Neuroprotective effect of oligodendrocyte precursor cell transplantation in a long-term model of periventricular leukomalacia

American Journal of Pathology

Volumn 175, Issue 6, 2009, Pages 2332-2342

  Webber, Daniel J ^a,b,c   Van Blitterswijk, Marka ^a,b   Chandran, Siddharthan ^a,b,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CELL LOSS; CELL THERAPY; CONTROLLED STUDY; ENCEPHALOMALACIA; INFLAMMATION; NERVE CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; STEM CELL TRANSPLANTATION; TISSUE;

EID: 73549124776     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.090051     Document Type: Article

References (71)

1. Back SA, Rivkees SA: Emerging concepts in periventricular white matter injury. Semin Perinatol 2004, 28:405-414
2. Drougia A, Giapros V, Krallis N, Theocharis P, Nikaki A, Tzoufi M, Andronikou S: Incidence and risk factors for cerebral palsy in infants with perinatal problems: a 15-year review. Early Hum Dev 2007, 83:541-547
3. Resch B, Vollaard E, Maurer U, Haas J, Rosegger H, Muller W: Risk factors and determinants of neurodevelopmental outcome in cystic periventricular leucomalacia. Eur J Pediatr 2000, 159:663-670
4. Pierrat V, Duquennoy C, van HI, Ernst M, Guilley N, de Vries LS: Ultrasound diagnosis and neurodevelopmental outcome of localised and extensive cystic periventricular leucomalacia. Arch Dis Child Fetal Neonatal Ed 2001, 84:F151-F156
5. Banker BQ, Larroche JC: Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch Neurol 1962, 7:386-410
6. Leviton A, Gressens P: Neuronal damage accompanies perinatal white-matter damage. Trends Neurosci 2007, 30:473-478
7. Blumenthal I: Periventricular leucomalacia: a review. Eur J Pediatr 2004, 163:435-442
8. Khwaja O, Volpe JJ: Pathogenesis of cerebral white matter injury of prematurity. Arch Dis Child Fetal Neonatal Ed 2008, 93:F153-F161
9. Volpe JJ: Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001, 50:553-562
10. Leviton A, Gilles F: Ventriculomegaly, delayed myelination, white matter hypoplasia, and "periventricular" leukomalacia: how are they related? Pediatr Neurol 1996, 15:127-136
11. Inage YW, Itoh M, Takashima S: Correlation between cerebrovascular maturity and periventricular leukomalacia. Pediatr Neurol 2000, 22:204-208
12. Nakamura Y, Okudera T, Hashimoto T: Vascular architecture in white matter of neonates: its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol 1994, 53:582-589
13. Bernardo A, Greco A, Levi G, Minghetti L: Differential lipid peroxidation, Mn superoxide, and bcl-2 expression contribute to the maturation-dependent vulnerability of oligodendrocytes to oxidative stress. J Neuropathol Exp Neurol 2003, 62:509-519
14. Karadottir R, Hamilton NB, Bakiri Y, Attwell D: Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nat Neurosci 2008, 11:450-456
15. 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 2002, 22:455-463
16. Ness JK, Romanko MJ, Rothstein RP, Wood TL, Levison SW: Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci 2001, 23:203-208
17. Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ: Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998, 18:6241-6253
18. Back SA, Riddle A, McClure MM: Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007, 38:724-730
19. Boggess KA: Pathophysiology of preterm birth: emerging concepts of maternal infection. Clin Perinatol 2005, 32:561-569
20. Cai Z, Pang Y, Lin S, Rhodes PG: Differential roles of tumor necrosis factor-alpha and interleukin-1 beta in lipopolysaccharide-induced brain injury in the neonatal rat. Brain Res 2003, 975:37-47
21. Leviton A, Paneth N, Reuss ML, Susser M, Allred EN, Dammann O, Kuban K, Van Marter LJ, Pagano M, Hegyi T, Hiatt M, Sanocka U, Shahrivar F, Abiri M, Disalvo D, Doubilet P, Kairam R, Kazam E, Kirpekar M, Rosenfeld D, Schonfeld S, Share J, Collins M, Genest D, Shen-Schwarz S: Developmental Epidemiology Network Investigators. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Pediatr Res 1999, 46:566-575
