Entry, dispersion and differentiation of microglia in the developing central nervous system

Anais da Academia Brasileira de Ciencias

Volumn 72, Issue 1, 2000, Pages 91-102

  Navascués, Julio ^a   Calvente, Ruth ^a   Marín Teva, José L ^a,b   Cuadros, Miguel A ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Hematopoietic lineage; Meninges; Microglia; Migration; Proliferation

Indexed keywords

ANIMAL; APOPTOSIS; CELL DIFFERENTIATION; CELL MOTION; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; CYTOLOGY; HUMAN; METABOLISM; MICROGLIA; MITOSIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; HUMANS; MICROGLIA; MITOSIS;

EID: 0033660578     PISSN: 00013765     EISSN: None     Source Type: Journal    
DOI: 10.1590/S0001-37652000000100013     Document Type: Article

References (100)

1. ABD-EL-BASSET A & FEDOROFF S 1995. Effect of bacterial wall lipopolysaccharide (LPS) on morphology, motility, and cytoskeletal organization of microglia incultures. J Neurosci Res 41: 222-237.
2. ASHWELL K 1989. Development of microglia in the albino rabbit retina. J Comp Neurol 287: 286-301.
3. ASHWELL K 1990. Microglia and cell death in the developing mouse cerebellum. Dev Brain Res 55: 219-230.
4. ASHWELL K 1991. The distribution of microglia and cell death in the fetal rat forebrain. Dev Brain Res 58: 1-12.
5. ASHWELL KWS & BOBRYSHEV YV 1996. The developmental role of microglia. In: LING EA, TAN CK & TAN CBC, editors. Topical Issues in Microglial Research. Singapore: Singapore Neuroscience Association, pp 65-82.
6. ASHWELL KWS, HOLLÄNDER H, STREIT W & STONE J 1989. The appearance and distribution of microglia in the developing retina of the rat. Vis Neurosci 2: 437-448.
7. BADIE B, SCHARTNER J. KLAVER J & VORPAHL J 1999. In vitro modulation of microglia motility by glioma cells is mediated by hepatocyte growth factor scatter factor. Neurosurgery 44: 1077-1082.
8. BEREZOVSKAYA O, MAYSINGER D & FEDOROFF S 1995. The hematopoietic cytokine, colony-stimulating factor 1, is also a growth factor in the CNS: congenital absence of CSF-1 in mice results in abnormal microglial response and increased neuron vulnerability to injury. Int J Dev Neurosci 13: 285-299.
9. BLEVINS G & FEDOROFF S 1995. Microglia in colony-stimulating factor-1 deficient op/op mice. J Neurosci Res 40: 535-544.
10. BOOTH PL & THOMAS WE 1991. Evidence for motility and pinocytosis in ramified microglia in tissue culture. Brain Res 548: 163-171.
11. BOYA J, CALVO J & PRADO A 1979. The origin of microglial cells. J Anat 129: 177-186.
12. BOYA J, CALVO JL, CARBONELL AL & BORREGON A 1991. A lectin histochemistry study on the development of rat microglial cells. J Anat 175: 229-236.
13. BROCKHAUS J, MÖLLER T & KETTENMANN H 1996. Phagocytozing ameboid microglial cells studied in a mouse corpus callosum slice preparation. Glia 16: 81-90.
14. CHAMAK B & MALLAT M 1991. Fibronectin and laminin regulate the in vitro differentiation of microglial cells. Neuroscience 45: 513-527.
15. CROSS AK & WOODROOFE MN 1999. 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 55: 17-23.
16. CUADROS MA & NAVASCUÉS J 1998. The origin and differentiation of microglial cells during development. Prog Neurobiol 56: 173-189.
17. CUADROS MA, MOUJAHID A, QUESADA A & NAVASCUÉS J 1994. Development of microglia in the quail optic tectum. J Comp Neurol 348: 207-224.
