Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants

Journal of Anatomy

Volumn 217, Issue 4, 2010, Pages 436-448

  Verney, Catherine ^a,b,c   Monier, Anne ^d   Fallet Bianco, Catherine ^e   Gressens, Pierre ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c PremUP   (France)

^d HOP UNIV DES ENFANTS REINE FABIOLA   (Belgium)

^e CENTRE HOSPITALIER SAINTE ANNE   (France)

Author keywords

Brain macrophages; CD45; CD68; Development; Double immunolabelling; Inductible nitric oxide synthase; Ionized calcium binding adapter molecule 1; N methyl D aspartate receptor 1; Periventricular leukomalacia; Vessels; White matter crossroads

Indexed keywords

ARTICLE; BRAIN CORTEX; BRAIN INJURY; BRAIN VENTRICLE; CHOROID PLEXUS; DIENCEPHALON; FOREBRAIN; HUMAN; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; INFANT; MACROPHAGE; MENINX; MICROGLIA; PRIORITY JOURNAL; TELENCEPHALON; WHITE MATTER INJURY;

ANTIGENS, CD; ANTIGENS, CD34; ANTIGENS, CD45; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CELL MOVEMENT; DIENCEPHALON; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; KI-67 ANTIGEN; MACROPHAGES; MICROGLIA; TELENCEPHALON;

EID: 77956461653     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2010.01245.x     Document Type: Article

References (73)

