Microglia in the human nervous system during development

Neuroembryology

Volumn 2, Issue 1, 2003, Pages 18-31

  Rezaie, Payam ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Astrocytes; Axonal guidance; Gliogenesis; Microglia; Phagocytosis; Synaptogenesis; Vascularisation

Indexed keywords

BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; DEVELOPMENTAL STAGE; DIENCEPHALON; FETUS DEVELOPMENT; HUMAN; MESENCEPHALON; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; RETINA; SHORT SURVEY; SPINAL CORD; TELENCEPHALON;

EID: 0344708486     PISSN: 14248522     EISSN: None     Source Type: Journal    
DOI: 10.1159/000068498     Document Type: Short Survey

References (138)

1. del Rio-Hortega P: El tercer elemento de los centros nerviosos. I. La microglía en estado normal. II. Intervención de la microglía en los procesos patológicos (células en bastoncito y vuerpos gránulo-adiposos. III. Naturaleza pro-able de la microglía. Bol Soc Esp Biol 1919;9:69-129.
2. Kreutzberg GW: Microglia: A sensor for pathological events in the CNS. Trends Neurosci 1996;19:312-318.
3. Kaur C, Hao AJ, Wu CH, Ling EA: Origin of microglia. Micros Res Tech 2001;54:2-9.
4. Rezaie P, Male D: Mesoglia and microglia: A historical review of the concept of mononuclear phagocytes within the central nervous system. J Hist Neurosci, in press.
5. Rezaie P, Male D: Colonisation of the developing human brain and spinal cord by microglia: A review. Microsc Res Tech 1999;45:359-382.
6. Rezaie P, Male D: Differentiation, ramification and distribution of microglia within the central nervous system examined. Neuroembryology 2002;1:29-44.
7. Kershman J: Genesis of microglia in the human brain. Arch Neurol Psychiatry 1939;41:25-50.
8. Hassan NF, Campbell DE, Rifat S, Douglas SD: Isolation and characterization of human fetal brain-derived microglia in in vitro culture. Neuroscience 1991;41:149-158.
9. Lauro GM, Babiloni D, Buttarelli FR, Starace G, Cocchia D, Ennas MG, Sogos V, Gremo F: Human microglia cultures: A powerful model to study their origin and immunoreactive capacity. Int J Dev Neurosci 1995;13:739-752.
10. Rezaie P, Trillo-Pazos G, Everall IP, Male DK: Expression of beta-chemokines and chemokine receptors in human fetal astrocyte and microglial co-cultures: Potential role of chemokines in the developing CNS. Glia 2002;37:64-75.
11. Streit WJ, Kreutzberg GW: Lectin binding by resting and reactive microglia. J Neurocytol 1987;16:249-260.
12. Flügel A, Bradl M, Kreutzberg GW, Graeber MB: Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J Neurosci Res 2001;66:74-82.
13. Hickey WF, Kimura H: Perivascular microglial cells of the CNS are bone marrow derived and present antigen in vivo. Science 1988;239:290-292.
14. Hickey WF, Vass K, Lassmann H: Bone marrow-derived elements in the central nervous system: An immunohistochemical and ultra-structural survey of rat chimeras. J Neuropathol Exp Neurol 1992;51:246-256.
15. Krivit W, Shapiro E, Kennedy W, Lipton M, Lockman L, Smith S, Summers CG, Wenger DA, Tsai MY, Ramsay NK: Treatment of late infantile metachromatic leukodystrophy by bone marrow transplantation. N Engl J Med 1990;322:28-32.
16. Unger ER, Sung JH, Manivel JC, Chenggis ML, Blazar BR, Krivit W: Male donor-derived cells in the brains of female sex-mismatched bone marrow transplant recipients: A Y-chromosome specific in situ hybridization study. J Neuropathol Exp Neurol 1993;52:460-470.
17. Andjelković AV, Nikolic B, Pachter JS, Zečević N: Macrophages/microglial cells in human central nervous system during development: An immunohistochemical study. Brain Res 1998;814:13-25.
18. Choi BH: Hematogenous cells in the central nervous system of developing human embryos and fetuses. J Comp Neurol 1981;196:683-694.
