Development of microglia in the postnatal rat hippocampus

Hippocampus

Volumn 8, Issue 5, 1998, Pages 458-474

  Dalmau, Ishar ^a   Finsen, Bente ^b   Zimmer, Jens ^b   González, Berta ^a   Castellano, Bernardo ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Differentiation; Distribution; Neuroglia, fascia dentata; Nucleoside diphosphatase

Indexed keywords

NUCLEOSIDE DIPHOSPHATASE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; MALE; MICROGLIA; NERVE PROJECTION; NONHUMAN; PERFORANT NERVE TRACT; PHAGOCYTOSIS; POSTNATAL DEVELOPMENT; PRECURSOR; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPTOGENESIS; TIME;

ACID ANHYDRIDE HYDROLASES; ANIMALS; ANIMALS, NEWBORN; CELL AGING; CELL DIFFERENTIATION; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HISTOCYTOCHEMISTRY; MALE; MICROGLIA; RATS; RATS, WISTAR; TIME FACTORS;

EID: 0031787049     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1998)8:5<458::AID-HIPO6>3.0.CO;2-N     Document Type: Article

References (101)

1. Acarín L, González B, Castro A, Castellano B. Microglial response to N-methyl-D-aspartate-mediated excitotoxicity in the immature rat brain. J Comp Neurol 1996;367:361-374.
2. Altman J, Das GD. Autoradiographic and histological evidences of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965;124: 319-335.
3. Altman J, Bayer SA Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 1990a;301:325-342.
4. Altman J, Bayer SA Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale J Comp Neurol 1990b;301:343-364.
5. Altman J, Bayer SA Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990c;301:365-381.
6. Ashwell K. Microglia and cell death in the developing mouse cerebellum. Dev Brain Res 1990;55:219-230.
7. Ashwell K. The distribution of microglial and cell death in the fetal rat forebrain. Dev Brain Res 1991;58:1-12.
8. Bancroft JD, Stewens A. Proteins and nucleic acid. In: Bancroft JD, Stevens A, eds. Theory and practice of histological techniques. Edinburg: Churchill Livingstone, 1996:139-150.
9. 3H-thymidine autoradiography J Comp Neurol 1980a;190:87-114.
10. Bayer SA Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J Comp Neurol 1980b;190:115-134.
11. Bayer SA, Altman JA Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog Neurobiol 1987;29:57-106.
12. Benveniste EN Astrocyte-microglia interactions. In: Murphy S, ed. Astrocytes: Pharmacology and function, vol. 15. San Diego: Academic Press, 1993:355-382.
13. Benveniste EN Cytokine production. In: Kettenmann H, Ransom BR, eds. Neuroglia. New York Oxford University Press, 1995:700-713.
14. Bignami A, Dahl D. Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J Comp Neurol 1974;153:27-38.
15. Boya J, Calvo JL, Carbonell AL, Borregon A A lectin histochemistry study on the development of rat microglial cells. J Anat 1991;175:229-236.
16. Caggiano AO, Brunjes PC. Microglia and the developing olfactory bulb. Neuroscience 1993;52:717-724.
17. Cammermeyer J. The life history of the microglial cell: A light microscopic study Neurosci Res 1970;3:43-129.
18. Castellano B, Gonzalez B, Dalmau I, Vela JM. Identification and distribution of microglial cells in the cerebral cortex of the lizard A histochemical technique J Comp Neurol 1991a;311:434-444.
19. Castellano B, González B, Jensen MB, Pedersen EB, Finsen BR, Zimmer J. A double staining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J Histochem Cytochem 1991b;39:561-568.
20. Chamak B, Mallat M. Fibronectin and laminin regulate the in vitro differentiation of microglial cells. Neuroscience 1991;45:513-527.
21. Chugani DC, Kedersha NL, Rome LH. Vault immunofluorescence in the brain: New insights regarding the origin of microglia J Neurosci 1991;11:256-268.
22. Cotman CW, Taylor D, Lynch G. Ultrastructural changes in synapses in the dentate gyrus of the rat during development. Brain Res 1973;63: 205-213.
23. Cuadros MA, Martin C, Coltey P, Almendros A, Navascués J. First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J Comp Neurol 1993;330:113-129.
24. Cuadros MA, Moujahid A, Quesada A, Navascués J. Development of microglia in the quail optic tectum J Comp Neurol 1994;348:207-224.
