Estrogen and microglia: A regulatory system that affects the brain

Journal of Neurobiology

Volumn 40, Issue 4, 1999, Pages 484-496

  Mor, Gil ^a   Nilsen, Jon ^a   Horvath, Tamas ^a   Bechmann, Ingo ^b   Brown, Santiago ^a   Garcia Segura, Luis Miguel ^c   Naftolin, Frederick ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c INSTITUTO CAJAL   (Spain)

Author keywords

Cytokines; Estrogen; Estrogen receptors; Microglia; Synaptic plasticity

Indexed keywords

CYTOKINE; ESTROGEN; ESTROGEN RECEPTOR; GROWTH FACTOR; SEX HORMONE;

ANTIGEN PRESENTING CELL; BEHAVIOR; CYTOKINE RELEASE; GLIA CELL; IMMUNOREGULATION; MICROGLIA; NERVE CELL PLASTICITY; NEUROENDOCRINE DISEASE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

ANIMALS; BRAIN; ESTROGENS; HUMANS; MICROGLIA; RECEPTORS, ESTROGEN;

EID: 0033567861     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19990915)40:4<484::AID-NEU6>3.0.CO;2-C     Document Type: Review

References (130)

1. Ahmed A, Penhale W, Talal N. 1985a. Sex hormones,immune response and autoimmune disease. Am J Pathol 121:531-551.
2. Ahmed, S, Penhale, W, Talal, N. 1985b. Sex hormones,immune response and autoimmune disease. Am J Pathol 121:531-551.
3. Akiyama H, Itagaki S, McGeer P. 1988. Major histocompatibility complex antigen expression on rat microglia following epidural kainic acid lesions. J Neurosci Res 20:147-157.
4. Akiyama H, McGeer P. 1990. Brain microglia constitutively express β2 integrins. J Neuroimmunol 30:81-93.
5. Al-Din AN, Kurdi A, Mubaidin A, et al. 1996. Epidemiology of multiple sclerosis in Arabs in Jordan: a comparative study between Jordanians and Palestinians. J Neurol Sci 135:162-167.
6. Banati R, Gehrmann J, Schubert P, et al. 1993a. Cytotoxicity of microglia. Glia 7:111-118.
7. Banati R, Schubert P, Rothe G, et al. 1993b. Detection of lysosomal cysteine proteinase in moicroglia: Flow cytometric measurement and histochemical localization of cathepsin B and L. Glia 7:183-191.
8. Bebo BJ, Schuster J, Vandenbark A, et al. 1998. Gender differences in experimental autoimmune encephalomyelitis develop during the induction of the immune response to encephalitogenic peptides. J Neurose Res 52:420-425.
9. Bechmann I, Mor G, Nilsen J, et al. 1999. FasL (CD95L, Apo1L) is expressed in the normal rat and human brain-evidence for the existence of an immunological brain barrier. Glia 27:62-74.
10. 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 labelling technique. Glia 20:145-154.
11. Blinzinger K, Kreutzberg G. 1968. Displacement of synaptic terminals froom regenerating motoneurons by microglial cells. Z Zellforsch 85:145-157.
12. Boya J, Calvo J, Carbonell A, et al. 1991. A lectin histochemistry study on the development of rat microglial cells. J Anat 175:229-236.
13. Boyle E, McGeer P. 1990. Cellular immune response in multple sclerosis plaques. Am J Pathol 137:575-584.
14. Brawer J, Naftolin F, Martin J, et al. 1978. Effects of a single injection of estradiol valerate on the hypothalamic arcuate nucleus and on reproductive function in the female rat. Endocrinology 103:501-512.
15. Brawer J, Schipper H, Naftolin F. 1980. Ovary-dependent degeneration in the hypothalamic arcuate nucleus. Endocrinology 107:274-279.
16. Brawer J, Schipper H, Robaire B. 1983. Effects of long-term androgen and estradiol exposure on the hypothalamus. Endocrinology 112:194-201.
17. Chrousos G. 1995. The hypothalamic-pituitary-adrenal axis amd immune-mediated inflamation. N Engl J Med 332: 1351-1362.
