytometric sorting. J. Immunol. 1995;154:4309–4321
  16. Gehrmann J, Kreutzberg GW. Microglia in experimental neuropathology. In:  Kettenmann H,  Ransom BR editor. Neuroglia. New York, Oxford: Oxford University Press; 1995;p. 883–904
  17. Gehrmann J, Matsumoto Y, Kreutzberg GW. Microglia: intrinsic immuneffector cell of the brain. Brain Res. Rev. 1995;20:269–287
  18. Gödde T, Jaggy A. Thorakolumbaler Bandscheibenvorfall beim Dackel (Diagnose und Therapie). Prakt. Tierarzt. 1993;7:653–663
  19. Goings GE, Kozlowski DA, Szele FG. Differential activation of microglia in neurogenic versus non-neurogenic regions of the forebrain. Glia. 2006;54(4):329–342
  20. Gudi V, Moharregh-Khabiani D, Skripuletz T, Koutsoudaki PN, Kotsiari A, Skuljec J, et al. Regional differences between grey and white matter in cuprizione induced demyelination. Brain Res. 2009;1283:127–138
  21. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007;10:1387–1394
  22. Havenith CEG, Askew D, Walker WS. Mouse resident microglia: isolation and characterization of immunoregulatory properties with naive CD4+ and CD8+ T-cells. Glia. 1998;22:348–359
  23. Jeffery ND, Smith PM, Lakatos A, Ibanez C, Ito D, Franklin RJM. Clinical canine spinal cord injury provides an opportunity to examine the issues in translating laboratory techniques into practical therapy. Spinal Cord. 2006;44:584–593
  24. Kim S, Cho SH, Kim KY, Shin KY, Kim HS, Park CH, et al. Alpha-synuclein induces migration of BV-2 microglial cells by up-regulation of CD44 and MT1-MMP. J. Neurochem. 2009;109:1483–1496
  25. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19:312–318
  26. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience. 1990;39(1):151–170
  27. Ling EA. Study in the changes of the proportions and numbers of various glial cell types in the spinal cord of neonatal and young adult rats. Acta Anat. 1976;96(2):188–195(Basel)
  28. Liu B, Wang K, Gao H-M, Mandavilli B, Wang J-Y, Hong J-S. Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J. Neurochem. 2001;77:182–189
  29. McCluskey LP, Lampson LA. Local immune regulation in the central nervous system by substance P vs. glutamate. J. Neuroimmunol. 2001;116(2):136–146
  30. Mittelbronn M, Dietz K, Schluesener HJ, Meyermann R. Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude. Acta Neuropathol. 2001;101(3):249–255
  31. Nakamura Y. Regulating factors for microglial activation. Biol. Pham. Bull. 2002;25(8):945–953
  32. Nickel R, Schummer A, Seiferle E. In: Lehrbuch der Anatomie der Haustiere, Band I, 6. Auflage. Berlin und Hamburg, Deutschland: Verlag Paul Parey; 1992;p. 133–147
  33. Perry VH. A revised view of the central nervous system microenvironment and major histocompatibility complex class II antigen presentation. J. Neuroimmunol. 1998;90:113–121
  34. Perry VH, Gordon S. Macrophages and the nervous system. Int. Ref. Cytol. 1991;125:203–244
  35. Perry VH, Matyszak MK, Fearn S. Altered antigen expression of microglia in the aged rodent CNS. Glia. 1993;7:60–67
  36. Phillips LM, Simon PJ, Lampson LA. Site-specific immune regulation in the brain: differential modulation of major histocompatibility complex (MHC) proteins in brainstem vs. hippocampus. J. Comp. Neurol. 1999;405(3):322–333
  37. Popovich PG. Role of microglia and macrophages in secondary injury of the traumatized spinal cord: troublemakers or scapegoats?. In:  Streit WJ editors. Microglia in the Regenerating and Degenerating Central Nervous System. New York, Inc.: Springer-Verlag; 2002;p. 152–165
  38. Purdy PD, White CL, Baer DL, Frawley WH, Reichard RR, Pride GL, et al. Percutaneous translumbar spinal cord compression injury in dogs from an angioplasty balloon: MR and histopathologic changes with balloon sizes and compression times. Am. J. Neuroradiol. 2004;25(8):1435–1442
