Role of microglia in the process of inflammation in the hypoxic developing brain

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 3, 2011, Pages 884-900

  Deng, Yi Yu ^a   Lu, Jia ^b   Ling, Eng Ang ^a   Kaur, Charanjit ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b DSO NATIONAL LABORATORIES   (Singapore)

Author keywords

Hypoxia; Inflammation; Microglia; Periventricular White Matter Damage; Review

Indexed keywords

COLONY STIMULATING FACTOR; COLONY STIMULATING FACTOR 1; CYTOCHROME P450; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GUANYLATE CYCLASE; HEMOGLOBIN; INTERLEUKIN 1; INTERLEUKIN 1BETA; INTERLEUKIN 3; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELIN BASIC PROTEIN; NITROGEN; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; SODIUM CHANNEL; SYNDECAN 2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; VOLTAGE GATED SODIUM CHANNEL; CHEMOKINE; CYTOKINE; ION CHANNEL;

ANTIGEN PRESENTATION; ARTICLE; ASTROCYTE; ASTROCYTOSIS; AXONAL INJURY; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN HYPOXIA; BRAIN INJURY; CALCIUM TRANSPORT; CELL MIGRATION; CELL PROLIFERATION; EXCITOTOXICITY; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; LEUKOCYTE; MACROGLIA; MICROENVIRONMENT; MICROGLIA; MUSCLE RELAXATION; MYELINATION; NERVE FIBER DEGENERATION; NONHUMAN; OLIGODENDROGLIA; PERINATAL ASPHYXIA; PHAGOCYTOSIS; PLACENTA INSUFFICIENCY; POSTNATAL DEVELOPMENT; PURKINJE CELL; SYNAPTIC TRANSMISSION; WHITE MATTER; BRAIN; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INJURY; METABOLISM; NERVE FIBER; PATHOLOGY; REVIEW;

AXONS; BLOOD-BRAIN BARRIER; BRAIN; CHEMOKINES; CYTOKINES; HUMANS; HYPOXIA, BRAIN; INFLAMMATION; ION CHANNELS; MICROGLIA; OLIGODENDROGLIA; REACTIVE OXYGEN SPECIES;

EID: 80053103017     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: None     Document Type: Article

References (189)

1. Acker T, Acker H. Cellular oxygen sensing need in CNS function: Physiological and pathological implications. J Exp Biol 207, 3171-3188 (2004)
2. Michiels C. Physiological and pathological responses to hypoxia. Am J Pathol. 164, 1875-1882 (2004)
3. Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 77, 731-758 (1997)
4. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. 21, 1133-1145 (2001)
5. Perlman JM. Intervention strategies for neonatal hypoxic-ischemic cerebral injury. Clin Ther. 28,1353-1365 (2006)
6. Taniguchi H, Andreasson K. The hypoxic-ischemic encephalopathy model of perinatal ischemia. J Vis Exp. 19, pii: 955. doi: 10.3791/955 (2008)
7. Osredkar D, Derganc M, Paro-Panjan D, Neubauer D. Amplitude-integrated electroencephalography in full-term newborns without severe hypoxic-ischemic encephalopathy: Case series. Croat Med J. 47, 285-291 (2006)
8. Johnston MV. Hypoxic and ischemic disorders of infants and children. Lecture for 38th meeting of Japanese Society of Child Neurology, Tokyo, Japan, July 1996. Brain Dev. 19, 235-239 (1997)
9. McQuillen PS, Ferriero DM. Selective vulnerability in the developing central nervous system. Pediatr Neurol. 30, 227-235 (2004)
10. Rezaie P, Dean A. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology. 22, 106-132 (2002)
11. Volpe JJ. Cerebral white matter injury of the premature infant-more common than you think. Pediatrics. 112, 176-180 (2003)
12. Folkerth RD. Periventricular leukomalacia: Overview and recent findings. Pediatr Dev Pathol. 9, 3-13 (2006)
13. Verklan MT. The chilling details: Fypoxic-ischemic encephalopathy. J Perinat Neonatal Nurs. 23, 59-68 (2009)
14. Kaur C, Ling EA. Antioxidants and neuroprotection in the adult and developing central nervous system. Curr Med Chem. 15, 3068-3080 (2008)
15. Cinat M, Waxman K, Vaziri ND, Daughters K, Yousefi S, Scannell G, Tominaga GT. Soluble cytokine receptors and receptor antagonists are sequentially released after trauma. J Trauma. 39, 112-118 (1995)
16. Ghirnikar RS, Lee YL, Eng LF. Inflammation in traumatic brain injury: Role of cytokines and chemokines. Neurochem Res. 23, 329-340 (1998)
17. Martin C, Boisson C, Haccoun M, Thomachot L, Mege JL. Patterns of cytokine evolution (tumor necrosis factoralpha and interleukin-6) after septic shock, hemorrhagic shock, and severe trauma. Crit Care Med. 25, 1813-1819 (1997)