18. Colton A, Gilbert D. 1987. Production of Superoxide by a CNS macrophage, the microglia. FEBS Lett 223:284-288.
19. Cuzner M, Hayes G, Newcombe J, et al. 1988. The nature of inflammatory components during demyelination in multiple sclerosis. J Neuroimmunol 20:203-209.
20. Danel L, Souweine G, Monier J, et al. 1983. Specific estrogen binding sites in human lymphoid cells and thymic cells. J Steroid Biochem Mol Biol 18:559-563.
21. De M, Sanford T, Wood GW. 1993. Relationship between macrophage colony-stimulating factor production by uterine epithelial cells and accumulation and distribution of macrophages in the uterus of pregnant mice. J Leuk Biol 53:240-248.
22. Dickson D, Lee S, Mattiace L, et al. 1993. Microglia and cytokines in neurological disease, with special refernce to AIDS and Alzheimer's disease. Glia 7:75-83.
23. Dickson D, Mattiace L, Kure K, et al. 1991. Microglia in human disease with an emphasis on acquired immune deficiency syndrome. Lab Invest 64:135-156.
24. Dijkstra C, Dopp E, Joling P, et al. 1985. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognised by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589-599.
25. Dunning H, Furth J. 1935. Studies in the relation between microglia, histiocytes and monocytes. Am J Pathol 11: 895-919.
26. Esiri M, Reading M. 1987. Macrophage populations associated with multiple sclerosis plaques. Neuropath Appl Neuro 13:451-465.
27. Flaris N, Densmore T, Molleston M, et al. 1993. Characterization of microglia and macrophages in the central nervous system of rats: definition of the differential expression of molecules using standard and novel monoclonal antibodies in normal CNS and in four models of parenchymal reaction. Glia 7:34-40.
28. Frei K, Siepl C, Groscurth P, et al. 1987. Antigen presentation and tumor cytotoxicity by interferon-γ-treated microglial cells. Eur J Immunol 12:237-243.
29. Garcia-Segura L, Luquin S, Parducz A, et al. 1994. Gonadal hormone regulation of glial fibrillary acidic protein immunoreactivity and glial ultrastructure in the rat neuroendocrine hypothalamus. Glia 10:59-69.
30. Gehrmann J, Bonnekoh P, Miyazawa T, et al. 1992. Immunocytochemical study of an early microglial activation in ischemia. J Cereb Blood Flow Metab 12:257-269.
31. Gehrmann J, Kreutzberg G. 1991. Characterization of two new monoclonal antibodies directed against rat microglia. J Comp Neurol 313:409-430.
32. Gehrmann J, Matsumoto Y, Kreutzberg GW. 1995. Microglia: Intrinsic immuneffector cell of the brain. Brain Res Rev 20:269-287.
33. Gerhmann J, Gold R, Linington C, et al. 1993. Microglial involvement in experimental autoimmune inflammation of the central nervous system. Glia 7:50-59.
34. Ghezzi A, Deplano V, Faroni J, et al. 1997. Multiple sclerosis in childhood: clinical features of 149 cases. Multiple Sclerosis 3:43-46.
35. Giulian D, Baker T. 1986. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163-2178.
36. Giulian D, Baker T. 1985. Peptides released by ameboid microglia regulate astroglial proliferation. J Cell Biol 101:2411-2415.
37. Giulian D, Baker T, Shin L, et al. 1986. Interleukin 1 of the central nervous system is produced by ameboid microglia. J Exp Med 164:594-604.
38. Griffith T, Brunner T, Fletcher S, et al. 1995. Fas ligand induces apoptosis as a mechanism of immune privilege. Science 270:1187-1192.
39. Gulshan S, McCruden A, Stimson W. 1990. Oestrogen receptors in macrophages. Scand J Immunol 31:691-697.
40. Hetier E, Ayala J, Denefle P, et al. 1988. Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J Neurosci Res 21:391-397.