19. Diaz-Araya CM, Provis JM, Penfold PL: Ontogeny and cellular expression of MHC and leukocyte antigens in human retina. Glia 1995;15:458-470.
20. Diaz-Araya CM, Provis JM, Penfold PL, Billson FA: Development of microglial topography in human retina. J Comp Neurol 1995;363:53-68.
21. Esiri MM, Al-Izzi MS, Reading MC: Macrophages, microglial cells, and HLA-DR antigens in fetal and infant brain. J Clin Pathol 1991;44:102-106.
22. Fujimoto E, Miki A, Mizoguti H: Histochemical study of the differentiation of microglial cells in the developing human cerebral hemispheres. J Anat 1989;166:253-264.
23. Gould SJ, Howard S: An immunohistological study of macrophages in the human fetal brain. Neuropathol Appl Neurobiol 1991;17:383-390.
24. Hutchins KD, Dickson DW, Rashbaum WK, Lyman WD: Localization of morphologically distinct microglial populations in the developing human fetal brain: Implications for ontogeny. Brain Res Dev Brain Res 1990;55:95-102.
25. Hutchins KD, Dickson DW, Rashbaum WK, Lyman WD: Localization of microglia in the human fetal cervical spinal cord. Brain Res Dev Brain Res 1992;66:270-273.
26. Máslińska D, Laure-Kamionowska M, Kaliszek A: Morphological forms and localization of microglial cells in the developing human cerebellum. Folia Neuropathol 1998,36:145-151.
27. Provis JM, Diaz CM, Penfold PL: Microglia in human retina: A heterogeneous population with distinct ontogenies. Perspect Dev Neurobiol 1996;3:213-222.
28. Provis JM, Leech J, Diaz CM, Penfold PL, Stone J, Keshet E: Development of the human retinal vasculature: Cellular relations and VEGF expression. Exp Eye Res 1997;65:555-568.
29. Rezaie P, Cairns NJ, Male DK: Expression of adhesion molecules on human fetal cerebral vessels: Relationship to microglial colonisation during development. Brain Res Dev Brain Res 1997;104:175-189.
30. Rezaie P, Patel K, Male DK: Microglia in the human fetal spinal cord - patterns of distribution, morphology and phenotype. Brain Res Dev Brain Res 1999;115:71-81.
31. Sollov'eva ZhV, Orlovskaia DD: Microglia-type cells in normal and pathologic human embryonic brains (in Russian). Zh Nevropatol Psikhiatr Im S S Korsakova 1979;79:852-857.
32. Stoltenburg G, Schmidt S, Marzheuser S, Herbst H, Spiegel H, Unger M: The central nervous system of infants born to HIV-positive mothers - neuropathology, immunohistochemistry and in situ hybridisation (in German). Verh Dtsch Ges Pathol 1991;75:191-194.
33. Stoltenburg-Didinger G, van Landeghem F: Microglia in human fetal brain. Clin Neuropathol 1997;5:290.
34. Weidenheim KM, Epshteyn I, Rashbaum WK, Lyman WD: Patterns of glial development in the human fetal spinal cord during the late first and second trimester. J Neurocytol 1994;23:343-353.
35. Wierzba-Bobrowicz T, Gwiazda E, Poszwinska Z: Morphological study of microglia in human mesencephalon during the development and aging. Folia Neuropathol 1995;33:77-83.
36. Wierzba-Bobrowicz T, Kosno-Kruszewska E, Gwiazda E, Lechowicz W: The comparison of microglia maturation in different structures of the human nervous system. Folia Neuropathol 1998;36:152-160.
37. Wierzba-Bobrowicz T, Kosno-Kruszewska E, Gwiazda E, Lechowicz W: Major histocompatibility complex class II (MHC II) expression during the development of human fetal cerebral occipital lobe, cerebellum, and hematopoietic organs. Folia Neuropathol 2000;38:111-118.
38. Wierzba-Bobrowicz T, Kosno-Kruszewska E, Gwiazda E, Lechowicz W, Schmidt-Sidor B: Major histocompatibility complex class II (MHC II) expression in the normal and pathological human fetal spinal cord. Folia Neuropathol 2001;39:49-56.
