Vulnerability of premyelinating oligodendrocytes to white-matter damage in neonatal brain injury

Neuroscience Bulletin

Volumn 29, Issue 2, 2013, Pages 229-238

  Liu, Xiao Bo ^a   Shen, Yan ^a   Plane, Jennifer M ^a   Deng, Wenbin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

myelin; neonatal brain injury; oligodendrocyte; periventricular leukomalacia; prematurity; white matter

Indexed keywords

ASTROCYTOSIS; BRAIN INJURY; CELL ACTIVATION; CELL LOSS; CELL MATURATION; CEREBRAL PALSY; DISEASE MODEL; ENCEPHALOMALACIA; EXCITOTOXICITY; GLIA; HUMAN; INFLAMMATION; MICROGLIA; MYELINATION; NEONATAL BRAIN INJURY; NERVE CELL PLASTICITY; NERVE FIBER; NEWBORN; NEWBORN PERIOD; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PATHOGENESIS; PREMATURITY; REVIEW; SYNAPSE; WHITE MATTER INJURY;

ANIMALS; BRAIN INJURIES; CELL SURVIVAL; DISEASE MODELS, ANIMAL; HUMANS; INFANT; LEUKOENCEPHALOPATHIES; MICE; MYELIN SHEATH; OLIGODENDROGLIA; PREMATURE BIRTH;

EID: 84877873987     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-013-1311-5     Document Type: Review

References (55)