41. Hickey W, Kimura H. 1988. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290-292.
42. Homo-Delarche F, Fitzpatrick F, Christeff N, et al. 1991. Sex steroids, glucocorticoids, stress and autoimmunity. J Steroid Biochem Mol Biol 40:619-637.
43. Ignatius M, Gebicke-Harter P, Skene J, et al. 1986. Expression of apolipoprotein E during nerve degeneration and regeneration. Proc Natl Acad Sci USA 83:1125-1129.
44. Imamoto K, Leblond C. 1978. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J Comp Neurol 180:139-164.
45. Itagaki S, McGeer P, Akiyama H. 1988. Presence of T-cytotoxic suppressor and leukocyte common antigen positive cells in Alzheimer's disease brain tissue. Neurosci Lett 91:259-264.
46. Jansson L, Olsson T, Holmdahl R. 1994. Estrogen induces a potent suppression of experimental autoimmune encephalitis and collagen-induced arthritis in mice. J Neuroimmunol 53:203-207.
47. Jones T, Kennedy R. 1993. Cytokines and hypothalamic-pituitary function. Cytokine 5:531-538.
48. Juba A. 1934. Untersuchungen uber die Entwicklung der Hortgaschen Microglia des Menschen. Arch Psychiat Nervenkr 101:577-592.
49. Kalman B, Olsson O, Link H, et al. 1989. Estradiol potentiates poke-weed mitogen-induced B cell stimulation in multiple sclerosis and healthy subjects. Acta Neurol Scand 79:340-346.
50. Kalra P, Sahu A, Kalra S. 1990. Interleukin-1 inhibits the ovarian steroid-induced luteinizing hormone (LH) releasing hormone in rats. Endocrinology 126:2145-2152.
51. Kawamata T, Akiyama H, Yamada T, et al. 1992. Immunological reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am J Pathol 40:691-707.
52. Keefe D, Garcia-Segura LM, Naftolin F. 1994. New insights into estrogen action on the brain. Neurobiol Aging 15:495-497.
53. Kidron D, Saphier D, Ovadia J, et al. 1989. Central administration of immunomodulatory factors alters neural activity and adrenocortical secretion. Brain Behav Immunol 3:15-27.
54. Kiefer R, Gold R, Gehrmann J, et al. 1993a. Transforming growth factor beta expression in reactive spinal cord microglia and menigeal inflammatory cells during experimental allergic neuritis. J Neurosci Res 36:391-398.
55. Kiefer R, Lingholm D, Kreutzberg G. 1993b. Interleukin-6 and transforming growth factor-beta 1 mRNAs are induced in the rat facial nucleus following motoneuron axotomy. Eur J Neurosci 5:775-781.
56. Kuiper GGJM, Enmark E, Pelto-Huikko M, et al. 1996. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93:5925-5930.
57. Kuiper GGJM, Gustafsson J-A. 1996. The novel estrogen receptor-β subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410:87-90.
58. Lai R, Visser L, Poppema S. 1991. Tissue distribution of restricted leukocyte common antigens. Lab Invest 64: 844-854.
59. Larocca L, Piantelli M, Leone G, et al. 1990. Type II oestrogen binding sites in acute lymphoid and myeloid leukaemias: growth inhibitory effect of oestrogen and flavenoids. Br J Haematol 75:489-495.
60. Lawson L, Perry V, Dri P, et al. 1991. Heterogeneity in the distribution and morphology of microglia in the normal, adult mouse brain. Neuroscience 39:151-170.
61. Lee S, Liu W, Roth P, et al. 1993. Macrophage colony stimulating factor in human fetal astrocytes and microglia: differential regulation by cytokines and lipopolysaccharide, and modulation of class II MHC on microglia. J Immunol 150:594-604.
62. Lindholm D, Castren E, Kiefer R, et al. 1992. Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 117: 395-400.
