Abstract
This report deals with the distribution, morphology and specific topical relationships of bone-marrow-derived cells (free cells) in the spinal meninges and dorsal root ganglia of the normal rat. The morphology of these cells has been studied by transmission and scanning electron microscopy. Cells expressing the major histocompatibility complex (MHC) class II gene product have been recognized by immunofluorescence. At the level of the transmission electron microscope, free cells are found in all layers of the meninges. Many of them display characteristic ultrastructural features of macrophages, whereas others show a highly vacuolated cytoplasm and are endowed with many processes. These elements lack a conspicuous lysosomal system and might represent dendritic cells. Scanning electron microscopy has revealed that free cells contact the cerebrospinal fluid via abundant cytoplasmic processes that cross the cell layers of the pia mater and of the arachnoid. Cells expressing the MHC class II antigen are also found in all layers of the meninges. They are particularly abundant in the layers immediately adjacent to the subarachnoid space, in the neighbourhood of dural vessels, along the spinal roots and in the dural funnels. In addition to the meninges, strong immunoreactivity for MHC class II antigen is observed in the dorsal root ganglia. The ultrastructural and immunohistochemical findings of this study suggest the existence of a well-developed system of immunological surveillance of the subarachnoid space and of the dorsal root ganglia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Annu Rev Immunol 2:283–318
Auger MJ, Ross JA (1992) The biology of the macrophage. In: Lewis CE, McGee JO'D (eds) The macrophage: the natural immune system. Oxford University Press, Oxford New York Tokyo, pp 1–74
Austyn JM (1987) Lymphoid dendritic cells. Immunology 62:161–170
Barker CF, Billingham RE (1977) Immunologically privileged sites. Adv Immunol 25:1–54
Benacerraf B (1981) Role of MHC gene products in immune regulation. Science 212:1229–1238
Biondi G (1934) Zur Histopathologie des menschlichen Plexus chorioideus und des Ependyms. Arch Psychiatr Nervenkr 101:666–728
Bleier R, Siggelkow I, Albrecht R (1982) Macrophages of hypothalamic third ventricle. J Neuropathol Exp Neurol 41:315–329
Carpenter SJ, McCarthy LE, Borison HL (1970) Electron microscopic study on the epiplexus (Kolmer) cells of the cat choroid plexus. Z Zellforsch 110:471–486
Chazal J, Vanneuville G, Scheye T, Guillot M (1989) Mise au point sur la résorption lymphatique du liquide cérébrospinal après revue de la littérature. Bull Assoc Anat (Nancy) 73:43–46
Fraher JP, McDougall RD (1975) Macrophages related to leptomeninges and ventral nerve roots. An ultrastructural study. J Anat 120:537–549
Frei K, Siepl C, Groscurth P, Bodmer S, Schwerdel C, Fontana A (1987) Antigen presentation and tumor cytotoxicity by interferon-γ-treated microglial cells. Eur J Immunol 17:1271–1278
Frei K, Siepl C, Groscurth P, Bodmer S, Fontana A (1988) Immunobiology of microglial cells. Adv Neuroimmunol 540:218–227
Gracber MB, Streit WJ, Büringer D, Sparks DL, Kreutzberg GW (1992) Ultrastructural location of major histocompatibility complex (MHC) class II positive perivascular cells in histologically normal human brain. J Neuropathol Exp Neurol 51:303–311
Hickey WF (1990) T-lymphocyte entry and antigen recognition in the central nervous system. In: Ader RA, Feletn D, Cohen N (eds) Psychoneuroimmunology, 2nd edn. Academic Press, New York, pp 149–175
Hickey WF (1991) Migration of hematogeneous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol 1:97–105
Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290–292
Hickey WF, Vass K, Lassmann H (1992) Bone marrow-derived elements in the central nervous system: an immunohistochemical and ultrastructural survey of rat chimeras. J Neuropathol Exp Neurol 51:246–256
Janeway CA, Bottomly K, Babich J, Conrad P, Conzen S, Jones B, Kaye J, Katz M, McVay L, Murphy DB, Tite J (1984) Quantitative variation in Ia antigen expression plays a central role in immune regulation. Immunol Today 5:99–105
Jordan FL, Thomas WE (1988) Brain macrophages: questions of origin and interrelationship. Brain Res Rev 13:165–178
Keller JT, Marfurt CF (1991) Peptidergic and serotoninergic innervation of the rat dura mater. J Comp Neurol 309:515–534
Kolmer W (1921) Über eine eigenartige Beziehung von Wanderzellen zu den Chorioidealplexus des Gehirns der Wirbeltiere. Anat Anz 54:15–19
Krahn V (1981) Leukodiapedesis and leukocyte migration in the leptomeninges and in the subarachnoid space. J Neurol 226:43–52
Malloy JJ, Low FN (1976) Scanning electron microscopy of the subarachnoid space in the dog. J Comp Neurol 167:257–284
Merker G (1972) Einige Feinstrukturbefunde an den Plexus chorioidei von Affen. Z Zellforsch 134:565–584
Meyermann R, Lampert PW, Korr H, Wekerle H (1987) The bloodbrain barrier-a strict border to lymphoid cells? Stroke Microcirc 289–296
Morse DE, Low FN (1972) The fine structure of subarachnoid macrophages in the rat. Anat Rec 174:469–476
Nong YH, Titus RG, Ribeiro JM, Remold HG (1989) Peptides encoded by the calcitonin gene inhibit macrophage function. J Immunol 143:45–49
Peck R (1987) Neuropeptides modulating macrophage function. Ann NY Acad Sci 496:264–270
Perry VH, Gordon S (1988) Macrophages and microglia in the nervous system. Trends Neurosci 11:273–277
Perry VH, Gordon S (1991) Macrophages and the nervous system. Int Rev Cytol 125:203–244
Phipps RP, Roper RL, Stein SH (1989) Alternative antigen presentation pathways: accessory cells which down-regulate immune responses. Reg Immunol 2:326–339
Rio Hortega del P (1932) Microglia. In: Penfield WG (ed) Cytology and cellular pathology of the nervous system. Hoeber, New York, pp 482–534
Romani N, Schuler G (1989) Structural and functional relationships between epidermal Langerhans cells and dendritic cells. Res Immunol 140:895–898
Steinman RM (1991) The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271–296
Streit WJ, Graeber MB, Kreutzberg GW (1989) Expression of la antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury. Exp Neurol 105:115–126
Sturrock RR (1988) An ultrastructural study of the development of leptomeningeal macrophages in the mouse and rabbit. J Anat 156:207–215
Thomas WE (1992) Brain macrophages: evaluation of microglia and their function. Brain Res Rev 17:61–74
Usui M, Aoki I, Sunshine GH, Dorf ME (1984) A role for macrophages in suppressor cell induction. J Immunol 132:1728–1734
Williams AE, Blakemore WF (1990) Monocyte-mediated entry of pathogens into the central nervous system. Neuropathol Appl Neurobiol 16:377–392
Williamson JSP, Bradley D, Wayne Streilein J (1989) Immunoregulatory properties of bone marrow-derived cells in the iris and ciliary body. Immunology 67:96–102
Zenker W, Rinne B, Bankoul S, Le Hir M, Kaissling B (1992) 5′-Nucleotidase in spinal meningeal compartments in the rat. Histochemistry 98:135–139
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Braun, J.S., Kaissling, B., Le Hir, M. et al. Cellular components of the immune barrier in the spinal meninges and dorsal root ganglia of the normal rat: immunohistochemical (MHC class II) and electron-microscopic observations. Cell Tissue Res 273, 209–217 (1993). https://doi.org/10.1007/BF00312822
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00312822