Physiological roles of microglia during development

Journal of Neurochemistry

Volumn 119, Issue 5, 2011, Pages 901-908

  Pont Lezica, Lorena ^a   Béchade, Catherine ^a   Belarif Cantaut, Yasmine ^a   Pascual, Olivier ^a   Bessis, Alain ^a  

^a CNRS   (France)

Author keywords

apoptosis; astrocytes; axon growth; glia; microglia

Indexed keywords

ANGIOGENESIS; APOPTOSIS; ASTROCYTE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; DEVELOPMENTAL STAGE; GLIA; HIPPOCAMPUS; HUMAN; MACROPHAGE; MESENCHYME; MICROGLIA; NERVE CELL NECROSIS; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; RADIAL GLIA; REVIEW; TISSUE DISTRIBUTION; VASCULARIZATION;

ANIMALS; CELL COMMUNICATION; CENTRAL NERVOUS SYSTEM; HUMANS; MICROGLIA; NEURONS; YOLK SAC;

EID: 81255199251     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07504.x     Document Type: Review

References (88)

1. Aarum J., Sandberg K., Haeberlein S. L. B., and, Persson M. A. A., (2003) Migration and differentiation of neural precursor cells can be directed by microglia. Proc. Natl Acad. Sci. USA 100, 15983-15988. (Pubitemid 38021101)
2. Alliot F., Godin I., and, Pessac B., (1999) Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res. Dev. Brain Res. 117, 145-152. (Pubitemid 29531505)
3. Amor S., Puentes F., Baker D., and, Valk P. V. D., (2010) Inflammation in neurodegenerative diseases. Immunology 129, 154-69.
4. Antony J. M., Paquin A., Nutt S. L., Kaplan D. R., and, Miller F. D., (2011) Endogenous microglia regulate development of embryonic cortical precursor cells. J. Neurosci. Res. 89, 286-298.
5. Ashwell K., (1989) Development of microglia in the albino rabbit retina. J. Comp. Neurol. 287, 286-301. (Pubitemid 19239064)
6. Ashwell K. W., Holländer H., Streit W., and, Stone J., (1989) The appearance and distribution of microglia in the developing retina of the rat. Vis. Neurosci. 2, 437-448.
7. Barres B. A., (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60, 430-440.
8. Béchade C., Pascual O., Triller A., and, Bessis A., (2011) Nitric oxide regulates astrocyte maturation in the hippocampus: involvement of NOS2. Mol. Cell. Neurosci. 46, 762-769.
9. Bessis A., Béchade C., Bernard D., and, Roumier A., (2007) Microglial control of neuronal death and synaptic properties. Glia 55, 233-8. (Pubitemid 46225955)
10. Block M. L., Zecca L., and, Hong J.-S., (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. (Pubitemid 46011999)
11. Brown A. S., and, Patterson P. H., (2011) Maternal infection and schizophrenia: implications for prevention. Schizophr. Bull. 37, 284-290.
12. Calderõ J., Brunet N., Ciutat D., Hereu M., and, Esquerda J. E., (2009) Development of microglia in the chick embryo spinal cord: implications in the regulation of motoneuronal survival and death. J. Neurosci. Res. 87, 2447-2466.
13. Carmeliet P., and, Tessier-Lavigne M., (2005) Common mechanisms of nerve and blood vessel wiring. Nature 436, 193-200. (Pubitemid 41021263)
14. Chamak B., Morandi V., and, Mallat M., (1994) Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J. Neurosci. Res. 38, 221-233. (Pubitemid 24155739)
15. Checchin D., Sennlaub F., Levavasseur E., Leduc M., and, Chemtob S., (2006) Potential role of microglia in retinal blood vessel formation. Invest. Ophthalmol. Vis. Sci. 47, 3595-3602. (Pubitemid 351639729)
16. Cuadros M. A., García-Martín M., Martin C., and, Ríos A., (1991) Haemopoietic phagocytes in the early differentiating avian retina. J. Anat. 177, 145-158.
17. Cuadros M. A., Moujahid A., Martin-Partido G., and, Navascués J., (1992) Microglia in the mature and developing quail brain as revealed by a monoclonal antibody recognizing hemopoietic cells. Neurosci. Lett. 148, 11-14. (Pubitemid 23007692)
18. Cuadros M. A., Martin C., Coltey P., Almendros A., and, Navascués J., (1993) First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J. Comp. Neurol. 330, 113-129. (Pubitemid 23095318)