39. Wierzba-Bobrowicz T, Lechowicz W, Kosno-Kruszewska E: A morphometric evaluation of morphological types of microglia and astroglia in human fetal mesencephalon. Folia Neuropathol 1997;35:29-35.
40. Wierzba-Bobrowicz T, Lewandowska E, Schmidt-Sidor B, Gwiazda E: The comparison of microglia maturation in CNS of normal human fetuses and fetuses with Down's syndrome. Folia Neuropathol 1999;37:227-234.
41. Wierzba-Bobrowicz T, Schmidt-Sidor B, Gwiazda E, Lechowicz W, Kosno-Kruszewska E: Major histocompatibility complex class II expression in the frontal and temporal lobes in the human fetus during development. Folia Neuropathol 2000;38:73-77.
42. Zečević N, Andjelković A, Matthieu J, Tosić M: Myelin basic protein immunoreactivity in the human embryonic CNS. Brain Res Dev Brain Res 1998;105:97-108.
43. Wekerle H, Linington CH, Lassman H, Meyermann R: Cellular immune reactivity within the CNS. Trends Neurosci 1986;9:271-277.
44. Alliot F, Godin I, Pessac B: Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res Dev Brain Res 1999;117:145-152.
45. Herbomel P, Thisse B, Thisse C: Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 2001;238:274-288.
46. Sorokin SP, Hoyt RF Jr, Blunt DG, McNelly NAF: Macrophage development. II. Early ontogeny of macrophage populations in brain, liver and lungs of rat embryos as revealed by a lectin marker. Anat Rec 1992;232:527-550.
47. Penfold PL, Provis JM, Madigan MC, van Driel D, Billson FA: Angiogenesis in normal human retinal development: The involvement of astrocytes and macrophages. Graefe's Arch Clin Exp Ophthalmol 1990;228:255-263.
48. Becker O, Mito T, Takashima S, Onodera K: Growth and development of the brain in Down syndrome. Prog Clin Biol Res 1991;373:133-152.
49. Schwab JM, Schluesener HJ, Seid K, Meyermann R: IL-16 is differentially expressed in the developing human fetal brain by microglial cells in zones of neuropoiesis. Int J Dev Neurosci 2001;19:93-100.
50. Tanaka J, Toku K, Matsuda S, Sudo J, Fujita H, Sakanaka M, Maeda N: Induction of resting microglia in culture medium devoid of glycine and serine. Glia 1998;24:198-215.
51. Ferrer I, Bernet E, Soriano ET, delRio T, Fonseca M: Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 1990;39:451-458.
52. Ume DA, Perry VH, Gordon S: Immunohistochemical localization of a macrophage-specific antigen in mouse retina: Phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol 1983;97:253-257.
53. Innocenti GM, Koppel H, Clarke S: Transitory macrophages in the white matter of the developing visual cortex. I. Light and electron microscopic characteristics and distribution. Brain Res 1983;313:39-53.
54. Innocenti GM, Clarke S, Koppel H: Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. Brain Res 1983;313:55-66.
55. Perry VH, Hume DA, Gordon S: Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985;15:313-326.
56. Hamilton SP, Rome LH: Stimulation of in vitro myelin synthesis by microglia. Glia 1994;11:326-335.
57. Aldoskogius H: Microglia in neuroregeneration. Microsc Res Tech 2001;54:40-46.
58. Giulian D, Woodward J, Young D, Krebs JF, Lachman LB: Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci 1988;8:2485-2490.
59. Pennell NA, Streit WJ: Colonization of neural allografts by host microglial cells: Relationship to graft neovascularization. Cell Transplant 1997;6:221-230.
60. Perry VH, Gordon S: Macrophages and microglia in the nervous system. Trends Neurosci 1988;11:273-277.
61. Rakic S, Zečević N: Programmed cell death in the developing human telencephalon. Eur J Neurosci 2000;12:2721-2734.
62. Ashwell K: Microglia and cell death in the developing mouse cerebellum. Brain Res Dev Brain Res 1990;55:219-230.
63. Ashwell K: The distribution of microglia and cell death in the fetal rat forebrain. Brain Res Dev Brain Res 1991;58:1-12.