25. Dahl, D, Rueger DC, Bignami. Vimentin, the 57,000 molecular weight protein of fibroblast filament, is the major cytoskeletal component in immature glia Eur J Cell Biol 1981;24:191-196.
26. Dalmau I, Castellano B, Pedersen EB, Finsen B, Zimmer J, Gonzalez B. Reduction of the microglial cell number in rat primary glial cell cultures by exogenous addition of dibutyryl cyclic adenosine monophosphate. J Neuroimmunol 1996;70:123-129.
27. Dalmau I, Finsen B, Tønder N, Zimmer J, González B, Castellano B. Development of microglia in the prenatal rat hippocampus. J Comp Neurol 1997a;377:70-84.
28. Dalmau I, Vela JM, Gonzalez B, Castellano B. Expression of LFA-1α and ICAM-1 in the developing rat brain; A potential mechanism for the recruitment of microglial cell precursors. Dev Brain Res 1997b;103: 163-170.
29. Dalmau I, Vela JM, Gonzalez B, Castellano B. Expression of purine metabolism-related enzymes by microglial cells in the developing rat brain. J Comp Neurol, 1998; in press.
30. Davis EJ, Foster TD, Thomas WE. Cellular forms and functions of brain microglia Brain Res Bull 1994;1:73-78.
31. Del Río Hortega P Microglia In; Penfield W, ed. Cytology and cellular pathology of the nervous system, vol. 2. New York Paul B. Hoeber, 1932:481-534.
32. Del Rio JA Martínez A, Fonseca M, Auladell C, Soriano E. Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody Cereb Cortex 1995;5:13-21.
33. Del Río JA Heimrich B, Borrell V, Forster E, Drakew A Alcantara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E. A role for Cajal-Retzius cells and reeling in the development of hippocampal connections. Nature 1997;385:70-74.
34. Fabry Z, Fitzsimmons KM, Herlein JA, Moninger TO, Dobbs MB, Hart MN. Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol 1993;47:23-34.
35. Fabry Z, Raine CS, Hart MN. Nervous tissue as an immune compartment: The dialect of the immune response in the CNS. Immunol Today 1994;15:218-224.
36. Fagan AM, Gage FH. Mechanisms of sprouting in the adult central nervous system: Cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus. Neuroscience 1994;58:705-725.
37. Ferrer I, Serrano T, Soriano E. Naturally occurring cell death in the subicular complex and hippocampus in the rat during development. Neurosci Res 1990a;8:60-66.
38. Ferrer I, Bernet E, Soriano E, Del Río JA Fonseca M. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 1990b;39:451-458.
39. Finsen B, Tønder N, Xavier GF, Sørensen JC, Zimmer J. Induction of microglial immunomolecules by anterogradely degenerating mossy fibers in the rat hippocampal formation. J Chem Neuroanat 1993;6: 267-275.
40. Finsen B, Lehrmann E, Castellano B, Kiefer R, Zimmer J. The role of microglial cells and brain macrophages in transient global cerebral ischemia In: Ling EA, Tan CK, Tan CBC, eds. Topical issues in microglial research Singapore: Singapore Neuroscience Association, 1996:297-318.
41. Frei K, Siepl C, Groscurth P, Bodmer S, Schwerdel C, Fontana A Antigen presentation and tumor cytotoxicity by interferon-γ-treated microglial cells, Eur J Immunol 1987;17:1271-1278.
42. Fricke R, Cowan WM. An autoradiographic study of the development of the entorhinal and commissural afferents to the dentate gyrus of the rat. J Comp Neurol 1977;173:231-250.
43. Gaarskjaer FB. The organization and development of the hippocampal mossy fiber system. Brain Res Rev 1986;11:335-357.
44. Giulian D, CorpuzM. Microglial secretion products and their impact on the nervous system. Adv Neurol 1993;59:315-320.
45. Giulian D, Ingeman JE. Colony-stimulating factors as promoters of ameboid microglia J Neurosci 1988;8:4707-4717.
46. Giulian D, Baker TJ, Shih L-CN, Lachman L. Interleukin 1 of the central nervous system is produced by ameboid microglia J Exp Med 1986;164:594-604.
47. Giulian D, Woodward J, Young DG, Krebs JF, Lachman LB. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J Neurosci 1988;8:2485-2490.
48. Graeber MB, Streit WJ. Perivascular microglia defined Trends Neurosci 1990;13:366.
49. Graeber MB, Streit WJ, Kreutzberg GW Identity of ED2-positive perivascular cells in rat brain. J Neurosci Res 1989;22:103-106.
50. Hagg T, Varon S, Louis J-C. Ciliary neurotrophic factor (CNTF) promotes low-affinity nerve growth factor receptor and CD4 expression by rat CNS microglia. J Neuroimmunol 1993;48:177-188.