19. Cuadros M. A., Rodríguez-Ruiz J., Calvente R., Almendros A., Marín-Teva J. L., and, Navascués J., (1997) Microglia development in the quail cerebellum. J. Comp. Neurol. 389, 390-401. (Pubitemid 28353903)
20. Dalmau I., Finsen B., Tønder N., Zimmer J., González B., and, Castellano B., (1997a) Development of microglia in the prenatal rat hippocampus. J. Comp. Neurol. 377, 70-84. (Pubitemid 27023827)
21. Dalmau I., Vela J. M., González B., and, Castellano B., (1997b) Expression of LFA-1alpha and ICAM-1 in the developing rat brain: a potential mechanism for the recruitment of microglial cell precursors. Brain Res. Dev. Brain Res. 103, 163-170. (Pubitemid 27521407)
22. Dalmau I., Finsen B., Zimmer J., González B., and, Castellano B., (1998) Development of microglia in the postnatal rat hippocampus. Hippocampus 8, 458-474. (Pubitemid 28505238)
23. Davalos D., Grutzendler J., Yang G., Kim J. V., Zuo Y., Jung S., Littman D. R., Dustin M. L., and, Gan W.-B., (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758. (Pubitemid 43085841)
24. Dieterlen-Lievre F., (1975) On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J. Embryol. Exp. Morphol. 33, 607-619.
25. Fantin A., Vieira J. M., Gestri G., Denti L., Schwarz Q., Prykhozhij S., Peri F., Wilson S. W., and, Ruhrberg C., (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116, 829-840.
26. Frade J. M., and, Barde Y. A., (1998) Microglia-derived nerve growth factor causes cell death in the developing retina. Neuron 20, 35-41. (Pubitemid 28078347)
27. Frei K., Bodmer S., Schwerdel C., and, Fontana A., (1986) Astrocyte-derived interleukin 3 as a growth factor for microglia cells and peritoneal macrophages. J. Immunol. 137, 3521-3527. (Pubitemid 17193310)
28. Ginhoux F., Greter M., Leboeuf M., et al. (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845.
29. Giulian D., Young D. G., Woodward J., Brown D. C., and, Lachman L. B., (1988) Interleukin-1 is an astroglial growth factor in the developing brain. J. Neurosci. 8, 709-714. (Pubitemid 18078093)
30. Hanisch U.-K., and, Kettenmann H., (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394. (Pubitemid 350014685)
31. Haynes S. E., Hollopeter G., Yang G., Kurpius D., Dailey M. E., Gan W.-B., and, Julius D., (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9, 1512-1519. (Pubitemid 44862659)
32. Herbomel P., Thisse B., and, Thisse C., (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735-3745. (Pubitemid 29440473)
33. Herbomel P., Thisse B., and, Thisse C., (2001) Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev. Biol. 238, 274-288. (Pubitemid 32977296)
34. Innocenti G. M., Clarke S., and, Koppel H., (1983) Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. Brain Res. 313, 55-66. (Pubitemid 14211302)
35. Kettenmann H., (2007) Neuroscience: the brain's garbage men. Nature 446, 987-989. (Pubitemid 46676052)
36. Kettenmann H., Hanisch U.-K., Noda M., and, Verkhratsky A., (2011) Physiology of microglia. Physiol. Rev. 91, 461-553.
37. Kreutzberg G. W., (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318. (Pubitemid 26349059)
38. Kriegstein A. R., and, Noctor S. C., (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392-399. (Pubitemid 38829254)
39. Lee S. C., Liu W., Brosnan C. F., and, Dickson D. W., (1994) GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia 12, 309-318.
40. Ling E. A., (1976) Some aspects of amoeboid microglia in the corpus callosum and neighbouring regions of neonatal rats. J. Anat. 121, 29-45.
41. Ling E. A., and, Wong W. C., (1993) The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7, 9-18.
42. Ling E. A., Penney D., and, Leblond C. P., (1980) Use of carbon labeling to demonstrate the role of blood monocytes as precursors of the ® ameboid cells  present in the corpus callosum of postnatal rats. J. Comp. Neurol. 193, 631-657. (Pubitemid 11233741)
43. Long J. M., Kalehua A. N., Muth N. J., Calhoun M. E., Jucker M., Hengemihle J. M., Ingram D. K., and, Mouton P. R., (1998) Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol. Aging 19, 497-503. (Pubitemid 29065499)