64. Milligan CE, Cunningham TJ, Levitt P: Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. J Comp Neurol 1991;314:125-135.
65. Upender MB, Naegele JR: Activation of micro-glia during developmentally regulated cell death in the cerebral cortex. Dev Neurosci 1999;21:491-505.
66. Chan WY, Kostovic I, Takashima S, Feldhaus C, Stoltenburg-Didinger G, Verney C, Yew D, Ulfig N: Normal and abnormal development of the human cerebral cortex. Neuroembryology 2002;1:78-90.
67. Mazzoni IE, Kenigsberg RL: Microglia from the developing rat medial septal area can affect cholinergic and GABAergic neuronal differentiation in vitro. Neuroscience 1997;76:147-157.
68. Nagata K, Takei N, Nakajima K, Saito H, Kohsaka S: Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 1993;34:357-363.
69. Nakajima K, Nagata K, Hamanoue M, Takemoto N, Kohsaka S: Microglia-derived elastase produces a low-molecular weight plasminogen that enhances neurite outgrowth in rat neocortical explant cultures. J Neurochem 1993;61:2155-2163.
70. Lazar DA, Ellegala DB, Avellino AM, Dailey AT, Andrus K, Kliot M: Modulation of macrophage and microglial responses to axonal injury in the peripheral and central nervous systems. Neurosurgery 1999;45:593-600.
71. Prewitt CM, Niesman IR, Kane CJ, Houle JD: Activated macrophage/ microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 1997;148:433-443.
72. Rabchevsky AG, Streit WJ: Grafting of cultured microglial cells into the lesioned spinal cords of adult rats enhances neurite outgrowth. J Neurosci 1997;47:34-48.
73. Rezaie P, Dean A: Periventricular leukomalacia: The role of inflammatory mediators and microglia in pathogenesis. Neuroembryology 2002;1:91-96.
74. Neumann H, Misgeld T, Matsumoro K, We-kerle H: Neurotrophins inhibit major histo-compatibility class II inductibility of microglia: Involvement of the p75 neurotrophin receptor. Proc Natl Acad Sci USA 1998;95:5779-5784.
75. Streit WJ: Microglia and macrophages in the developing CNS. Neurotoxicology 2001;22:619-624.
76. Arey LB: Developmental Anatoma: A Textbook and Laboratory Manual of Embryology, ed 7. London, Saunders, 1965.
77. Iwama A, Zhang P, Darlington GJ, McKerscher SR, Maki R, Tenen DG: Use of RDA analysis of knockout mice to identify myeloid genes upregulated in vivo by PU.1 and C/EBPalpha. Nucleic Acids Res 1998;26:3034-3043.
78. Tenen DG: Abnormalities of the CEBPalpha transcription factor: A major target in acute myeloid leukemia. Leukemia 2001;15:688-689.
79. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG: Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci USA 1997;94:569-574.
80. Lieschke GJ, Stanley E, Grail D, Hodgson G, Sinickas V, Gall JA, Sinclair RA, Dunn AR: Mice lacking both macrophage- and granulocyte-macrophage colony-stimulating factor have macrophages and coexistent osteopetrosis and severe lung disease. Blood 1994;84:27-35.
81. Seymour JF, Lieschke GJ, Grial D, Quilici C, Hodgson G, Dunn AR: Mice lacking both granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF have impaired reproductive capacity, perturbed neonatal granulopoiesis, lung disease, amyloidosis and reduced long-term survival. Blood 1997;90:3037-3049.
82. Jeetle J, Hagger G, Topps S, Male D, Rezaie P: Microglia in the CD11b knockout mouse; poster presentation. Second International Symposium on Normal and Abnormal Development of the Human Fetal Brain, Rostock, May 24-26, 2002.
83. Fuentes ME, Durham SK, Swerdel MR, Lewin AC, Barton DS, Megill JR, Bravo R, Lira SA: Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J Immunol 1995;155:5769-5776.
84. Lee YB, Nagai A, Kim SU: Cytokines, chemokines and cytokine receptors in human microglia. J Neurosci Res 2002;69:94-103.