  39. Raivich G, Bohatschek M, Kloss C, Werner A, Jones L, Kreutzberg W. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res. Rev. 1999;30:77–105
  40. Rezaie P, Male D. Colonisation of the developing human brain and spinal cord by microglia: a review. Microsc. Res. Tech. 1999;45(6):359–382
  41. Rongzhu L, Suhua W, Guangwei X, Chunlan R, Fangan H, Suxian C, et al. Effects of acrylonitrile on antioxidant status of different brain regions in rats. Neurochem. Int. 2009;55:552–557
  42. Satoh J, Lee YB, Kim SU. T-cell costimulatory molecules B7-1 (CD80) and B7-2 (CD86) are expressed in human microglia but not in astrocytes in culture. Brain Res. 1995;704:92–96
  43. Schnell L, Fearn S, Klassen H, Schwab M, Perry H. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 1999;11:3648–3658
  44. Sedgwick JD, Schwender S, Imrich H, Dörries R, Butcher GW, ter Meulen V. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc. Natl Acad. Sci. 1991;88:7438–7442
  45. Somberg RL, Robinson JP, Felsburg PJ. Detection of canine interleukin-2 receptors by flow cytometry. Vet. Immunol. Immunopathol. 1992;33:17–24
  46. Stein VM, Czub M, Hansen R, Leibold W, Moore PF, Zurbriggen A, et al. Characterization of canine microglial cells isolated ex vivo. Vet. Immunol. Immunopathol. 2004;99:73–85
  47. Stirling DP, Yong VW. Dynamics in the inflammatory response after murine spinal cord injury revealed by flow cytometry. J. Neurosci. Res. 2008;86(9):1944–1958
  48. Stoll G, Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog. Neurobiol. 1999;58:233–247
  49. Stoll M, Capper D, Dietz K, Warth A, Schleich A, Schlaszus H, et al. Differential micoglial regulation in the human spinal cord under normal and pathological conditions. Neuropathol. Appl. Neurobiol. 2006;32(6):650–661
  50. Streit WJ. Microglial cells. In:  Kettenmann H,  Ransom BR editor. Neuroglia. New York: Oxford Univ. Press; 1995;p. 85–97
  51. Streit WJ. Microglia as neuroprotective immunocompetent cells of the CNS. Glia. 2002;40:133–139
  52. Streit WJ. Microglia senescence: does the brain's immune system have an expiration date?. Trends Neurosci. 2006;29(9):506–510
  53. Sullivan PG, Rabchevsky AG, Keller JN, Lovell M, Sodhi A, Hart RP, et al. Intrinsic differences in brain and spinal cord mitochondria: implication for therapeutic interventions. J. Comp. Neurol. 2004;474:524–534
  54. Ulevitch RJ, Tobias PS. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 1995;13:437–457
  55. Ulvestad E, Williams K, Bjerkvig R, Tiekotter K, Antel J, Matre R. Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J. Leuk. Biol. 1994;56:732–740
  56. Vass K, Lassmann H. Intrathecal application of interferon gamma. Progressive appearance of MHC antigens within the rat nervous system. Am. J. Pathol. 1990;137(4):789–800
  57. Williams K, Bar-Or A, Ulvestad E, Olivier A, Antel JP, Yong VW. Biology of adult human microglia in culture: comparison with peripheral blood monocytes and astrocytes. J. Neuropathol. Exp. Neurol. 1992;51(5):538–549
  58. Williams K, Ulvestad E, Antel JP. B7/BB-1 antigen expression on adult human microglia studied in vitro and in situ. Eur. J. Immunol. 1994;24:3031–3037
  59. Wunderli PS, Felsburg PJ. An improved method for the isolation of enriched canine peripheral blood mononuclear cell and peripheral blood lymphocyte preparations. Vet. Immunol. Immunopathol. 1989;20(4):335–344

PII: S0165-5728(10)00330-9

doi: 10.1016/j.jneuroim.2010.07.017

Journal of Neuroimmunology
Volume 227, Issue 1 , Pages 144-152 , 8 October 2010