44. Lucin K. M., and, Wyss-Coray T., (2009) Immune activation in brain aging and neurodegeneration: too much or too little? Neuron 64, 110-122.
45. Lyck L., Santamaria I. D., Pakkenberg B., Chemnitz J., Schrøder H. D., Finsen B., and, Gundersen H. J. G., (2009) An empirical analysis of the precision of estimating the numbers of neurons and glia in human neocortex using a fractionator-design with sub-sampling. J. Neurosci. Methods 182, 143-156.
46. Mallat M., Marín-Teva J. L., and, Chéret C., (2005) Phagocytosis in the developing CNS: more than clearing the corpses. Curr. Opin. Neurobiol. 15, 101-107. (Pubitemid 40249968)
47. Marín-Teva J. L., Dusart I., Colin C., Gervais A., van Rooijen N., and, Mallat M., (2004) Microglia promote the death of developing Purkinje cells. Neuron 41, 535-547. (Pubitemid 38253066)
48. Matthias K., Kirchhoff F., Seifert G., Hüttmann K., Matyash M., Kettenmann H., and, Steinhäuser C., (2003) Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J. Neurosci. 23, 1750-1758. (Pubitemid 36314730)
49. Miller F. D., and, Gauthier A. S., (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54, 357-369. (Pubitemid 46659814)
50. Monier A., Adle-Biassette H., Delezoide A.-L., Evrard P., Gressens P., and, Verney C., (2007) Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J. Neuropathol. Exp. Neurol. 66, 372-382. (Pubitemid 46701319)
51. Moore M. A., and, Metcalf D., (1970) Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br. J. Haematol. 18, 279-296.
52. Morgan S. C., Taylor D. L., and, Pocock J. M., (2004) Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-Notch signalling cascades. J. Neurochem. 90, 89-101. (Pubitemid 38879165)
53. Moujahid A., Navascués J., Marín-Teva J. L., and, Cuadros M. A., (1996) Macrophages during avian optic nerve development: relationship to cell death and differentiation into microglia. Anat. Embryol. 193, 131-144. (Pubitemid 26040028)
54. Nagata K., Takei N., Nakajima K., Saito H., and, Kohsaka S., (1993) Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J. Neurosci. Res. 34, 357-363. (Pubitemid 23060121)
55. Nakanishi M., Niidome T., Matsuda S., Akaike A., Kihara T., and, Sugimoto H., (2007) Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur. J. Neurosci. 25, 649-658.
56. Navascués J., Calvente R., Marín-Teva J. L., and, Cuadros M. A., (2000) Entry, dispersion and differentiation of microglia in the developing central nervous system. An. Acad. Bras. Cienc. 72, 91-102.
57. Nimmerjahn A., Kirchhoff F., and, Helmchen F., (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318. (Pubitemid 40746128)
58. Ohinata H., Tochinai S., and, Katagiri C., (1990) Occurrence of nonlymphoid leukocytes that are not derived from blood islands in Xenopus laevis larvae. Dev. Biol. 141, 123-129.
59. Paolicelli R. C., Bolasco G., Pagani F., et al. (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 233, 1456-1458.
60. Pelvig D. P., Pakkenberg H., Stark A. K., and, Pakkenberg B., (2008) Neocortical glial cell numbers in human brains. Neurobiol. Aging 29, 1754-1762.
61. Peri F., and, Nüsslein-Volhard C., (2008) Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell 133, 916-927. (Pubitemid 351707689)
62. Peters A., Josephson K., and, Vincent S. L., (1991) Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat. Rec. 229, 384-398.
63. Prinz M., and, Mildner A., (2011) Microglia in the CNS: immigrants from another world. Glia 59, 177-187.
64. Ransohoff R. M., and, Cardona A. E., (2010) The myeloid cells of the central nervous system parenchyma. Nature 468, 253-62.
65. Rezaie P., Patel K., and, Male D. K., (1999) Microglia in the human fetal spinal cord-patterns of distribution, morphology and phenotype. Brain Res. Dev. Brain Res. 115, 71-81. (Pubitemid 29288634)
66. Rezaie P., Trillo-Pazos G., Greenwood J., Everall I. P., and, Male D. K., (2002) Motility and ramification of human fetal microglia in culture: an investigation using time-lapse video microscopy and image analysis. Exp. Cell Res. 274, 68-82.