18. CUADROS MA, RODRÍGUEZ-RUIZ J, CALVENTE R, ALMENDROS A, MARÍN-TEVA JL & NAVASCUÉS J 1997. Microglia development in the quail cerebellum. J Comp Neurol 389: 390-401.
19. DALMAU I 1997. Las células de microglía en el cerebro de la rata en desarrollo. Doctoral Thesis. Universidad Autónoma de Barcelona, Barcelona, Spain.
20. DIAZ-ARAYA CM, PROVIS JM & PENFOLD PL 1995a. Ontogeny and cellular expression of MHC and leucocyte antigens in human retina. Glia 15: 458-470.
21. DIAZ-ARAYA CM, PROVIS JM, PENFOLD PL & BILLSON FA 1995b. Development of microglial topography in human retina. J Comp Neurol 363: 53-68.
22. EGENSPERGER R, MASLIM J, BISTI S, HOLLÄNDER H & STONE J 1996. Fate of DNA from retinal cells dying during development: uptake by microglia and macroglia (Müller cells). Dev Brain Res 97: 1-8.
23. ELKABES S, DICICCOBLOOM EM & BLACK IB 1996. Brain microglia macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16: 2508-2521.
24. FEDOROFFS 1995. Development of microglia. In: KETTENMANN H & RANSOM BR, editors. Neuroglia. New York: Oxford University Press, pp 162-181.
25. FEDOROFF S, ZHAI R & NOVAK JP 1997. Microglia and astroglia have a common progenitor cell. J Neurosci Res 50: 477-486.
26. FERRER I, BERNET E, SORIANO E, DEL Rio T & FONSECA M 1990. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 39: 451-458.
27. FLARIS NA, DENSMORE TL, MOLLESTON MC & HICKEY WF 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. FUJITA H, TANAKA J, TOKU K, TATEISHI N, SUZUKI Y, MATSUDA S, SAKANAKA M & MAEDA N 1996. Effects of GM-CSF and ordinary supplements on the ramification of microglia in culture: a morphometrical study. Glia 18: 269-281.
29. FUJITA H, TANAKA J, MAEDA N & SAKANAKA M 1998. Adrenergic agonists suppress the proliferation of microglia through beta 2-adrenergic receptor. Neurosci Lett 242: 37-40.
30. GANTER S, NORTHOFF H, MÄNNEL P & GEBICKE-HÄRTER PJ 1992. Growth control of cultured microglia. J Neurosci Res 33: 218-230.
31. GARCIA-VALENZUELA E & SHARMA SC 1999. Laminar restriction of retinal macrophagic response to optic nerve axotomy in the rat. J Neurobiol 40: 55-66.
32. GEHRMANN J, MATSUMOTO Y & KREUTZBERG GW 1995. Microglia: intrinsic immunoeffector cell of the brain. Brain Res Rev 20: 269-287.
33. GIULIAN D & BAKER TJ 1986. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6: 2163-2178.
34. GIULIAN D & INGEMANN JE 1988. Colony-stimulating factors as promoters of ameboid microglia. J Neurosci 8: 4707-4717.
35. GIULIAN D, JOHNSON B, KREBS JF, GEORGE JK & TAPSCOTT M 1991. Microglial mitogens are produced in the developing and injured mammalian brain. J Cell Biol 112: 323-333.
36. GIULIAN D, BARTEL S, BROKER J. LI X & KIRKPATRICK JB 1995. Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J Neurosci 15: 7712-7726.
37. GLABINSKI AR, BALASINGAM V, TANI M, KUNKEL SL, STRIETER RM, YONG VW & RANSOHOFF RM 1996. Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J Immunol 156:4363-4368.
38. HAAPANIEMI H, TOMITA M, TANAHASHI N, TAKEDA H, YOKOYAMA M & FUKUUCHI Y 1995. Non-amoeboid locomotion of cultured microglia obtained from newborn rat brain. Neurosci Lett 193: 121-124.
39. HALFTER W & FUA CS 1987. Immunohistochemical localization of laminin, neural cell adhesion molecule, collagen type IV and T-61 antigen in the embryonic retina of the Japanese quail by in vivo injection of antibodies. Cell Tiss Res 249: 487-496.