51. Hart MN, Fabry Z, Love-Homan L, Keiner J, Sadewasser KL, Moore SA Brain microvascular smooth muscle and endothelial cells produce granulocyte macrophage colony-stimulating factor and support colony formation of granulocyte-macrophage-like cells. Am J Pathol 1992; 141:421-427.
52. Hebel R, Stromberg MW. Nervous system. In: Hebel R, Stromberg MW, eds. Anatomy and embryology of the laboratory rat. Wörthsee: BioMed Verlag. 1986:124-217.
53. Hine RJ, Das GD. Neuroembryogenesis in the hippocampal formation of the rat. Z Anat Entwickl-Gesh 1974;144:173-186.
54. Hume DA, Perry VH, Gordon S. Immunohistochemical Iocalization 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 1983;97:253-257.
55. Imamoto K, Leblond CP. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J Comp Neurol 1978;180:139-163.
56. Imamura K, Suzumura A, Sawada M, Mabuchi C, Marunouchi T. Induction of MHC class II antigen expression on murine microglia by interleukin-3. J. Neuroimmunology 1994;55:119-125.
57. Innocenti GM, Clarke S, Koppel H. Transitory macrophages in the white matter of the developing visual cortex II. Development and relations with axonal pathways. Dev Brain Res 1983;11:55-66.
58. Jacobson M. Neuroglial ontogeny. In: Jacobson M, ed Developmental neurobiology New York Plenum Press, 1991a:95-142.
59. Jacobson M. Formation of dendrites and development of synaptic connections. In: Jacobson M, ed Developmental neurobiology New York Plenum Press, 1991b:223-283.
60. Jensen MB, Gonzalez B, Castellano B, Zimmer J. Microglial and astroglial reactions to anterograde axonal degeneration: Ahistochemical and immunocytochemical shudy of the adult rat fascia dentata after entorhinal path lesions, Exp Brain Res 1994;98:245-260.
61. Jensen MB, Finsen B, Zimmer J. Morphological and immunophenotypic microglial changes in denervated fascia dentata of adult rat. Correlation with blood-brain barrier damage and astroglial reactions. Exp Neurol 1997;143:103-116.
62. Jørgensen MB, Finsen BR, Jensen MB, Castellano B, Diemer N, Zimmer J. Microglial and astroglial reactions to ischemie and kainic acid-induced lesions of the adult rat hippocampus. Exp Neurol 1993;120: 70-88.
63. Landry CF, Ivy GO, Brown IR. Developmental expression of glial fibrillary acidic protein mRNA in the rat brain analyzed by in situ hybridization. J Neurosci Res 1990;25:194-203.
64. Lassmann H, Zimprich F, Vass K, Hickey WF. Microglial cells are a component of the perivascular glia limitans. J Neurosci Res 1991;28: 236-243.
65. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990;39:151-170.
66. Ling EA The origin and nature of microglia In: Federoff S, Hertz L, eds. Advances in cellular neurobiology vol II. New York Academic Press, 1981:33-82.
67. Ling EA, Wong WC. The origin and nature of ramified and amoeboid microglia A historical review and current contents Glia 1993;7:9-18.
68. Loughlin AJ, Woodroofe MN, Cuzner ML. Regulation of Fc receptor and major histocompatibility complex antigen expression on isolated rat microglia by tumour necrosis factor, interleukin-1 and lipopolysac-charide: Effects on interferon-gamma induced activation. Immunology 1992;75:170-175.
69. Loughlin AJ, Woodroofe MN, Cuzner ML. Modulation of interferon-γ-induced major histocompatibility complex class II and Fc receptor expression on isolated microglia by transforming growth factor-β1, interleukin-4, noradrenaline and glucocorticoids. Immunology 1993; 79:125-130.
70. Loy R. Development of afferent lamination in Ammon's horn of the rat. Anat Embryol 1980;159:257-275.
71. Loy R, Lynch G, Cotman CW Development of afferent lamination in the fascia dentata of the rat. Brain Res 1977;50:174-178.
72. Megyeri P, Abrahám CS, Temesvári P, Kovács J, Vas T, Speer CP. Recombinant human tumor necrosis factor alpha constricts pial arterioles and increases blood-brain barrier permeability in newborn piglets. Neurosci Lett 1992;148:137-140.
73. Moujahid A, Navascués J, Marín-Teva JL, Cuadros MA Macrophages during avian optic nerve development: Relationship to cell death and differentiation into microglia Anat Embryol 1996;193:131-144.
74. Murabe Y, Sano Y. Morphological studies on neuroglia. V. Microglial cells in the cerebral cortex of the rat, with special reference to their possible involvement in synaptic function Cell Tissue Res 1982a;223:493-506.