18. Delgado M, Ganea D. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: Potential therapeutic role in brain trauma. FASEB J. 17, 1922-1924 (2003)
19. Kaur C, Hao AJ, Wu CH, Ling EA. Origin of microglia. Microsc Res Tech. 54, 2-9 (2001)
20. Ling EA, Wong WC. The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia. 7, 9-18 (1993)
21. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci. 6, 2163-2178 (1986)
22. Napoli I, Neumann H. Protective effects of microglia in multiple sclerosis. Exp Neurol. 225, 24-28 (2009)
23. Kaur C, Ling EA. Periventricular white matter damage in the hypoxic neonatal brain: Role of microglial cells. Prog Neurobiol. 87, 264-280 (2009)
24. Deng Y, Lu J, Sivakumar V, Ling EA, Kaur C. Amoeboid microglia in the periventricular white matter induce oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signaling pathway in hypoxic neonatal rats. Brain Pathol. 18, 387-400 (2008)
25. Neumar RW. Molecular mechanisms of ischemic neuronal injury. Ann Emerg Med. 36, 483-506 (2000)
26. Calvert JW, Zhang JH. Pathophysiology of an hypoxicischemic insult during the perinatal period. Neurol Res. 27, 246-260 (2005)
27. Valkounova I, Maresova D, Trojan S. Perinatal complication: Fypoxic-ischemic encephalopathy. Sb Lek. 102, 455-463 (2001)
28. Cervós-Navarro J, Diemer NH. Selective vulnerability in brain hypoxia. Crit Rev Neurobiol. 6, 149-182 (1991)
29. Johnston MV, Trescher WH, Taylor GA. Hypoxic and ischemic central nervous system disorders in infants and children. Adv Pediatr. 42, 1-45 (1995)
30. Volpe JJ. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res. 50, 553-562 (2001)
31. Kaur C, Sivakumar V, Ang LS, Sundaresan A. Hypoxic damage to the periventricular white matter in neonatal brain: Role of vascular endothelial growth factor, nitric oxide and excitotoxicity. J Neurochem. 98, 1200-1216 (2006)
32. Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci. 22, 455-463 (2002)
33. Volpe JJ. Brain injury in the premature infant-Current concepts. Prev Med. 23, 638-645 (1994)
34. Baud O, Li J, Zhang Y, Neve RL, Volpe JJ, Rosenberg PA. Nitric oxide-induced cell death in developing oligodendrocytes is associated with mitochondrial dysfunction and apoptosis-inducing factor translocation. Eur J Neurosci. 20, 1713-1726 (2004)
35. Golan H, Kashtuzki I, Hallak M, Sorokin Y, Huleihel M. Maternal hypoxia during pregnancy induces fetal neurodevelopmental brain damage: Partial protection by magnesium sulfate. J Neurosci Res. 78, 430-441 (2004)
36. Sugai K, Ito M, Tateishi I, Funabiki T, Nishikawa M. Neonatal periventricular leukomalacia due to severe, poorly controlled asthma in the mother. Allergol Int. 55, 207-212 (2006)
37. Mu D, Jiang X, Sheldon RA, Fox CK, Hamrick SE, Vexler ZS, Ferriero DM. Regulation of hypoxia-inducible factor 1alpha and induction of vascular endothelial growth factor in a rat neonatal stroke model. Neurobiol Dis. 14, 524-534 (2003)
38. Mac Donald D. Asphyxia. Baillieres Clin Obstet Gynaecol. 9, 579-594 (1995)
39. As-Sanie S, Mercer B, Moore J. The association between respiratory distress and nonpulmonary morbidity at 34 to 36 weeks' gestation. Am J Obstet Gynecol. 189, 1053-1057 (2003)
40. Towfighi J, Mauger D, Vannucci RC, Vannucci SJ. Influence of age on the cerebral lesions in an immature rat model of cerebral hypoxia-ischemia: A light microscopic study. Brain Res Dev Brain Res. 100, 149-160 (1997)
41. Nakajima W, Ishida A, Lange MS, Gabrielson KL, Wilson MA, Martin LJ, Blue ME, Johnston MV. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci. 20, 7994-8004 (2000)
42. Sheldon RA, Hall JJ, Noble LJ, Ferriero DM. Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic. Neurosci Lett. 304, 165-168 (2001)
43. Towfighi J, Yager JY, Housman C, Vannucci RC. Neuropathology of remote hypoxic-ischemic damage in the immature rat. Acta Neuropathol. 81, 578-587 (1991)
44. Northington FJ, Ferriero DM, Graham EM, Traystman RJ, Martin LJ. Early neurodegeneration after hypoxiaischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis. 8, 207-219 (2001)