40. HALFTER W, RECKHAUS W & KRÖGER S 1987. Nondirected axonal growth on basal lamina from avian embryonic neural retina. J Neurosci 7: 3712-3722.
41. HAO C, RICHARDSON A & FEDOROFF S 1991. Macrophage-like cells originate from neuroepithelium in culture: characterization and properties of the macrophage-like cells. Int J Dev Neurosci 9: 1-14.
42. HUME DA, PERRY VH & GORDON S 1983. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol 97: 253-257.
43. IMAMOTO K & LEBLOND CP 1978. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J Comp Neurol 180: 134-164.
44. IVACKO J. SZAFLARSKI J, MALINAK C, FLORY C, WARREN JS & SILVERSTEIN FS 1997. Hypoxic-ischemic injury induces monocyte chemoattractant protein-1 expression in neonatal rat brain. J Cereb Blood Flow Metab 17: 759-770.
45. KAUR C & LING EA 1991. Study of the transformation of amoeboid microglial cells into microglia labelled with the isolectin Griffonia simplicifolia in postnatal rats. Acta Anat 142: 118-125.
46. KITAMURA T, MIYAKE T & FUJITA S 1984. Genesis of resting microglia in the gray matter of mouse hippocampus. J Comp Neurol 226: 421-433.
47. KLOSS CUA, KREUTZBERG GW & RAIVICH G 1997. Proliferation of ramified microglia on an astrocyte monolayer: characterization of stimulatory and inhibitory cytokines. J Neurosci Res 49: 248-254.
48. LAWSON LJ, PERRY VH, DRI P & GORDON S 1990. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience, 39: 151-170.
49. LAWSON LJ, PERRY VH & GORDON S 1992. Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48: 405-415.
50. LEE S, LIU W, BROSNAN C & DICKSON D 1994. GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia 12: 309-318.
51. LING EA 1976. Some aspects of amoeboid microglia in the corpus callosum and neighbouring regions of neonatal rats. J Anat 121: 29-45.
52. LING EA 1981. The origin and nature of microglia. In: FEDOROFF S, HERTZ L, editors. Advances in Cellular Neurobiology, Vol. 2. London: Academic Press, pp 33-82.
53. LING EA & TAN CK 1974. Ameboid microglia cells in the corpus callosum of neonatal rats. Arch Histol Jap 36: 265-280.
54. LING EA & WONG WC 1993. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7: 9-18.
55. LING EA, PENNEY D & LEBLOND CP 1980. Use of carbon labelling 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.
56. LIVA SM, KAHN MA, DOPP JM & DE VELLIS J 1999. Signal transduction pathways induced by GM-CSF in microglia: significance in the control of proliferation. Glia 26: 344-352.
57. LÓPEZ-GARCÍA C, NACHER J, CASTELLANO B, Luis DE LA IGLESIA JA & MOLOWNY A 1994. Transitory disappearance of microglia during the regeneration of the lizard medial cortex. Glia 12: 52-61.
58. MACIEJEWSKI-LENOIR D, CHEN SZ, FENG LL, MAKI R & BACON KB 1999. Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J Immunol 163: 1628-1635.
59. MALLAT M, CALVO CF & DOBBERTIN A 1996. Recruitment of brain macrophages: roles of cytokines and extracellular matrix proteins produced by glial or neuronal cells. Braz. J. Med. Biol. Res. 29: 1173-1177.
60. MARÍN-TEVA JL, ALMENDROS A, CALVENTE R, CUADROS MA & NAVASCUÉS J 1998. Tangential migration of ameboid microglia in the developing quail retina: mechanism of migration and migratory behavior. Glia 22: 31-53.
61. MARÍN-TEVA JL, ALMENDROS A, CALVENTE R, CUADROS MA & NAVASCUES J 1999a. Proliferation of actively migrating ameboid microglia in the developing quail retina. Anal Embryol 200: 289-300.