22. Cai Z, Pan ZL, Pang Y, Evans OB, Rhodes PG: Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 2000, 47:64-72
23. Pang Y, Cai Z, Rhodes PG: Disturbance of oligodendrocyte development, hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res Dev Brain Res 2003, 140:205-214
24. Kadhim H, Tabarki B, Verellen G, De PC, Rona AM, Sebire G: Inflammatory cytokines in the pathogenesis of periventricular leukomalacia. Neurology 2001, 56:1278-1284
25. Andrews T, Zhang P, Bhat NR: TNFalpha potentiates IFNgammainduced cell death in oligodendrocyte progenitors. J Neurosci Res 1998, 54:574-583
26. Cammer W: Effects of TNFalpha on immature and mature oligodendrocytes and their progenitors in vitro. Brain Res 2000, 864:213-219
27. Pang Y, Fan LW, Zheng B, Cai Z, Rhodes PG: Role of interleukin-6 in lipopolysaccharide-induced brain injury and behavioral dysfunction in neonatal rats. Neuroscience 2006, 141:745-755
28. Takahashi JL, Giuliani F, Power C, Imai Y, Yong VW: Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann Neurol 2003, 53:588-595
29. Pierson CR, Folkerth RD, Billiards SS, Trachtenberg FL, Drinkwater ME, Volpe JJ, Kinney HC: Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 2007, 114:619-631
30. Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ: Abnormal cerebral structure is present at term in premature infants. Pediatrics 2005, 115:286-294
31. 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
32. Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW, Duncan CC, Makuch RW, Gore JC, Ment LR: Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000, 284:1939-1947
33. Vannucci SJ, Hagberg H: Hypoxia-ischemia in the immature brain. J Exp Biol 2004, 207:3149-3154
34. Vannucci RC, Connor JR, Mauger DT, Palmer C, Smith MB, Towfighi J, Vannucci SJ: Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res 1999, 55:158-163
35. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE: Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 2004, 24:4412-4420
36. Cai Z, Lin S, Fan LW, Pang Y, Rhodes PG: Minocycline alleviates hypoxic-ischemic injury to developing oligodendrocytes in the neonatal rat brain. Neuroscience 2006, 137:425-435
37. Fan LW, Lin S, Pang Y, Rhodes PG, Cai Z: Minocycline attenuates hypoxia-ischemia-induced neurological dysfunction and brain injury in the juvenile rat. Eur J Neurosci 2006, 24:341-350
38. Wang X, Rousset CI, Hagberg H, Mallard C: Lipopolysaccharideinduced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 2006, 11:343-353
39. Hagberg H, Peebles D, Mallard C: Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 2002, 8:30-38
40. Fan LW, Pang Y, Lin S, Rhodes PG, Cai Z: Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neuroscience 2005, 133:159-168
41. Cai Z, Lin S, Rhodes PG: Neuroprotective effects of N- acetylaspartylglutamate in a neonatal rat model of hypoxia-ischemia. Eur J Pharmacol 2002, 437:139-145
42. Fan LW, Tien LT, Mitchell HJ, Rhodes PG, Cai Z: Alpha-phenyl-n-tertbutyl- nitrone ameliorates hippocampal injury and improves learning and memory in juvenile rats following neonatal exposure to lipopolysaccharide. Eur J Neurosci 2008, 27:1475-1484
43. Fitzgerald KA, Rowe DC, Golenbock DT: Endotoxin recognition and signal transduction by the TLR4/MD2-complex. Microbes Infect 2004, 6:1361-1367
44. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA, Volpe JJ, Vartanian T: The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002, 22:2478-2486
45. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T: Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci USA 2003, 100:8514-8519
46. Pang Y, Cai Z, Rhodes PG: Effects of lipopolysaccharide on oligodendrocyte progenitor cells are mediated by astrocytes and microglia. J Neurosci Res 2000, 62:510-520
47. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H: Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001, 13:1101-1106
48. Lindvall O, Kokaia Z: Stem cells for the treatment of neurological disorders. Nature 2006, 441:1094-1096