75. Murabe Y, Sano Y. Morphological studies on neuroglia VI. Postnatal development of microglial cells. Cell Tissue Res 1982b;225:469-485.
76. Murphy S, Simmons ML, Agulló L, García A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D, Schwartz JP Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 1993;16:323-328.
77. Navascués J, Cuadros MA, Almendros A Development of microglia: evidence from studies in the avian central nervous system. In: Ling EA, Tan CK, Tan CBC, eds. Topical issues in microglial research Singapore: Singapore Neuroscience Association, 1996:43-64.
78. Panek RB, Benveniste EN Class II gene expression in microglia Regulation by the cytokines IFN-γ, TNF-α, and TGF-β. J Immunol 1995;154:2846-2854.
79. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Sidney: Academic Press, 1986.
80. Paxinos G, Törk I, Tecott LH, Valentine KL. Atlas of the developing rat brain. San Diego: Academic Press, 1991.
81. Perry VH, Gordon S. Macrophages and the nervous system. Int Rev Cytol 1991;125:203-244.
82. Perry VH, Hume DA, Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985;15:313-326.
83. Peters A, Palay SL, Webster H deF. The neuroglial cells. In Peters A, Palay SL, Webster H deF, eds. The fine structure of the nervous system. Neurons and their supporting cells New York: Oxord University Press, 1991:273-311.
84. Kami A, Rabié A Effect of thyroid deficiency on the development of glia in the hippocampal formation of the rat: An immunocytochemical study Glia1988;1:337-345.
85. Rickmann M, Amaral DG, Cowan WM. Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 1987;264:449-479.
86. Robertson PL, Du Bois M, Bowman PD, Goldstein GW Angiogenesis in developing rat brain: An in vivo and in vitro study Dev Brain Res 1985;355:219-223.
87. Rössler K, Neuchrist C, Kitz K, Scheiner O, Kraft D, Lassmann H. Expression of leucocyte adhesion molecules at the human blood-brain barrier. J Neurosci Res 1992;31:365-374.
88. Schlessinger AR, Cowan WM, Gottlieb DI. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 1975;159:149-176.
89. Smith ME, McFarlin DE, Dhib-Jalbut S. Differential effect of interleu-kin-1β on Ia expression in astrocytes and microglia. J Neuroimmunol 1993;46:97-104.
90. Soriano E, Del Río JA, Martínez A, Super H. Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 1994;342:571-595.
91. Sørensen JC, Dalmau I, Zimmer J, Finsen B. Microglial reactions to tracer identified thalamic neurons after frontal motocortex lesions in adult rats. Exp Brain Res 1996;112:203-212.
92. Super H, Soriano E. The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with lipophilic tracer DiI. J Comp Neurol 1994;344:101-120.
93. Suzumura A, Marunouchi T, Yamamoto H. Morphological transformation of microglia in vitro. Brain Res 1991;545:301-306.
94. Streit WJ. Microglial celk In: Kettenmann H, Ransom BR, eds. Neuroglia. New York: Oxford University Press, 1995:85-96.
95. Tanaka J, Maeda N. Microglial ramification requires nondiffusible factors derived from astrocytes. Exp Neurol 1996;137:367-375.
96. Thomas WE. Brain macrophages: Evaluation of microglia and their functions. Brain Res Rev 1992;17:61-74.
97. Vela JM, Dalmau I, González B, Castellano B. Morphology and distribution of microglial cells in the young and adult mouse cerebellum. J Comp Neurol 1995;361:602-616.
98. Wu CH, Wen CY, Shieh JY, Ling EA A quantitative study of the differentiation of microglial cells in the developing cerebral cortex in rats. J Anat 1993;182:403-413.
99. Zimmer J. Proximity as a factor in the regulation of aberrant axonal growth in postnatally deafferented fascia dentata. Brain Res 1974;72: 137-142.
100. Zimmer J. Development of the hippocampus and fascia dentata: morphological and histochemical aspects. In: Corner MA, Baker RE, Van de Pol NE, Swaab DF, eds. Progress in brain research: Maturation of the nervous system. Amsterdam: Elsevia/North-Holland Biochemical Press, 1978:171-190.
101. Zimmer J, Haug F-MS. Laminar differentiation of the hippocampus, fascia dentata and subiculum in developing rats, observed with the timm sulphide silver method. J Comp Neurol 1978;179:581-618.