62. MARÍN-TEVA JL, CALVENTE R, CUADROS MA, ALMENDROS A & NAVASCUÉS J 1999b. Circumferential migration of ameboid microglia in the margin of the developing quail retina. Glia 27: 226-238.
63. MARÍN-TEVA JL, CUADROS MA, CALVENTE R, ALMENDROS A & NAVASCUÉS J 1999c. Naturally occurring cell death and migration of microglial precursors in the quail retina during normal development. J Comp Neurol 412: 255-275.
64. MILLIGAN CE, CUNNINGHAM TJ & LEVITT P 1991. Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. J Comp Neurol 314: 125-135.
65. MOUJAHID A, NAVASCUÉS J, MARÍN-TEVA JL & CUADROS MA 1996. Macrophages during avian optic nerve development: relationship to cell death and differentiation into microglia. Anat Embryol 193: 131-144.
66. MURABE Y & SANO Y 1982. Morphological studies on neuroglia. VI. Postnatal development of microglial cells. Cell Tiss Res 225: 469-485.
67. NAVASCUÉS J, MOUJAHID A, ALMENDROS A, MARÍN-TEVA JL & CUADROS MA 1995. Origin of microglia in the quail retina: central-to-peripheral and vitreal-to-scleral migration of microglial precursors during development. J Comp Neurol 354: 209-228.
68. NAVASCUÉS J. CUADROS MA & ALMENDROS A 1996. Development of microglia: evidence from studies in the avian central nervous system. In: LING EA, TAN CK & TAN CBC, editors. Topical Issues in Microglia Research. Singapore: Singapore Neuroscience Association, pp 43-64.
69. PEARSON HE, PAYNE BR & CUNNINGHAM TJ 1993. Microglial invasion and activation in response to naturally occurring neuronal degeneration in the ganglion cell layer of the postnatal cat retina. Dev Brain Res 76: 249-255.
70. PERRY VH 1987. Macrophages, microglia and cell death in the developing mouse brain. Pontif Acad Scient Scripta Varia 59: 281-295.
71. PERRY VH & GORDON S 1991. Macrophages and the nervous system. Int Rev Cytol 125: 203-244.
72. PERRY VH & LAWSON LJ 1992. Macrophages in the Central Nervous System. In: LEWIS EC & MCGEE JOD, editors. The Macrophage. Oxford: IRL Press, pp 389-413.
73. PERRY VH, HUME DA & GORDON S 1985. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15: 313-326.
74. RAIVICH G, MORENO-FLORES MT, MÖLLER JC & KREUTZBERG GW 1994. Inhibition of posttraumatic microglial proliferation in a genetic model of macrophage colony-stimulating factor deficiency in the mouse. Eur J Neurosci 6: 1615-1618.
75. RAKIC S & ZECEVIC N 1998. Apoptosis and microglia in the fetal human brain. Soc Neurosci Abst 24: 807.
76. RIO-HORTEGA P 1932. Microglia. In: PENFIELD W, editor. Cytology and Cellular Pathology of the Nervous System, Vol. 2. New York: Paul B. Hoeber, pp 481-534.
77. RINGHEIM GE 1995. Mitogenic effects of interleukin-5 on microglia. Neurosci Lett 201: 131-134.
78. SAWADA M, SUZUMURA A, YAMAMOTO H & MARUNOUCHI T 1990. Activation and proliferation of the isolated microglia by colony stimulating factor-1 and possible involvement of protein kinase C. Brain Res 509: 119-124.
79. SCHNITZER J 1989. Enzyme-histochemical demonstration of microglial cells in the adult and postnatal rabbit retina. J Comp Neurol 282: 249-263.
80. SHAFIT-ZAGARDO B, SHARMA N, BERMAN JW, BORNSTEIN MB & BROSNAN CF 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.
81. STEWART PA & WILEY MJ 1981. Structural and histochemical features of the avian blood-brain barrier. J Comp Neurol 202: 157-167.