67. Rezaie P., Ulfig N., and, Male D., (2003) Distribution and morphology of GFAP-positive astrocytes in the human fetal brain at second trimester. Neuroembryology 2, 50-63. (Pubitemid 37485328)
68. Rezaie P., Dean A., Male D., and, Ulfig N., (2005) Microglia in the cerebral wall of the human telencephalon at second trimester. Cereb. Cortex 15, 938-949. (Pubitemid 40848063)
69. Rigato C., Buckinx R., Le-Corronc H., Rigo J. M., and, Legendre P., (2011) Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks. Glia 59, 675-695.
70. Rivest S., (2009) Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 9, 429-39.
71. Rymo S. F., Gerhardt H., Wolfhagen Sand F., Lang R., Uv A., and, Betsholtz C., (2011) A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS ONE 6, e15846.
72. Sánchez-Lõpez A., Cuadros M. A., Calvente R., Tassi M., Marín-Teva J. L., and, Navascués J., (2004) Radial migration of developing microglial cells in quail retina: a confocal microscopy study. Glia 46, 261-273. (Pubitemid 38679206)
73. Santos A. M., Calvente R., Tassi M., Carrasco M.-C., Martín-Oliva D., Marín-Teva J. L., Navascués J., and, Cuadros M. A., (2008) Embryonic and postnatal development of microglial cells in the mouse retina. J. Comp. Neurol. 506, 224-239.
74. Schlegelmilch T., Henke K., and, Peri F., (2011) Microglia in the developing brain: from immunity to behaviour. Curr. Opin. Neurobiol. 21, 5-10.
75. Sedel F., Béchade C., Vyas S., and, Triller A., (2004) Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J. Neurosci. 24, 2236-2246. (Pubitemid 38314555)
76. Sierra A., Encinas J. M., Deudero J. J. P., Chancey J. H., Enikolopov G., Overstreet-Wadiche L. S., Tsirka S. E., and, Maletic-Savatic M., (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7, 483-95.
77. Sorokin S. P., Hoyt Jr R. F., Blunt D. G., and, McNelly N. A., (1992) Macrophage development: II. Early ontogeny of macrophage populations in brain, liver, and lungs of rat embryos as revealed by a lectin marker. Anat. Rec. 232, 527-550.
78. Stence N., Waite M., and, Dailey M. E., (2001) Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33, 256-266. (Pubitemid 32219134)
79. Stevens B., Allen N. J., Vazquez L. E., et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178. (Pubitemid 350235022)
80. Takahashi K., Yamamura F., and, Naito M., (1989) Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: a light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. J. Leukoc. Biol. 45, 87-96. (Pubitemid 19077294)
81. Tanaka J., and, Maeda N., (1996) Microglial ramification requires nondiffusible factors derived from astrocytes. Exp. Neurol. 137, 367-375. (Pubitemid 26080333)
82. Tremblay M.-È., Lowery R. L., and, Majewska A. K., (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8, e1000527.
83. Verney C., Monier A., Fallet-Bianco C., and, Gressens P., (2010) Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 217, 436-448.
84. Wake H., Moorhouse A. J., Jinno S., Kohsaka S., and, Nabekura J., (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974-3980.
85. Wakselman S., Béchade C., Roumier A., Bernard D., Triller A., and, Bessis A., (2008) Developmental neuronal death in hippocampus requires the microglial CD11b integrin and DAP12 immunoreceptor. J. Neurosci. 28, 8138-8143.
86. Watkins L. R., Hutchinson M. R., Ledeboer A., Wieseler-Frank J., Milligan E. D., and, Maier S. F., (2007) Norman Cousins Lecture. Glia as the ® bad guys  implications for improving clinical pain control and the clinical utility of opioids. Brain Behav. Immun. 21, 131-146. (Pubitemid 46038918)
87. Zhang S. C., and, Fedoroff S., (1996) Neuron-microglia interactions in vitro. Acta Neuropathol. 91, 385-395. (Pubitemid 26088974)
88. Zhou M., Schools G. P., and, Kimelberg H. K., (2006) Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J. Neurophysiol. 95, 134-143. (Pubitemid 44698923)