49. Foote AK, Blakemore WF: Inflammation stimulates remyelination in areas of chronic demyelination. Brain 2005, 128:528-539
50. Bambakidis NC, Miller RH: Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion. Spine J 2004, 4:16-26
51. Sharp J, Keirstead HS: Therapeutic applications of oligodendrocyte precursors derived from human embryonic stem cells. Curr Opin Biotechnol 2007, 18:434-440
52. Zhao C, Zawadzka M, Roulois AJ, Bruce CC, Franklin RJ: Promoting remyelination in multiple sclerosis by endogenous adult neural stem/precursor cells: defining cellular targets. J Neurol Sci 2008, 265:12-16
53. Windrem MS, Schanz SJ, Guo M, Tian GF, Washco V, Stanwood N, Rasband M, Roy NS, Nedergaard M, Havton LA, Wang S, Goldman SA: Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008, 2:553-565
54. Martino G, Pluchino S: The therapeutic potential of neural stem cells. Nat Rev Neurosci 2006, 7:395-406
55. Pluchino S, Furlan R, Martino G: Cell-based remyelinating therapies in multiple sclerosis: evidence from experimental studies. Curr Opin Neurol 2004, 17:247-255
56. Wilkins A, Compston A: Trophic factors attenuate nitric oxide mediated neuronal and axonal injury in vitro: roles and interactions of mitogen-activated protein kinase signalling pathways. J Neurochem 2005, 92:1487-1496
57. Wilkins A, Majed H, Layfield R, Compston A, Chandran S: Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci 2003, 23:4967-4974
58. Wilkins A, Chandran S, Compston A: A role for oligodendrocytederived IGF-1 in trophic support of cortical neurons. Glia 2001, 36:48-57
59. Anderson TJ, Schneider A, Barrie JA, Klugmann M, McCulloch MC, Kirkham D, Kyriakides E, Nave KA, Griffiths IR: Late-onset neurodegeneration in mice with increased dosage of the proteolipid protein gene A role for oligodendrocyte- derived IGF-1 in trophic support of cortical neurons. J Comp Neurol 1998, 394:506-519
60. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA: Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 1998, 280:1610-1613
61. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA: Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 2003, 33:366-374
62. Webber DJ, Compston A, Chandran S: Minimally manipulated oligodendrocyte precursor cells retain exclusive commitment to the oligodendrocyte lineage following transplantation into intact and injured hippocampus. Eur J Neurosci 2007, 26:1791-1800
63. Hampton DW, Steeves JD, Fawcett JW, Ramer MS: Spinally upregulated noggin suppresses axonal and dendritic plasticity following dorsal rhizotomy. Exp Neurol 2007, 204:366-379
64. MacDermid VE, McPhail LT, Tsang B, Rosenthal A, Davies A, Ramer MS: A soluble Nogo receptor differentially affects plasticity of spinally projecting axons. Eur J Neurosci 2004, 20:2567-2579
65. McQuillen PS, Sheldon RA, Shatz CJ, Ferriero DM: Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. J Neurosci 2003, 23:3308-3315
66. Fan LW, Pang Y, Lin S, Tien LT, Ma T, Rhodes PG, Cai Z: Minocycline reduces lipopolysaccharide-induced neurological dysfunction and brain injury in the neonatal rat. J Neurosci Res 2005, 82:71-82
67. Paintlia MK, Paintlia AS, Contreras MA, Singh I, Singh AK: Lipopolysaccharide-induced peroxisomal dysfunction exacerbates cerebral white matter injury: attenuation by N-acetyl cysteine. Exp Neurol 2008, 210:560-576
68. Paintlia MK, Paintlia AS, Barbosa E, Singh I, Singh AK: N-acetylcysteine prevents endotoxin-induced degeneration of oligodendrocyte progenitors and hypomyelination in developing rat brain. J Neurosci Res 2004, 78:347-361
69. Feldhaus B, Dietzel ID, Heumann R, Berger R: Effects of interferongamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors. J Soc Gynecol Investig 2004, 1:89-96
70. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, Ffrench-Constant C, Franklin RJ: Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 2006, 54:297-303
71. Blakemore WF, Franklin RJ: Remyelination in experimental models of toxin-induced demyelination. Curr Top Microbiol Immunol 2008, 318:193-212