63. Ling E. 1979. Transformation of monocytes into amoeboid microglia and into microglia in the corpus cllosum of postnatal rats, as shown by labelling monocytes by carbon particles. J Anat 128:847-858.
64. Ling E, Penney D, Leblond C. 1980. Use of carbon-labeling to demonstrate the role of blood monocytes as precursors of the "amoeboid cells" present in the corpus callosum of postnatal rats. J Comp Neurol 193:631-657.
65. Ling E, Tan C. 1974. Amoeboid microglial cells in the corpus callosum of neonatal rats. Arch Histol Jpn 36: 265-280.
66. Ling E, Wong W. 1993. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7:9-18.
67. Lodge P, Sriram S. 1996. Regulation of microglial activation by TGF-beta, IL-1 and CSF-1. J Leuk Biol 60:502-508.
68. Lyson K, McCann S. 1991. The effect of interleukin 6 on pituitary hormone releasing in vivo and in vitro. Neuroendcrinology 54:262-266.
69. Mahley R. 1988. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240: 622-630.
70. Malipiero U, Frei K, Fontana A. 1990. Production of colony stimulating factors by astrocytes. J Immunol 144:3816-3821.
71. 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. Immunology 76:209-216.
72. Mattiace L, Davies P, Dickson D. 1990. Detection of HLA-DR on microglia in the human brain is a function of clinical and technical factors. Am J Pathol 136:1101-1114.
73. McDonnell G, Hawkins S. 1998. An epidemiological study of multiple sclerosis in Northern Ireland. Neurology 50: 423-428.
74. McFarland H. 1969. The management of multiple sclerosis: 3. Apparent suppression of symptoms by an estrogen-progestin compound. Missouri Med 66:209-211.
75. McGeer P, Itagaki S, McGeer E. 1988. Expression of the histocompatibility glycoprotein HLA-DR in neurological disease. Acta Neuropathol 76:550-557.
76. McGeer P, Itagaki S, Tago H, et al. 1987. Reactive microglia in patients with senile dementia of the Alzheimer's type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci Lett 79:195-200.
77. Moalem G, Leibowitz-Amit R, Yoles E, et al. 1999. Autoimmune T cells protect neurons from secondary degeneration after central nerveous system axotomy. Nat Med 5:49-55.
78. Mor G, Amir-Zaltsman Y, Barnard G, et al. 1993. Evidence for the presence of estrogen receptors in monocytes. Endocr J 1:387-395.
79. Mor G, Amir-Zaltsman Y, Barnard G, et al. 1992. Characterization of an antiidiotypic antibody mimicking the actions of estradiol and its interaction with estrogen receptors. Endocrinology 130:3633-3640.
80. Mor G. Gutierrez L, Eliza M, et al. 1998. Fas-Fas ligand system induced apoptosis in human placenta and gestational trophoblastic disease. American Journal of Reproductive Immunology 40:89-95.
81. Mor G, Kohen F, Brown S, et al. 1999. Regulation of Fas ligand expression in breast cancer cells by estrogen: functional differences between estradiol and tamoxifen. J Exp Med (submitted).
82. Mor G, Naftolin F. 1998. Oestrogen, menopause and the immune system. The Journal of the British Menopause Society 4:4-8.
83. Mori S, Leblond C. 1969. Identification of microglia in light and electron microscopy. J Comp Neurol 135:57-80.
84. Naftolin F, Mor G, Horvath T, et al. 1996a. Synaptic remodeling in the arcuate nucleus during the estrous cycle is induced by estrogen and precedes the preovulatory gonadotropin surge. Endocrinology 137:5576-5580.
85. Naftolin F, Mor G, Horvath T, et al. 1996b. Synaptic remodeling in the arcuate nucleus during the estrus cycle is induced by estrogen and precedes the midcycle gonadotrophin surge. Endocrinology 137:5576-5580.