45. Taylor RM, Lee JP, Palacino JJ, Bower KA, Li J, Vanier MT, Wenger DA, Sidman RL, Snyder EY. Intrinsic resistance of neural stem cells to toxic metabolites may make them well suited for cell nonautonomous disorders: evidence from a mouse model of Krabbe leukodystrophy. J Neurochem. 97, 1585-1599 (2006)
46. Rees S, Inder T. Fetal and neonatal origins of altered brain development. Early Hum Dev. 81, 753-761 (2005)
47. Johnston MV, Nakajima W, Hagberg H. Mechanisms of hypoxic neurodegeneration in the developing brain. Neuroscientist. 8, 212-220 (2002)
48. Choi DW. Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol. 6, 667-672 (1996)
49. Bernert G, Hoeger H, Mosgoeller W, Stolzlechner D, Lubec B. Neurodegeneration, neuronal loss, and neurotransmitter changes in the adult guinea pig with perinatal asphyxia. Pediatr Res. 54, 523-528 (2003)
50. Somjen GG, Aitken PG, Czeh G, Jing J, Young JN. Cellular physiology of hypoxia of the mammalian central nervous system. Res Publ Assoc Res Nerv Ment Dis. 71, 51-65 (1993)
51. Charriaut-Marlangue C, Remolleau S, ggoun-Zouaoui D, Ben-Ari Y. Apoptosis and programmed cell death: A role in cerebral ischemia. Biomed Pharmacother. 52, 264-269 (1998)
52. Zanelli SA, Numagami Y, McGowan JE, Mishra OP, ivoria-Papadopoulos M. NMDA receptor-mediated calcium influx in cerebral cortical synaptosomes of the hypoxic guinea pig fetus. Neurochem Res. 24, 437-446 (1999)
53. Biagas K. Hypoxic-ischemic brain injury: Advancements in the understanding of mechanisms and potential avenues for therapy. Curr Opin Pediatr. 11, 223-228 (1999)
54. Erecinska M, Silver IA. Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol. 128, 263-276 (2001)
55. Beilharz EJ, Williams CE, Dragunow M, Sirimanne ES, Gluckman PD. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Brain Res Mol Brain Res. 29, 1-14 (1995)
56. Edwards AD, Yue X, Cox P, Hope PL, Azzopardi DV, Squier MV, Mehmet H. Apoptosis in the brains of infants suffering intrauterine cerebral injury. Pediatr Res. 42, 684-689 (1997)
57. Paterson JA, Privat A, Ling EA, Leblond CP. Investigation of glial cells in semithin sections. 3. Transformation of subependymal cells into glial cells, as shown by radioautography after 3 H-thymidine injection into the lateral ventricle of the brain of young rats. J Comp Neurol. 149, 83-102 (1973)
58. Thomas JL, Spassky N, Perez Villegas EM, Olivier C, Cobos I, Goujet-Zalc C, Martinez S, Zalc B. Spatiotemporal development of oligodendrocytes in the embryonic brain. J Neurosci Res. 59, 471-476 (2000)
59. Baumann N, Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev. 81, 871-927 (2001)
60. Kinney HC, Back SA. Human oligodendroglial development: Relationship to periventricular leukomalacia. Semin Pediatr Neurol. 5, 180-189 (1998)
61. Kohlhauser C, Mosgoller W, Hoger H, Lubec B. Myelination deficits in brain of rats following perinatal asphyxia. Life Sci. 67, 2355-2368 (2000)
62. Skoff RP, Bessert DA, Barks JD, Song D, Cerghet M, Silverstein FS. Hypoxic-ischemic injury results in acute disruption of myelin gene expression and death of oligodendroglial precursors in neonatal mice. Int J Dev Neurosci. 19, 197-208 (2001)
63. Back SA. Perinatal white matter injury: The changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev. 12, 129-140 (2006)
64. Mitrovic B, Parkinson J, Merrill JE. An in vitro Model of Oligodendrocyte Destruction by Nitric Oxide and Its Relevance to Multiple Sclerosis. Methods. 10, 501-513 (1996)
65. Ludwin SK. The pathobiology of the oligodendrocyte. J Neuropathol Exp Neurol. 56, 111-124 (1997)
66. Casaccia-Bonnefil P. Cell death in the oligodendrocyte lineage: A molecular perspective of life/death decisions in development and disease. Glia. 29, 124-135 (2000)
67. Deng YY, Lu J, Ling EA, Kaur C. Microglia-Derived macrophage colony stimulating factor promotes generation of proinflammatory cytokines by astrocytes in the periventricular white matter in the hypoxic neonatal brain. Brain Pathol. 20, 909-925 (2010)
68. Fern R, Davis P, Waxman SG, Ransom BR. Axon conduction and survival in CNS white matter during energy deprivation: A developmental study. J Neurophysiol. 79, 95-105 (1998)
69. Stys PK. General mechanisms of axonal damage and its prevention. J Neurol Sci. 233, 3-13 (2005)