1. Allendoerfer KL, Shatz CJ. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 1994, 17:185-218.
2. Aloisi F, Ria F, Adorini L. Regulation of T-cell responses by CNS antigen-presenting cells: different roles for microglia and astrocytes. Immunol Today 2000, 21:141-147.
3. Andjelkovic AV, Nikolic B, Pachter JS. Macrophages/microglial cells in the human central nervous system during development: an immunohistochemical study. Brain Res 1998, 814:13-25.
4. Ashwell K. The distribution of microglia and cell death in the fetal rat forebrain. Dev Brain Res 1991, 58:1-12.
5. Banati RB, Graeber MB. Surveillance, intervention and cytotoxicity: is there a protective role for microglia? Dev Neurosci 1994, 16:114-127.
6. Baud O, Daire JL, Dalmaz Y. Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol 2004, 14:1-10.
7. Billiards SS, Haynes RL, Folkerth RD. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 2006, 497:199-208.
8. Billiards SS, Haynes RL, Folkerth RD. Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 2008, 18:153-163.
9. Chamak B, Dobbertin A, Mallat M. Immunohistochemical detection of thrombospondin in microglia in the developing rat brain. Neuroscience 1995, 69:177-187.
10. Chan WY, Kohsaka S, Rezaie P. The origin and cell lineage of microglia: new concepts. Brain Res Rev 2007, 53:344-354.
11. Choi BH. Hematogenous cells in the central nervous system of developing embryos and fetuses. J Comp Neurol 1981, 196:683-694.
12. Cuadros MA, Martin C, Coltey P. First appearance, distribution and origin of macrophages in the early development of the avian nervous system. J Comp Neurol 1993, 330:113-129.
13. Dick AD, Pell M, Brew BJ, Foulcher E, Sedgwick JD. Direct ex vivo flow cytometric analysis of human microgial cells CD14 expression: examination of central nervous system biopsy specimens from HIV-scropositive patients with other neurological diseases. AIDS 1997, 11:1699-1708.
14. Earle KL, Mitrofanis J. Identification of transient microglial cell colonies in the forebrain white matter of developing rats. J Comp Neurol 1997, 387:371-384.
15. 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.
16. Fedoroff S, Zhai R, Novak JP. Microglia and astroglia have a common progenitor cell. J Neurosci Res 1997, 50:477-486.
17. Ferrer I, Bernet E, Soriano E. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 1990, 39:451-458.
18. Folkerth RD. Neuropathologic substrate of cerebral palsy. J Child Neurol 2005, 20:940-948.
19. 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.
20. Giulian D. Ameboid microglia as effectors of inflammation in the central nervous system. J Neurosci Res 1987, 18:155-171.
21. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 1986, 6:2163-2178.
22. Gould SJ, Howard S. An immunohistological study of macrophages in the human fetal brain. Neuropathol Appl Neurobiol 1991, 17:383-390.
23. Graeber MB, Streit WJ. Microglia: immune network in the CNS. Brain Pathol 1990, 1:2-5.
24. Hao C, Richardson A, Fedoroff S. Macrophage-like cells originate from the neuroepithelium in culture: Characterization and properties of macrophage-like cells. Int J Dev Neurosci 1991, 9:1-14.
25. Haynes RL, Folkerth RD, Trachtenberg FL. Nitrosative stress and inducible nitric oxide synthase expression in periventricular leukomalacia. Acta Neuropathol 2009, 118:391-399.
26. Hickey WF, Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988, 239:290-292.
27. Hutchins KD, Dickson DW, Kure K. Evidence that microglia in the human brain may be derived from the neurectoderm. J Neuropathol Exp Neurol 1989, 48:342.
28. Hutchins KD, Dickson DW, Rashbaum WK. Localization of morphologically distinct microglial populations in the developing human fetal brain: implications for ontogeny. Brain Res Dev Brain Res 1990, 55:95-102.
29. 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. Dev Brain Res 1983a, 11:39-53.
30. 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 1983b, 11:55-66.
31. Ito D, Imai Y, Ohsawa K. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 1998, 57:1-9.
32. Judas M, Rados M, Jovanov-Milosevic N. Structural, immunocytochemical, and mr imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. Am J Neuroradiol 2005, 26:2671-2684.
33. Kadhim H, Tabarki B, Verellen G. Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 2001, 56:1278-1284.
34. Kadhim H, Tabarki B, De Prez C. Interleukin-2 in the pathogenesis of perinatal white matter damage. Neurology 2002, 58:1125-1128.
35. Kershman J. Genesis of microglia in the human brain. Arch Neurol Psychiatry 1939, 41:24-50.
36. Khwaja O, Volpe JJ. Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008, 93:F153-F161.
37. Konigsmark BW, Sidman RL. Origin of brain macrophages in the mouse. J Neuropathol Exp Neurol 1963, 22:643-676.
38. Kostovic I, Molliver ME. A new interpretation of laminar development of cerebral cortex: synaptogenesis in different layers of neopallium in the human fetus. Anat Rec 1974, 178:395.
39. Kostovic I, Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 1990, 297:441-470.
40. Larroque B, Ancel PY, Marret S. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet 2008, 371:813-820. EPIPAGE Study Group
41. Ling EA. The origin and nature of microglia. Advances in Cellular Neurobiology 1981, 33-82. Fedoroff SHertz L. eds, New York, Academic
42. Ling EA, Wong WC. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 1993, 7:9-18.
43. Mallard C, Welin AK, Peebles D. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 2003, 28:215-223.
44. Marin-Teva JL, Dusart I, Colin C. Microglia promote the death of developing Purkinje cells. Neuron 2004, 41:535-547.
45. 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.
46. Monier A, Evrard P, Gressens P. Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J Comp Neurol 2006, 499:565-582.
47. Monier A, Adle-Biassette H, Delezoide A-L. Microglial colonization of developing human cortex. J Neuropathol Exp Neurol 2007, 66:372-382.
48. Navascues J, Calvente R, Marin-Teva JL. Entry, dispersion and differentiation of microglia in the developing central nervous system. An Acad Bras Cienc 2000, 72:91-102.
49. Olivier P, Baud O, Evrard P. Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 2005, 64:998-1006.
50. Perry VH, Hume DA, Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 1985, 15:313-326.
51. Rakic P. Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond B Biol Sci 1977, 278:245-260.
52. Rakic S, Zecevic N. Programmed cell death in the developing human telencephalon. Eur J Neurosci 2000, 12:2721-2734.
53. Rezaie P. Microglia in the human nervous system during development. Neuroembryology 2003, 2:18-31.
54. Rezaie P. Microglia - from origins to differentiation, distribution and dynamics within the mammalian central nervous system. Trends in Glial Research, Basic and Applied 2007, 1-41. Dheen STLing EA. eds, Kerala, Research Signpost
55. Rezaie P, Male D. Colonization of the developing human brain and spinal cord by microglia: A review. Microsc Res Tech 1999, 45:359-382.
56. Rezaie P, Male D. Differentiation, ramification and distribution of microglia within the central nervous system examined. Neuroembryology 2002, 1:29-43.
57. 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.
58. Rezaie P, Dean A, Male D. Microglia in the cerebral wall of the human telencephalon at second trimester. Cereb Cortex 2005, 15:938-949.
59. del Rio Hortega P. El " tercer clemento" de los centros nerviosos. Bol Soc Esp Biol 1919, 9:68-120.
60. del Rio Hortega P. Microglia. Section X. Cytology and Cellular Pathology of the Nervous System 1932, 481-534. Penfield W. ed, New York, Hoeber
61. Rochefort N, Quenech'du N, Watroba L. Microglia and astrocytes may participate in the shaping of visual callosal projections during postnatal development. J Physiol Paris 2002, 96:183-192.
62. Shatz CJ, Chun JJ, Luskin MB. The role of the subplate in the development of the mammalian telencephalon. Cerebral Cortex 1988, 35-58. Peters A, Jones EG, eds, New York, Plenum Press
63. Spassky N, de Castro F, Le Bras B. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J Neurosci 2002, 22:5992-6004.
64. Streit WJ, Graeber MB, Kreutzberg GW. Functional plasticity of microglia: a review. Glia 1988, 1:301-307.
65. Tahraoui SL, Marret S, Bodénant C. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001, 11:56-71.
66. Tsai HH, Miller RH. Glial cell migration directed by axon guidance cues. Trends Neurosci 2002, 25:173-175.
67. Verney C, Milosevic A, Alvarez C. Immuno-cytochemical evidence of well-developed dopaminergic and noradrenergic innervations in the frontal cerebral cortex of human fetuses at midgestation. J Comp Neurol 1993, 336:331-344.
68. Verney C, Fallet-Bianco C, Pogledic I. Characteristics of Glial Cells in Diffuse Versus Focal White Matter Lesions of Preterm Infants 2009, Paris, Euroglia
69. Volpe JJ. The encephalopathy of prematurity - brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 2009, 16:167-178.
70. Wierzba-Bobrowicz T, Gwiazda E, Poswinska Z. Morphological study of microglia in human mesencephalon during the development and aging. Folia Neuropathol 1995, 33:77-83.
71. 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.
72. Yoon BH, Romero R, Kim CJ. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol 1997, 177:406-411.
73. Zecevic N, Verney C. Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 1995, 351:509-535.