86. Nissl F. 1899. Ueber einige Beziehungen zwischen Nervenzellerkrankungen und gliosen Erscheinungen bei verschiedenen Psychosen. Arch Psychol 32:1-21.
87. Owens T, Renno T, Taupin V, et al. 1994. Inflamatory cytokines in the brain: does the CNS shape immune responses? Immunol Today 15:566-571.
88. Perry V, Gordon S. 1988. Macrophages and microglia in the nervous system. Trends Neurosci 11:273-277.
89. Pierce J, DiMarco E, Cox G, et al. 1990. Macrophage colony stimulating factor (CSF-1) induces proliferation, chemotaxis, and reversible monocytic differentiation in myeloid progenitor cells transfected with the human cfms/CSF-1 receptor cDNA. Proc Natl Acad Sci USA 87:5613-5617.
90. Poirier J. 1996. Apolipoprotein E in the brain and its role in Alzheimer's disease. J Psychiatr Neurosci 21:128-134.
91. Pollard J. 1997. Role of colony-stimulating factor-1 in reproduction and development. Mol Reprod Dev 46:54-60.
92. Pollard J, Bartocci A, Arcecci R, et al. 1987. Apparent role of macrophage growth factor in placental development. Nature 330:484-486.
93. Pow D, Perry V, Morris J, et al. 1989. Microglia and the neurohypophysis associate with and endocytose terminal portions of neurosecretory neurons. Neuroscience 33: 567-578.
94. Righi M, Mori L, DeLibero G, et al. 1989. Monokine production by microglia cell clones. Eur J Immunol 19: 1443-1448.
95. Rio-Hortega PD. 1932. Microglia. In: Penfield W, editor. Cytology and cellular pathology of the nervous system. Vol. 2. New York: Paul B Hoeber. p 481-534.
96. Rivier C, Vale W. 1989. In the rat interleukin lα acts at the level of the brain and the gonads to interfere with gonadotropin and sex steroids secretion. Endocrinology 124: 2105-2109.
97. Rogers J, Luber-Narod J, Styren S, et al. 1988. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol Aging 9:339-349.
98. Sandyk R. 1996. Estrogen's impact on cognitive functions in multiple sclerosis. Int J Neurosci 86:23-31.
99. Santha K, Juba A. 1933. Weiter Untersuchungen uber die Entwicklung der Hortegaschen Mikroglia. Arch Psychiatr Nervenkr 98:598-613.
100. Saphier D. 1989. Neurophysiological and endocrine consequences of immune activity. Brain Behav Immun 14:63-87.
101. Saphier D, Abramsky O, Mor G, et al. 1987. Multiunit electrical activity in conscious rats during an immune response. Brain Behav Immun 1:40-51.
102. Sarchielli P, Orlacchio A, Vicinanza F, et al. 1997. Cytokine secretion and nitric oxide production by mononuclear cells of patients with multiple sclerosis. J Neuroimmunol 80:76-86.
103. Sawada M, Kondo N, Suzumura A, et al. 1989. Production of tumor necrosis factor-α by microglia and astrocytes in culture. Brain Res 491:394-397.
104. Sawada M, Suzumura A, Yamamoto H, et al. 1990. Activation and production of the isolated microglia by colony stimulating factor-1 and possible involvement of protein kinase C. Brain Res 509:119-124.
105. Schipper H. 1991. Gomori-positive astrocytes: biological properties and implications for neurologic and neuroendocrine disorders. Glia 4:365-377.
106. Schipper H, Lechan L, Reichlin S. 1990. Glial peroxidase activity in the hypothalamic arcuate nucleus: effects of estradiol valerate induced persistent estrus. Brain Res 507:200-207.
107. Sedgwick J, Schwender S, Imrich H, et al. 1991. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA 88:7438-7442.
108. Seifer D, Roa-Peña L, Keefe D, et al. 1994. Increasing hypothalamic arcuate nucleus glial peroxidase activity in aging female rats is reduced by an antiestrogen and a gonadotropin-releasing hormone agonist. Menopause 1:83-90.