70. Cuthill DJ, Fowler JH, McCulloch J, Dewar D. Different patterns of axonal damage after intracerebral injection of malonate or AMPA. Exp Neurol. 200, 509-520 (2006)
71. McCarran WJ, Goldberg MP. White matter axon vulnerability to AMPA/kainate receptor-mediated ischemic injury is developmentally regulated. J Neurosci. 27, 4220-4229 (2007)
72. Fowler JH, Edgar JM, Pringle A, McLaughlin M, McCulloch J, Griffiths IR, Garbern JY, Nave KA, Dewar D. Alpha-Amino-3-hydroxy-5-methylisoxazole-4- propionic acid-mediated excitotoxic axonal damage is attenuated in the absence of myelin proteolipid protein. J Neurosci Res. 84, 68-77 (2006)
73. Tezel G. TNF-Alpha signaling in glaucomatous neurodegeneration. Prog Brain Res. 173, 409-421 (2008)
74. Kaur C, Ling EA. Blood brain barrier in hypoxicischemic conditions. Curr Neurovasc Res. 5, 71-81 (2008)
75. Li JJ, Lu J, Kaur C, Sivakumar V, Wu CY, Ling EA. Effects of hypoxia on expression of transforming growth factor-Beta1 and its receptors I and II in the amoeboid microglial cells and murine BV-2 cells. Neuroscience. 156, 662-672 (2008)
76. Li JJ, Lu J, Kaur C, Sivakumar V, Wu CY, Ling EA. Expression of angiotensin II and its receptors in the normal and hypoxic amoeboid microglial cells and murine BV-2 cells. Neuroscience. 158, 1488-1499 (2009)
77. Farber K, Kettenmann H. Functional role of calcium signals for microglial function. Glia. 54, 656-665 (2006)
78. Dheen ST, Jun Y, Yan Z, Tay SS, Ling EA. Retinoic acid inhibits expression of TNF-Alpha and iNOS in activated rat microglia. Glia. 50, 21-31 (2005)
79. Hanisch UK, Kettenmann H. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 10, 1387-1394 (2007)
80. Panickar KS, Norenberg MD. Astrocytes in cerebral ischemic injury: Morphological and general considerations. Glia. 50, 287-298 (2005)
81. Yu AC, Lee YL, Eng LF. Astrogliosis in culture: I. The model and the effect of antisense oligonucleotides on glial fibrillary acidic protein synthesis. J Neurosci Res. 34, 295-303 (1993)
82. Deguchi K, Oguchi K, Takashima S. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol. 16, 296-300 (1997)
83. Davies SJ, Goucher DR, Doller C, Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci. 19, 5810-5822 (1999)
84. Di GS, Movsesyan V, Ahmed F, Cernak I, Schinelli S, Stoica B, Faden AI. Cell cycle inhibition provides neuroprotection and reduces glial proliferation and scar formation after traumatic brain injury. Proc Natl Acad Sci USA. 102, 8333-8338 (2005)
85. Brown RC, Mark KS, Egleton RD, Davis TP. Protection against hypoxia-induced blood-Brain barrier disruption: Changes in intracellular calcium. Am J Physiol Cell Physiol. 286, C1045-C1052 (2004)
86. Fischer S, Clauss M, Wiesnet M, Renz D, Schaper W, Karliczek GF. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am J Physiol. 276, C812-C820 (1999)
87. Mark KS, Davis TP. Cerebral microvascular changes in permeability and tight junctions induced by hypoxiareoxygenation. Am J Physiol Heart Circ Physiol. 282, H1485-H1494 (2002)
88. Kaur C, Sivakumar V, Zhang Y, Ling EA. Hypoxiainduced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia. 54, 826-839 (2006)
89. Kaur C, Sivakumar V, Ling EA. Melatonin protects periventricular white matter from damage due to hypoxia. J Pineal Res. 48, 185-193 (2010)
90. Saed GM, Munkarah AR, bu-Soud HM, Diamond MP. Hypoxia upregulates cyclooxygenase-2 and prostaglandin E(2) levels in human peritoneal fibroblasts. Fertil Steril. 83 Suppl 1, 1216-1219 (2005)
91. Varez-Diaz A, Hilario E, de Cerio FG, Soler A, varez-Diaz FJ. Hypoxic-ischemic injury in the immature brain-key vascular and cellular players. Neonatology. 92, 227-235 (2007)
92. Dammann O, Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res. 42, 1-8 (1997)
93. Yoon BH, Romero R, Kim CJ, Koo JN, Choe G, Syn HC, Chi JG. High expression of tumor necrosis factoralpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol. 177, 406-411 (1997)
94. Kadhim H, Tabarki B, De PC, Sebire G. Cytokine immunoreactivity in cortical and subcortical neurons in periventricular leukomalacia: Are cytokines implicated in neuronal dysfunction in cerebral palsy? Acta Neuropathol. 105, 209-216 (2003)