82. STOLL G & JANDER S 1999. The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 58: 233-247.
83. STREIT WJ, GRAEBER MB & KREUTZBERG GW 1988. Functional plasticity of microglia: a review. Glia 1: 301-307.
84. SUGITA Y, BECERRA SP, CHADER GJ & SCHWARTZ JP 1997. Pigment epithelium-derived factor (PEDF) has direct effects on the metabolism and proliferation of microglia and indirect effects on astrocytes. J Neurosci Res 49: 710-718.
85. SUZUMURA A & SAWADA M 1996. Microglia as immunoregulatory cells in the central nervous system. In: LING EA, TAN CK & TAN CBC, editors. Topical Issues in Microglia Research. Singapore: Singapore Neuroscience Association, pp 189-202.
86. SUZUMURA A, SAWADA M, YAMAMOTO H & MARUNOUCHI T 1990. Effects of colony stimulating factors on isolated microglia in vitro. J Neuroimmunol 30: 111-120.
87. SUZUMURA A, MARUNOUCHI T & YAMAMOTO H 1991. Morphological transformation of microglia in vitro. Brain Res 545: 301-306.
88. SUZUMURA A, SAWADA M, ITOH Y & MARUNOUCHI T 1994. Interleukin-4 induces proliferation and activation of microglia but suppresses their induction of class II major histocompatibility complex antigen expression. J Neuroimmunol 53: 209-218.
89. TANAKA J & MAEDA N 1996. Microglial ramification requires nondiffusible factors derived from astrocytes. Exp Neurol 137: 367-375.
90. TANAKA J, TOKU K, SAKANAKA M & MAEDA N 1999. Morphological differentiation of microglial cells in culture: involvement of insoluble factors derived from astrocytes. Neurosci Res 34: 207-215.
91. THANOS S 1991. The relationship of microglial cells to dying neurons during natural neuronal cell death and axotomy-induced degeneration of the rat retina. Eur J Neurosci 3: 1189-1207.
92. THANOS S, MOORE S & HONG Y 1996. Retinal microglia. Progr Ret Eye Res 15: 331-361.
93. VELA-HERNÁNDEZ JM, DALMAU I, GONZÁLEZ B & CASTELLANO B 1997. Abnormal expression of the proliferating cell nuclear antigen (PCNA) in the spinal cord of the hypomyelinated jimpy mutant mice. Brain Res 747: 130-139.
94. WARD SA, RANSOM PA, BOOTH PL & THOMAS WE 1991. Characterization of ramified microglia in tissue culture: pinocytosis and motility. J Neurosci Res 29: 13-28.
95. WILMS H, HARTMANN D & SIEVERS J 1997. Ramification of microglia, monocytes and macrophages in vitro: influences of various epithelia and mesenchymal cells and their conditioned media. Cell Tiss Res 287: 447-458.
96. WILMS H, WOLLMER MA & SIEVERS J 1999. In-vitro staining specificity of the antibody 5-D-4 for microglia but not for monocytes and macrophages indicates that microglia are a unique subgroup of the myelomonocytic lineage. J Neuroimmunol 98: 89-95.
97. WOLSWIJK G 1995. Strongly GD3+ cells in the developing and adult rat cerebellum belong to the microglial lineage rather than to the oligodendrocyte lineage. Glia 13: 13-26.
98. WONG ROL, HUGHES A 1987. Role of cell death in the topogenesis of neuronal distributions in the developing cat retinal ganglion cell layer. J Comp Neurol 262: 496-511.
99. WU CH, WEN CY, SHIEH JY & LING EA 1996. Use of lectin as a tool for the study of microglial cells: expression and regulation of lectin receptors in normal development and under experimental conditions. In: LING EA, TAN CK & TAN CBC, editors. Topical Issues in Microglia Research. Singapore: Singapore Neuroscience Association, pp 83-202.
100. XU J, KAUR C & LING EA 1993. Variation with age in the labelling of ameboid microglial cells in rats following intraperitoneal or intravenous injection of a fluorescent dye. J Anat 182: 55-63.