85. Pouly S, Becher B, Blain M, Antel JP: Expression of a homologue of rat NG2 on human microglia. Glia 1999;27:259-268.
86. Coraci IS, Husemann J, Berman JW, Hulette C, Dufour JH, Campanella GK, Luster AD, Silverstein SC, El Khoury JB: CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to β-amyloid fibrils. Am J Pathol 2002;160:101-112.
87. Lee SC, Liu W, Brosnan CF, Dickson DW: Characterization of primary human fetal dissociated central nervous system cultures with an emphasis on microglia. Lab Invest 1992;67:465-476.
88. Hu S, Ali H, Sheng WS, Ehrlich LC, Peterson PK, Chao CC: Gp-41-mediated astrocyte inducible nitric oxide synthase mRNA expression: Involvement of interleukin-1beta production by microglia. J Neurosci 1999;19:6468-6474.
89. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW: Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1β. J Immunol 1993;150:2659-2667.
90. Lee SC, Liu W, Brosnan CF, Dickson DW: GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia 1994;12:309-318.
91. Sebire G, Emilie D, Wallon C, Hery C, De-vergne O, Delfraissy JF, Galanaud P, Tardieu M: In vitro production of IL-6, IL-1beta and tumor necrosis factor-alpha by human embryonic microglial and neural cells. J Immunol 1993;150:1517-1523.
92. Chao CC, Gekker G, Hu S, Peterson PK: Human microglial cell defense against Toxoplasma gondii. The role of cytokines. J Immunol 1994;152:1246-1252.
93. Lafortune L, Nalbantoglu J, Antel JP: Expression of tumor necrosis factor alpha (TNFα) and interleukin 6 (IL-6) mRNA in adult human astrocytes: Comparison with adult microglia and fetal astrocytes. J Neuropathol Exp Neurol 1996;55:515-521.
94. Sheng WS, Hu S, Kravitz FH, Peterson PK, Chao CC: Tumour necrosis factor alpha upregulates human microglial cell production of interleukin-10 in vitro. Clin Diagn Lab Immunol 1995;2:604-608.
95. Ehrlich LC, Hu S, Sheng WS, Sutton RL, Rockswold GL, Peterson PK, Chao CC: Cytokine regulation of human microglial cell II-8 production. J Immunol 1998;160:1944-1948.
96. Janabi N, Hau I, Tardieu M: Negative feedback between prostaglandin and alpha- and beta-chemokine synthesis in human microglial cells and astrocytes. J Immunol 1999;162:1701-1706.
97. Lipovsky MM, Gekker G, Hu S, Ehrlich LC, Hoepelman AI, Peterson PK: Cryptococcal glucoronoxylomannan induces interleukin-8 (IL-8) production by human microglia but inhibits neutrophil migration toward IL-8. J Infect Dis 1998;177:260-263.
98. Lee YB, Satoh J, Walker DG, Kim SU: Interleukin-15 gene expression in human astrocytes and microglia in culture. Neuroreport 1996;7:1062-1066.
99. Chao CC, Hu S, Sheng WS, Peterson PK: Tumor necrosis factor-alpha production by human fetal microglial cells: Regulation by other cytokines. Dev Neurosci 1995;17:97-105.
100. Deguchi K, Mizuguchi M, Takashima S: Im-munohistochemical expression of tumor necrosis factor alpha in neonatal leukomalacia. Pediatr Neurol 1996;14:13-16.
101. Fine SM, Maggirwar SB, Elliot PR, Epstein LG, Gelbard HA, Dewhurst S: Proteasome blockers inhibit TNF-α release by lipopolysaccharide stimulated macrophages and microglia: Implications for HIV-1 dementia. J Neuroimmunol 1999;95:55-64.
102. Liu J, Zhao ML, Brosnan CF, Lee SC: Expression of type II nitric oxide synthase in primary human astrocytes and microglia: Role of IL-1β and IL-1 receptor antagonist. J Immunol 1996;157:3569-3576.
103. Hua LL, Lee SC: Distinct patterns of stimulus-inducible chemokine mRNA accumulation in human fetal astrocytes and microglia. Glia 2000;30:74-81.