95. Ling EA, Leblond CP. Investigation of glial cells in semithin sections. II. Variation with age in the numbers of the various glial cell types in rat cortex and corpus callosum. J Comp Neurol. 149, 73-81 (1973)
96. Lawson LJ, Perry VH, Gordon S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience. 48, 405-415 (1992)
97. Benveniste EN. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J Mol Med. 75, 165-173 (1997)
98. Perry VH, Hume DA, Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience. 15, 313-326 (1985)
99. Ling EA, Ng YK, Wu CH, Kaur C. Microglia: Its development and role as a neuropathology sensor. Prog Brain Res. 132, 61-79 (2001)
100. Dheen ST, Kaur C, Ling EA. Microglial activation and its implications in the brain diseases. Curr Med Chem. 14, 1189-1197 (2007)
101. Deng YY, Lu J, Ling EA, Kaur C. Monocyte chemoattractant protein-1 (MCP-1) produced via NF-kappaB signaling pathway mediates migration of amoeboid microglia in the periventricular white matter in hypoxic neonatal rats. Glia. 57, 604-621 (2009)
102. Kaur C, Too HF, Ling EA. Phagocytosis of Escherichia coli by amoeboid microglial cells in the developing brain. Acta Neuropathol. 107, 204-208 (2004)
103. Ling EA, Tseng CY, Voon FC, Wong WC. Isolation and culture of amoeboid microglial cells from the corpus callosum and cavum septum pellucidum in postnatal rats. J Anat. 137 (Pt 2), 223-233 (1983)
104. Li YB, Kaur C, Ling EA. Neuronal degeneration and microglial reaction in the fetal and postnatal rat brain after transient maternal hypoxia. Neurosci Res. 32, 137-148 (1998)
105. Kaur C, You Y. Ultrastructure and function of the amoeboid microglial cells in the periventricular white matter in postnatal rat brain following a hypoxic exposure. Neurosci Lett. 290, 17-20 (2000)
106. Xu J, Ling EA. Upregulation and induction of major histocompatibility complex class I and II antigens on microglial cells in early postnatal rat brain following intraperitoneal injections of recombinant interferon-Gamma. Neuroscience. 60, 959-967 (1994)
107. Xu J, Ling EA. Expression of major histocompatibility complex class II antigen on amoeboid microglial cells in early postnatal rat brain following intraperitoneal injections of lipopolysaccharide. Exp Brain Res. 100, 287-292 (1994)
108. Kaur C, Dheen ST, Ling EA. From blood to brain: Amoeboid microglial cell, a nascent macrophage and its functions in developing brain. Acta Pharmacol Sin. 28, 1087-1096 (2007)
109. Ladeby R, Wirenfeldt M, Dalmau I, Gregersen R, Garcia-Ovejero D, Babcock A, Owens T, Finsen B. Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury. Glia. 50, 121-131 (2005)
110. Ladeby R, Wirenfeldt M, Garcia-Ovejero D, Fenger C, ssing-Olesen L, Dalmau I, Finsen B. Microglial cell population dynamics in the injured adult central nervous system. Brain Res Brain Res Rev. 48,196-206 (2005)
111. Urrea C, Castellanos DA, Sagen J, Tsoulfas P, Bramlett HM, Dietrich WD. Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor Neurol Neurosci. 25, 65-76 (2007)
112. Denes A, Vidyasagar R, Feng J, Narvainen J, McColl BW, Kauppinen RA, Allan SM. Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab. 27, 1941-1953 (2007)
113. Henze C, Hartmann A, Lescot T, Hirsch EC, Michel PP. Proliferation of microglial cells induced by 1-methyl-4-phenylpyridinium in mesencephalic cultures results from an astrocyte-Dependent mechanism: Role of granulocyte macrophage colony-stimulating factor. J Neurochem. 95, 1069-1077 (2005)
114. Remington LT, Babcock AA, Zehntner SP, Owens T. Microglial recruitment, activation, and proliferation in response to primary demyelination. Am J Pathol. 170, 1713-1724 (2007)
115. Byrnes KR, Faden AI. Role of cell cycle proteins in CNS injury. Neurochem Res. 32, 1799-1807 (2007)
116. Sawada M, Suzumura A, Yamamoto H, Marunouchi T. Activation and proliferation of the isolated microglia by colony stimulating factor-1 and possible involvement of protein kinase C. Brain Res. 509,119-124 (1990)
117. Schobitz B, de Kloet ER, Sutanto W, Holsboer F. Cellular localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Eur J Neurosci. 5, 1426-1435 (1993)