1. Hack M, Wilson-Costello D, Friedman H, Taylor GH, Schluchter M, Fanaroff AA. Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g: 1992-1995. Arch Pediatr Adolesc Med 2000, 154: 725-731.
2. Silbereis JC, Huang EJ, Back SA, Rowitch DH. Towards improved animal models of neonatal white matter injury associated with cerebral palsy. Dis Model Mech 2010, 3: 678-688.
3. Titomanlio L, Kavelaars A, Dalous J, Mani S, El Ghouzzi V, Heijnen C, et al. Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann Neurol 2011, 70: 698-712.
4. Volpe JJ. Neurology of the Newborn, 4th ed. Philadelphia: WB Saunders, 2001: 217-276.
5. Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009, 8: 110-124.
6. Banker BQ, Larroche JC. Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch Neurol 1962, 7: 386-410.
7. Leviton A, Gilles FH. Acquired perinatal leukoencephalopathy. Ann Neurol 1984, 16: 1-8.
8. Gilles FH, Averill DR Jr, Kerr CS. Neonatal endotoxin encephalopathy. Ann Neurol 1977, 2: 49-56.
9. Deng W, Pleasure J, Pleasure D. Progress in periventricular leukomalacia. Arch Neurol 2008, 65: 1291-1295.
10. Pleasure D, Soulika A, Singh SK, Gallo V, Bannerman P. Inflammation in white matter: clinical and pathophysiological aspects. Ment Retard Dev Disabil Res Rev 2006, 12: 141-146.
11. Deng W. Neurobiology of injury to the developing brain. Nat Rev Neurol 2010, 6: 328-336.
12. Back SA, Luo NL, Borenstein NS, Levine JM, Volpe JJ, Kinney HC. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001, 21: 1302-1312.
13. Kinney HC, Back SA. Human oligodendroglial development: relationship to periventricular leukomalacia. Semin Pediatr Neurol 1998, 5: 180-189.
14. Levine JM, Reynolds R, Fawcett JW. The oligodendrocyte precursor cell in health and disease. Trends Neurosci 2001, 24: 39-47.
15. Pfeiffer SE, Warrington AE, Bansal R. The oligodendrocyte and its many cellular processes. Trends Cell Biol 1993, 3: 191-197.
16. Raff MC, Miller RH, Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 1983, 303: 390-396.
17. Deng W, Poretz RD. Oligodendroglia in developmental neurotoxicity. Neurotoxicology 2003, 24: 161-178.
18. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ. Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 1993, 13: 1441-1453.
19. DeSilva TM, Kabakov AY, Goldhoff PE, Volpe JJ, Rosenberg PA. Regulation of glutamate transport in developing rat oligodendrocytes. J Neurosci 2009, 29: 7898-7908.
20. Back SA, Craig A, Kayton RJ, Luo NL, Meshul CK, Allcock N, et al. Hypoxia-ischemia preferentially triggers glutamate depletion from oligodendroglia and axons in perinatal cerebral white matter. J Cereb Blood Flow Metab 2007, 27: 334-347.
21. Desilva TM, Kinney HC, Borenstein NS, Trachtenberg FL, Irwin N, Volpe JJ, et al. The glutamate transporter EAAT2 is transiently expressed in developing human cerebral white matter. J Comp Neurol 2007, 501: 879-890.
22. Shen Y, Liu XB, Pleasure DE, Deng W. Axon-glia synapses are highly vulnerable to white matter injury in the developing brain. J Neurosci Res 2012, 90: 105-121.
23. Shen Y, Plane JM, Deng W. Mouse models of periventricular leukomalacia. J Vis Exp 2010. doi: 10. 3791/1951.
24. Lehnardt S, Henneke P, Lien E, Kasper DL, Volpe JJ, Bechmann I, et al. A mechanism for neurodegeneration induced by group B streptococci through activation of the TLR2/MyD88 pathway in microglia. J Immunol 2006, 177: 583-592.
25. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, et al. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002, 22: 2478-2486.
26. Billiards SS, Haynes RL, Folkerth RD, Trachtenberg FL, Liu LG, Volpe JJ, et al. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 2006, 497: 199-208.
27. Pitt D, Nagelmeier IE, Wilson HC, Raine CS. Glutamate uptake by oligodendrocytes: Implications for excitotoxicity in multiple sclerosis. Neurology 2003, 61: 1113-1120.
28. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 2000, 20: 6804-6810.
29. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 1999, 51: 7-61.
30. Lipton SA, Rosenberg PA. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 1994, 330: 613-622.
31. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, et al. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 2002, 81: 390-402.
32. Matute C, Sanchez-Gomez MV, Martinez-Millan L, Miledi R. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci U S A 1997, 94: 8830-8835.
33. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 1998, 4: 291-297.
34. Yoshioka A, Bacskai B, Pleasure D. Pathophysiology of oligodendroglial excitotoxicity. J Neurosci Res 1996, 46: 427-437.
35. Fern R, Moller T. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 2000, 20: 34-42.
36. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, et al. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 2004, 24: 4412-4420.
37. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 2000, 20: 9235-9241.
38. Deng W, Neve RL, Rosenberg PA, Volpe JJ, Jensen FE. Alpha-amino-3- hydroxy-5-methyl-4-isoxazole propionate receptor subunit composition and cAMP-response elementbinding protein regulate oligodendrocyte excitotoxicity. J Biol Chem 2006, 281: 36004-36011.
39. Deng W, Rosenberg PA, Volpe JJ, Jensen FE. Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci U S A 2003, 100: 6801-6806.
40. Deng W, Wang H, Rosenberg PA, Volpe JJ, Jensen FE. Role of metabotropic glutamate receptors in oligodendrocyte excitotoxicity and oxidative stress. Proc Natl Acad Sci U S A 2004, 101: 7751-7756.
41. Karadottir R, Cavelier P, Bergersen LH, Attwell D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 2005, 438: 1162-1166.
42. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 2006, 439: 988-992.
43. Salter MG, Fern R. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 2005, 438: 1167-1171.
44. Haynes RL, Baud O, Li J, Kinney HC, Volpe JJ, Folkerth DR. Oxidative and nitrative injury in periventricular leukomalacia: a review. Brain Pathol 2005, 15: 225-233.
45. Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 2003, 62: 441-450.
46. Griffiths M, Neal JW, Gasque P. Innate immunity and protective neuroinflammation: new emphasis on the role of neuroimmune regulatory proteins. Int Rev Neurobiol 2007, 82: 29-55.
47. Glezer I, Zekki H, Scavone C, Rivest S. Modulation of the innate immune response by NMDA receptors has neuropathological consequences. J Neurosci 2003, 23: 11094-11103.
48. Lechpammer M, Manning SM, Samonte F, Nelligan J, Sabo E, Talos DM, et al. Minocycline treatment following hypoxic/ischaemic injury attenuates white matter injury in a rodent model of periventricular leucomalacia. Neuropathol Appl Neurobiol 2008, 34: 379-393.
49. Liu W, Shen Y, Plane JM, Pleasure DE, Deng W. Neuroprotective potential of erythropoietin and its derivative carbamylated erythropoietin in periventricular leukomalacia. Exp Neurol 2011, 230: 227-239.
50. Fields RD. Myelination: an overlooked mechanism of synaptic plasticity? Neuroscientist 2005, 11: 528-531.
51. Anjari M, Srinivasan L, Allsop JM, Hajnal JV, Rutherford MA, Edwards AD, et al. Diffusion tensor imaging with tract-based spatial statistics reveals local white matter abnormalities in preterm infants. Neuroimage 2007, 35: 1021-1027.
52. Arzoumanian Y, Mirmiran M, Barnes PD, Woolley K, Ariagno RL, Moseley ME, et al. Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol 2003, 24: 1646-1653.
53. Inder TE, Huppi PS, Warfield S, Kikinis R, Zientara GP, Barnes PD, et al. Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann Neurol 1999, 46: 755-760.
54. Inder TE, Wells SJ, Mogridge NB, Spencer C, Volpe JJ. Defining the nature of the cerebral abnormalities in the premature infant: a qualitative magnetic resonance imaging study. J Pediatr 2003, 143: 171-179.
55. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000, 284: 1939-1947.