109. Selmaj K, Raine C. 1988. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann Neurol 23:339-346.
110. Shafit-Zagardo B, Sharma M, Berman J, et al. 1993. CSF-1 expression is upregulated in astrocyte cultures by IL-1 and TNF and affects microglial proliferation and morphology in organotypic cultures. Int J Dev Neurosci 11: 189-198.
111. Shibasaki H, Kuroiwa Y. 1976. Sex difference of multiple sclerosis in Japan. Neurology 26:821-824.
112. Springer T. 1990. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol 111:3129-3139.
113. Stagaard M, Balslev Y, Lundberg J, et al. 1987. Microglia in the hypendyma of the rat subcommissural organ following brain lesion with serotonin neurotoxin. J Neurocytol 16,:31-142.
114. Stone DJ, Rozovsky I, Morgan TE, et al. 1997. Astrocytes and microglia respond to estrogen with increased apoE mRNA in vivo and in vitro. Exp Neurol 143:313-318.
115. Streit W, Graeber M, Kreutzberg G. 1989a. Expression of Ia antigen on perivascular and microglial cells after sublethal and lethal motoneuron injury. Exp Neurol 105.
116. Streit W, Graeber M, Kreutzberg G. 1989b. Peripheral nerve lesion produces increased levels of MHC antigens in the CNS. J Neuroimmunol 21:117-123.
117. Streit WJ, Kreutzberg GW. 1987. Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248-263.
118. Styren S, Civin W, Rogers J. 1990. Molecular, cellular and pathologic characterization of HLA-DR immunoreactivity in normal elderlyt and Alzheimer's disease brain. Exp Neurol 110:93-104.
119. Thery C, Hetier E, Edvard C, et al. 1991. Free radical killing of neurons. Eur J Neurosci 3:1155-1164.
120. Thomas W. 1992. Brain macrophages: evaluation of microglia and their functions. Brain Res Rev 17:61-74.
121. Tooyama I, Kimura H, Akiyama H, et al. 1990. Reactive microglia express class I and class II major histocompatibility antigens in Alzheimer's disease. Brain Res 523: 273-280.
122. Trooster W, Teelken A, Kampinga J, et al. 1993. Suppression of acute experimental allergic encephalomyelitic by the synthetic sex hormone 17-alpha-ethinylestradiol: an immunological study in the Lewis rat. Int Arch Allerg Immunol 102:133-140.
123. Voskuhl R, Pitchekian-Halabi H, MacKenzie-Graham A, et al. 1996. Gender differences in autoimmune demyelination in the mouse: implications for multiple sclerosis. Ann Neurol 39:724-733.
124. Wang J, Griffin J, Rambaldi A, et al. 1988. Induction of monocyte migration by recombinant macrophage colony stimulating factor. J Immunol 141:575-579.
125. Weetman A, McGregor A, ReesSmith B, et al. 1981. Sex hormones enhance immunoglobulin synthesis by human peripheral blood lymphocytes. Immunol Lett 3:343-346.
126. Weinstein D, Walker D, Akiyama H, et al. 1990. Herpes simplex type I infection of the CNS induces major histocompatibility complex antigen expression on rat microglia. J Neurosci Res 26:55-65.
127. Weinstein Y, Ran S, Segal S. 1989. Sex associated differences in regulation of immune responsees controlled by the MHC of the mouse. J Immunol 132:656-661.
128. Wood G. 1980. Immunohistological identification of macrophages in the murine placenta, yolk sac and pregnant uteri. Placenta 1:309-317.
129. Woodroofe M, Bellamy A, Feldman M, et al. 1986. Immunocytochemical characteristics of the immune reaction in the central nervous system in multiple sclerosis: possible role for microglia in lesion growth. J Neurol Sci 74:135-152.
130. Zeev-Brann A, Lazarov-Spiegler O, Brenner T, et al. 1998. Differential effects of central and peripheral nerves on macrophages and microglia. Glia 23:181-190.