118. Zhou Y, Ling EA, Dheen ST. Dexamethasone suppresses monocyte chemoattractant protein-1 production via mitogen activated protein kinase phosphatase-1 dependent inhibition of Jun N-terminal kinase and p38 mitogen-Activated protein kinase in activated rat microglia. J Neurochem. 102, 667-678 (2007)
119. Brockhaus J, Moller T, Kettenmann H. Phagocytozing ameboid microglial cells studied in a mouse corpus callosum slice preparation. Glia. 16, 81-90 (1996)
120. Lazar G, Pal E. Removal of cobalt-labeled neurons and nerve fibers by microglia from the frog's brain and spinal cord. Glia. 16, 101-107 (1996)
121. Eugenin EA, Dyer G, Calderon TM, Berman JW. HIV-1 tat protein induces a migratory phenotype in human fetal microglia by a CCL2 (MCP-1)-Dependent mechanism: Possible role in NeuroAIDS. Glia. 49, 501-510 (2005)
122. Hanisch UK. Microglia as a source and target of cytokines. Glia. 40, 140-155 (2002)
123. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci. 4, 1116-1122 (2001)
124. Andrews T, Zhang P, Bhat NR. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res. 54, 574-583 (1998)
125. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI. Tumor necrosis factor-Alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci. 26, 12633-12641 (2006)
126. Ledgerwood EC, Pober JS, Bradley JR. Recent advances in the molecular basis of TNF signal transduction. Lab Invest. 79, 1041-1050 (1999)
127. Grehan S, Uhlar CM, Sim RB, Herbert J, Whitehead AS. Expression of a biologically active recombinant mouse IL-1 receptor antagonist and its use in vivo to modulate aspects of the acute phase response. J Immunol. 159, 369-378 (1997)
128. Vela JM, Molina-Holgado E, revalo-Martin A, Almazan G, Guaza C. Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol Cell Neurosci. 20, 489-502 (2002)
129. Stanley ER, Berg KL, Einstein DB, Lee PS, Pixley FJ, Wang Y, Yeung YG. Biology and action of colony-stimulating factor-1. Mol Reprod Dev. 46, 4-10 (1997)
130. Hao AJ, Dheen ST, Ling EA. Expression of macrophage colony-stimulating factor and its receptor in microglia activation is linked to teratogen-induced neuronal damage. Neuroscience. 112, 889-900 (2002)
131. Rovida E, Spinelli E, Sdelci S, Barbetti V, Morandi A, Giuntoli S, Dello SP. ERK5/BMK1 is indispensable for optimal colony-stimulating factor 1 (CSF-1)-induced proliferation in macrophages in a Src-Dependent fashion. J Immunol. 180, 4166-4172 (2008)
132. Taub DD, Proost P, Murphy WJ, Anver M, Longo DL, Van DJ, Oppenheim JJ. Monocyte chemotactic protein-1 (MCP-1),-2, and-3 are chemotactic for human T lymphocytes. J Clin Invest. 95, 1370-1376 (1995)
133. Gunn MD, Nelken NA, Liao X, Williams LT. Monocyte chemoattractant protein-1 is sufficient for the chemotaxis of monocytes and lymphocytes in transgenic mice but requires an additional stimulus for inflammatory activation. J Immunol. 158, 376-383 (1997)
134. Babcock AA, Kuziel WA, Rivest S, Owens T. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci. 23, 7922-7930 (2003)
135. Hayashi M, Luo Y, Laning J, Strieter RM, Dorf ME. Production and function of monocyte chemoattractant protein-1 and other beta-Chemokines in murine glial cells. J Neuroimmunol. 60, 143-150 (1995)
136. Che X, Ye W, Panga L, Wu DC, Yang GY. Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice. Brain Res. 902, 171-177 (2001)
137. Minami M, Satoh M. Chemokines and their receptors in the brain: Pathophysiological roles in ischemic brain injury. Life Sci. 74, 321-327 (2003)
138. Fenoglio C, Galimberti D, Lovati C, Guidi I, Gatti A, Fogliarino S, Tiriticco M, Mariani C, Forloni G, Pettenati C, Baron P, Conti G, Bresolin N, Scarpini E. MCP-1 in Alzheimer's disease patients: A-2518G polymorphism and serum levels. Neurobiol Aging. 25, 1169-1173 (2004)
139. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO. Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci USA. 95, 3117-3121 (1998)
140. Simpson JE, Newcombe J, Cuzner ML, Woodroofe MN. Expression of monocyte chemoattractant protein-1 and other beta-Chemokines by resident glia and inflammatory cells in multiple sclerosis lesions. J Neuroimmunol. 84, 238-249 (1998)
141. Sorensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest. 103, 807-815 (1999)