104. McManus CM, Brosnan CF, Berman JW: Cytokine induction of MIP-1α and MIP-1β in human fetal microglia. J Immunol 1998;160:1449-1455.
105. McManus CM, Liu JS, Hahn MT, Hua LL, Brosnan CF, Berman JW, Lee SC: Differential induction of chemokines in human microglia by type I and II interferons. Glia 2000;29:273-280.
106. Peterson PK, Hu S, Salak-Johnson J, Molitor TW, Chao CC: Differential production of and migratory response to beta chemokines by human microglia and astrocytes. J Infect Dis 1997;175:478-481.
107. Rezaie P, Trillo-Pazos G, Greenwood J, Everall IP, Male DK: Motility and ramification of human fetal microglia in culture: An investigation using time-lapse video microscopy and image analysis. Exp Cell Res 2002;274:68-82.
108. Si QS, Nakamura Y, Schubert P, Rudolphi K, Kataoka K: Adenosine and propentofylline inhibit the proliferation of cultured microglial cells. Exp Neurol 1996;137:345-349.
109. DiPucchio T, Ennas MG, Presta M, Lauro GM: Basic fibroblast growth factor modulates in vitro differentiation of human fetal microglia. Neuroreport 1996;7:2813-2817.
110. Presta M, Urbinati C, Dell'era P, Lauro GM, Sogos V, Balaci L, Ennas MG, Gremo F: Expression of basic fibroblast growth factor and its receptors in human fetal microglia cells. Int J Dev Neurosci 1995;13:29-39.
111. Lee SC, Liu W, Roth P, Dickson DW, Berman JW, Brosnan CF: 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 1993;150:594-604.
112. Jaranowska A, Bussolino F, Sogos V, Arese M, Lauro GM, Gremo F: Platelet-activating factor production by human fetal microglia. Effect of lipopolysaccharide and tumor necrosis factor-α. Mol Chem Neuropathol 1995;24:95-106.
113. Colasanti M, Persichini T, Di Pucchio T, Gremo F, Lauro GM: Human ramified microglial cells produce nitric oxide upon Escherichia coli lipopolysaccharide and tumor necrosis factor alpha stimulation. Neurosci Lett 1995;200:144-146.
114. Ding M, St Pierre BA, Parkinson JF, Medber-ry P, Wong JL, Rogers NE, Ignarro LJ, Merrill JE: Inducible nitric-oxide synthase and nitric oxide production in human fetal astrocytes and microglia. A kinetic analysis. J Biol Chem 1997;272:11327-11335.
115. Ding M, Merrill JE: The kinetics and regulation of the induction of type II nitric oxide synthase and nitric oxide in human fetal glial cell cultures. Mol Psychiatry 1997;2:117-119.
116. Peterson PK, Hu S, Anderson WR, Chao CC: Nitric oxide production and neurotoxicity mediated by activated microglia from human versus mouse brain. J Infect Dis 1994;170:457-460.
117. Espey MG, Chernyshev ON, Reinhard JF Jr, Namboodiri MA, Colton CA: Activated human microglia produce the excitotoxin quinolinic acid. Neuroreport 1997;8:431-434.
118. Cross AK, Woodroofe MN: Chemokine modulation of matrix metalloproteinase and TIMP production in adult rat brain microglia and a human microglial cell line in vitro. Glia 1999;28:183-189.
119. Ghorpade A, Persidskaia R, Suryadevara R, Che M, Liu XJ, Persidsky Y, Gendelman HE: Mononuclear phagocyte differentiation, activation, and viral infection regulate matrix metalloproteinase expression: Implications for human immunodeficiency virus type 1-associated dementia. J Virol 2001;75:6572-6583.
120. Green SP, Cairns B, Rae J, Errett-Baroncini C, Hongo JA, Erickson RW, Curnutte JT: Induction of gp91-phox, a component of the phagocyte NADPH oxidase, in microglial cells during central nervous system inflammation. J Cereb Blood Flow Metab 2001;21:374-384.