142. Glabinski AR, Bielecki B, Ransohoff RM. Chemokine upregulation follows cytokine expression in chronic relapsing experimental autoimmune encephalomyelitis. Scand J Immunol. 58, 81-88 (2003)
143. Ambrosini E, Aloisi F. Chemokines and glial cells: A complex network in the central nervous system. Neurochem Res. 29, 1017-1038 (2004)
144. Calvo CF, Yoshimura T, Gelman M, Mallat M. Production of monocyte chemotactic protein-1 by rat brain macrophages. Eur J Neurosci 8:1725-1734 (1996)
145. Muessel MJ, Klein RM, Wilson AM, Berman NE. Ablation of the chemokine monocyte chemoattractant protein-1 delays retrograde neuronal degeneration, attenuates microglial activation, and alters expression of cell death molecules. Brain Res Mol Brain Res. 103, 12-27 (2002)
146. Hughes PM, Allegrini PR, Rudin M, Perry VH, Mir AK, Wiessner C. Monocyte chemoattractant protein-1 deficiency is protective in a murine stroke model. J Cereb Blood Flow Metab. 22, 308-317 (2002)
147. 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. 55, 17-23 (1999)
148. Husemann J, Loike JD, Anankov R, Febbraio M, Silverstein SC. Scavenger receptors in neurobiology and neuropathology: Their role on microglia and other cells of the nervous system. Glia. 40, 195-205 (2002)
149. Cartier L, Hartley O, Dubois-Dauphin M, Krause KH. Chemokine receptors in the central nervous system: Role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev. 48, 16-42 (2005)
150. Imai Y, Kohsaka S. Intracellular signaling in M-CSFinduced microglia activation: Role of Iba1. Glia. 40, 164-174 (2002)
151. Sperlagh B, Zsilla G, Baranyi M, Illes P, Vizi ES. Purinergic modulation of glutamate release under ischemiclike conditions in the hippocampus. Neuroscience. 149, 99-111 (2007)
152. Kettenmann H, Hoppe D, Gottmann K, Banati R, Kreutzberg G. Cultured microglial cells have a distinct pattern of membrane channels different from peritoneal macrophages. J Neurosci Res. 26, 278-287 (1990)
153. Eder C. Ion channels in microglia (brain macrophages) Am J Physiol. 275, C327-C342 (1998)
154. Li F, Lu J, Wu CY, Kaur C, Sivakumar V, Sun J, Li S, Ling EA. Expression of Kv1.2 in microglia and its putative roles in modulating production of proinflammatory cytokines and reactive oxygen species. J Neurochem. 106, 2093-2105 (2008)
155. Kaur C, Sivakumar V, Dheen ST, Ling EA. Insulin-like growth factor I and II expression and modulation in amoeboid microglial cells by lipopolysaccharide and retinoic acid. Neuroscience. 138, 1233-1244 (2006)
156. Wu CY, Kaur C, Lu J, Cao Q, Guo CH, Zhou Y, Sivakumar V, Ling EA. Transient expression of endothelins in the amoeboid microglial cells in the developing rat brain. Glia. 54, 513-525 (2006)
157. Prentice HM, Milton SL, Scheurle D, Lutz PL. Gene transcription of brain voltage-Gated potassium channels is reversibly regulated by oxygen supply. Am J Physiol Regul Integr Comp Physiol. 285, R1317-R1321 (2003)
158. Conforti L, Bodi I, Nisbet JW, Millhorn DE. O2-sensitive K+ channels: Role of the Kv1.2-subunit in mediating the hypoxic response. J Physiol. 524 Pt 3, 783-793 (2000)
159. Wu CY, Kaur C, Sivakumar V, Lu J, Ling EA. Kv1.1 expression in microglia regulates production and release of proinflammatory cytokines, endothelins and nitric oxide. Neuroscience. 158, 1500-1508 (2009)
160. Hodgkin AL, Huxley AF, Katz B. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol. 116, 424-448 (1952)
161. Sontheimer H, Waxman SG. Ion channels in spinal cord astrocytes in vitro. II. Biophysical and pharmacological analysis of two Na+ current types. J Neurophysiol. 68, 1001-1011 (1992)
162. Kreutzberg GW. Microglia: A sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318 (1996)
163. Black JA, Liu S, Waxman SG. Sodium channel activity modulates multiple functions in microglia. Glia. 57, 1072-1081 (2009)
164. Hsueh YP, Sheng M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-Binding protein CASK/LIN-2 during rat brain development. J Neurosci. 19, 7415-7425 (1999)
165. Gotte M, Yip GW. Heparanase, hyaluronan, and CD44 in cancers: A breast carcinoma perspective. Cancer Res. 66, 10233-10237 (2006)
166. Yip GW, Smollich M, Gotte M. Therapeutic value of glycosaminoglycans in cancer. Mol Cancer Ther. 5, 2139-2148 (2006)
167. Tumova S, Woods A, Couchman JR. Heparan sulfate proteoglycans on the cell surface: Versatile coordinators of cellular functions. Int J Biochem Cell Biol. 32, 269-288 (2000)
168. Lories V, Cassiman JJ, Van den BH, David G. Differential expression of cell surface heparan sulfate proteoglycans in human mammary epithelial cells and lung fibroblasts. J Biol Chem. 267, 1116-1122 (1992)
169. Mertens G, Cassiman JJ, Van den BH, Vermylen J, David G. Cell surface heparan sulfate proteoglycans from human vascular endothelial cells. Core protein characterization and antithrombin III binding properties. J Biol Chem. 267, 20435-20443 (1992)
170. Modrowski D, Basle M, Lomri A, Marie PJ. Syndecan-2 is involved in the mitogenic activity and signaling of granulocyte-macrophage colony-stimulating factor in osteoblasts. J Biol Chem. 275, 9178-9185 (2000)
171. Clasper S, Vekemans S, Fiore M, Plebanski M, Wordsworth P, David G, Jackson DG. Inducible expression of the cell surface heparan sulfate proteoglycan syndecan-2 (fibroglycan) on human activated macrophages can regulate fibroblast growth factor action. J Biol Chem. 274, 24113-24123 (1999)
172. Jalkanen M, Elenius K, Salmivirta M. Syndecan-A cell surface proteoglycan that selectively binds extracellular effector molecules. Adv Exp Med Biol. 313, 79-85 (1992)
173. Rosenberg RD, Shworak NW, Liu J, Schwartz JJ, Zhang L. Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J Clin Invest. 100, S67-S75 (1997)
174. Bartlett AH, Hayashida K, Park PW. Molecular and cellular mechanisms of syndecans in tissue injury and inflammation. Mol Cells. 24, 153-166 (2007)
175. Lewis C, Murdoch C. Macrophage responses to hypoxia: Implications for tumor progression and anticancer therapies. Am J Pathol. 167, 627-635 (2005)
176. Taylor CT, Colgan SP. Therapeutic targets for hypoxia-elicited pathways. Pharm Res. 16, 1498-1505 (1999)
177. Brown LF, Dubin D, Lavigne L, Logan B, Dvorak HF, Van de WL. Macrophages and fibroblasts express embryonic fibronectins during cutaneous wound healing. Am J Pathol. 142, 793-801 (1993)
178. Edwards IJ, Wagner WD, Owens RT. Macrophage secretory products selectively stimulate dermatan sulfate proteoglycan production in cultured arterial smooth muscle cells. Am J Pathol. 136, 609-621 (1990)
179. Yeaman C, Rapraeger AC. Membrane-Anchored proteoglycans of mouse macrophages: P388D1 cells express a syndecan-4-like heparan sulfate proteoglycan and a distinct chondroitin sulfate form. J Cell Physiol. 157, 413-425 (1993)
180. Edwards IJ, Xu H, Obunike JC, Goldberg IJ, Wagner WD. Differentiated macrophages synthesize a heparan sulfate proteoglycan and an oversulfated chondroitin sulfate proteoglycan that bind lipoprotein lipase. Arterioscler Thromb Vasc Biol. 15, 400-409 (1995)
181. Kaur C, Sivakumar V, Yip GW, Ling EA. Expression of syndecan-2 in the amoeboid microglial cells and its involvement in inflammation in the hypoxic developing brain. Glia. 57, 336-349 (2009)
182. Babior BM. Phagocytes and oxidative stress. Am J Med. 109, 33-44 (2000)
183. Block ML, Hong JS. Chronic microglial activation and progressive dopaminergic neurotoxicity. Biochem Soc Trans. 35, 1127-1132 (2007)
184. Shimohama S, Tanino H, Kawakami N, Okamura N, Kodama H, Yamaguchi T, Hayakawa T, Nunomura A, Chiba S, Perry G, Smith MA, Fujimoto S. Activation of NADPH oxidase in Alzheimer's disease brains. Biochem Biophys Res Commun. 273, 5-9 (2000)
185. Grisham MB, Jourd'Heuil D, Wink DA. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites:Implications in inflammation. Am J Physiol. 276, G315-G321 (1999)
186. Beckman JS. Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol. 9, 836-844 (1996)
187. You Y, Kaur C. Expression of induced nitric oxide synthase in amoeboid microglia in postnatal rats following an exposure to hypoxia. Neurosci Lett. 279, 101-104 (2000)
188. Kaur C, Sivakumar V, Lu J, Tang FR, Ling EA. Melatonin attenuates hypoxia-induced ultrastructural changes and increased vascular permeability in the developing hippocampus. Brain Pathol. 18: 533-547 (2008)
189. Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol. 151, 2132-2141 (1993)