121. Balaci L, Presta M, Ennas MG, Dell'Era P, Sogos V, Lauro G, Gremo F: Differential expression of fibroblast growth factor receptors by human neurons, astrocytes and microglia. Neuroreport 1994;6:197-200.
122. Gasque P, Singhrao SK, Neal JW, Gotze O, Morgan BP: Expression of the receptor for complement C5a (CD88) is upregulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. Am J Pathol 1997;150:31-41.
123. Peterson PK, Gekker G, Hu S, Sheng WS, Anderson WR, Ulevitch RJ, Tobias PS, Gustafson KV, Molitor TW, Chao CC: CD14 receptor-mediated uptake of nonopsonized Mycobacterium tuberculosis by human microglia. Infect Immun 1995;63:1598-1602.
124. Liu W, Brosnan CF, Dickson DW, Lee SC: Macrophage colony-stimulating factor mediates astrocyte-induced microglial ramification in human fetal central nervous system culture. Am J Pathol 1994;145:48-53.
125. Chao CC, Gekker G, Hu S, Sheng WS, Shark KB, Bu DF, Archer S, Bidlack JM, Peterson PK: Kappa opioid receptors in human microglia downregulate human immunodeficiency virus 1 expression. Proc Natl Acad Sci USA 1996;93:8051-8056.
126. Chao CC, Hu S, Shark KB, Sheng WS, Gekker G, Peterson PK: Activation of μ opioid receptors inhibits microglial cell chemotaxis. J Pharmacol Exp Ther 1997;281:998-1004.
127. Lipovsky MM, Gekker G, Hu S, Hoepelman AI, Peterson PK: Morphine enhances complement receptor-mediated phagocytosis of Cryptococcus neoformans by human microglia. Clin Immunol Immunopathol 1998;87:163-167.
128. Peterson PK, Gekker G, Hu S, Sheng WS, Molitor TW, Chao CC: Morphine stimulates phagocytosis of Mycobacterium tuberculosis by human microglial cells: Involvement of a G protein-coupled opiate receptor. Adv Neuroimmunol 1995;5:299-309.
129. Chao CC, Gekker G, Sheng WS, Hu S, Loh HH, Peterson PK: Orphan opioid receptor oligonucleotides inhibit HIV-1 expression in human brain cells. Adv Exp Med Biol 1998;437:83-90.
130. Lai JP, Zhan GX, Campbell DE, Douglas SD, Ho WZ: Detection of substance P and its receptor in human fetal microglia. Neuroscience 2000;101:1137-1144.
131. Gabuzda D, He J, Ohagen A, Vallat AV: Chemokine receptors in HIV-1 infection of the central nervous system. Semin Immunol 1998;10:203-213.
132. He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, Mackay CR, Sodroski J, Gabuzda D: CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 1997;385:645-649.
133. Vallat AV, De Girolami U, He J, Mhashilkar A, Marasco W, Shi B, Gray F, Bell J, Keohane C, Smith TW, Gabuzda D: Localization of HIV-1 co-receptors CCR5 and CXCR4 in the brain of children with AIDS. Am J Pathol 1998;152:167-178.
134. Cross AK, Woodroofe MN: Chemokines induce migration and changes in actin polymerization in adult rat brain microglia and a human fetal microglial cell line in vitro. J Neurosci Res 1999;55:17-23.
135. Hegg CC, Hu S, Peterson PK, Thayer SA: Beta-chemokines and human immunodeficiency virus type-1 proteins evoke intracellular calcium increases in human microglia. Neuroscience 2000;98:191-199.
136. Kitai R, Zhao ML, Zhang N, Hua LL, Lee SC: Role of MIP-1β and RANTES in HIV-1 infection of microglia: Inhibition of infection and induction by IFNβ. J Neuroimmunol 2000;110:230-239.
137. McLarnon JG, Xu R, Lee YB, Kim SU: Ion channels of human microglia in culture. Neuroscience 1997;78:1217-1228.
138. Lai JP, Douglas SD, Shaheen F, Pleasure DE, Ho WZ: Quantification of substance P mRNA in human immune cells by real-time reverse transcriptase PCR assay. Clin Diagn Lab Immunol 2002;9:138-143.