Erythropoietin amplifies stroke-induced oligodendrogenesis in the rat

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Zhang, Li ^a   Chopp, Michael ^a,b   Zhang, Rui Lan ^a   Wang, Lei ^a   Zhang, Jing ^a   Wang, Ying ^a   Toh, Yier ^a   Santra, Manoranjan ^a   Lu, Mei ^a   Zhang, Zheng Gang ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE PHOSPHODIESTERASE; RECOMBINANT ERYTHROPOIETIN; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; IN VITRO STUDY; MALE; MOUSE; MYELINATED NERVE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; RAT; SUBVENTRICULAR ZONE; WHITE MATTER; ANIMAL; CELL DIVISION; DRUG EFFECT; NERVE FIBER; PATHOLOGY; STROKE;

LENTIVIRUS; RATTUS;

ANIMALS; AXONS; CELL DIVISION; ERYTHROPOIETIN, RECOMBINANT; OLIGODENDROGLIA; RATS; STROKE;

EID: 77956200745     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011016     Document Type: Article

References (53)

1. Dewar D, Underhill SM, Goldberg MP (2003) Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 23: 263-274.
2. Pantoni L, Garcia JH, Gutierrez JA (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27: 1641-1646; discussion 1647.
3. Petito CK, Olarte JP, Roberts B, Nowak TS Jr, Pulsinelli WA (1998) Selective glial vulnerability following transient global ischemia in rat brain. J Neuropathol Exp Neurol 57: 231-238.
4. Gregersen R, Christensen T, Lehrmann E, Diemer NH, Finsen B (2001) Focal cerebral ischemia induces increased myelin basic protein and growth-associated protein-43 gene transcription in peri-infarct areas in the rat brain. Exp Brain Res 138: 384-392.
5. Tanaka K, Nogawa S, Suzuki S, Dembo T, Kosakai A (2003) Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in peri-infarct area in the rat brain. Brain Res 989: 172-179.
6. Gensert JM, Goldman JE (1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19: 197-203.
7. Roy NS, Wang S, Harrison-Restelli C, Benraiss A, Fraser RA, et al. (1999) Identification, isolation, and promoter-defined separation of mitotic oligodendrocyte progenitor cells from the adult human subcortical white matter. J Neurosci 19: 9986-9995.
8. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, et al. (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26: 7907-7918.
9. Keirstead HS, Blakemore WF (1997) Identification of post-mitotic oligodendrocytes incapable of remyelination within the demyelinated adult spinal cord. J Neuropathol Exp Neurol 56: 1191-1201.
10. Carroll WM, Jennings AR, Ironside LJ (1998) Identification of the adult resting progenitor cell by autoradiographic tracking of oligodendrocyte precursors in experimental CNS demyelination. Brain 121 (Pt2): 293-302.
11. Norton WT (1996) Do oligodendrocytes divide? Neurochem Res 21: 495-503.
12. Taniguchi Y, Amazaki M, Furuyama T, Yamaguchi W, Takahara M, et al. (2009) Sema4D deficiency results in an increase in the number of oligodendrocytes in healthy and injured mouse brains. J Neurosci Res.
13. Sugawa M, Sakurai Y, Ishikawa-Ieda Y, Suzuki H, Asou H (2002) Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci Res 44: 391-403.
14. Zhang J, Li Y, Cui Y, Chen J, Lu M, et al. (2005) Erythropoietin treatment improves neurological functional recovery in EAE mice. Brain Res 1034: 34-39.
15. Vitellaro-Zuccarello L, Mazzetti S, Madaschi L, Bosisio P, Gorio A, et al. (2007) Erythropoietin-mediated preservation of the white matter in rat spinal cord injury. Neuroscience 144: 865-877.
16. Sargin D, Hassouna I, Sperling S, Siren AL, Ehrenreich H (2009) Uncoupling of neurodegeneration and gliosis in a murine model of juvenile cortical lesion. Glia 57: 693-702.
17. Iwai M, Stetler RA, Xing J, Hu X, Gao Y, et al. (2010) Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 41: 1032-1037.
18. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M (2004) Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 35: 1732-1737.
19. Iwai M, Cao G, Yin W, Stetler RA, Liu J, et al. (2007) Erythropoietin promotes neuronal replacement through revascularization and neurogenesis after neonatal hypoxia/ischemia in rats. Stroke 38: 2795-2803.
20. Ness JK, Valentino M, McIver SR, Goldberg MP (2005) Identification of oligodendrocytes in experimental disease models. Glia 50: 321-328.
21. Mathews MB, Bernstein RM, Franza BR Jr, Garrels JI (1984) Identity of the proliferating cell nuclear antigen and cyclin. Nature 309: 374-376.
22. Zhang RL, Zhang ZG, Lu M, Wang Y, Yang JJ, et al. (2006) Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke. J Cereb Blood Flow Metab 26: 857-863.
23. Yam PS, Dewar D, McCulloch J (1998) Axonal injury caused by focal cerebral ischemia in the rat. J Neurotrauma 15: 441-450.
24. Paterson JA, Privat A, Ling EA, Leblond CP (1973) 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.
25. Reynolds R, Wilkin GP (1988) Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 102: 409-425.
26. Imamoto K, Leblond CP (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells. J Comp Neurol 180: 139-163.
27. LeVine SM, Goldman JE (1988) Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. J Comp Neurol 277: 441-455.
28. Levison SW, Goldman JE (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10: 201-212.
29. Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, et al. (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20: 2218-2228.
30. Scolding N, Franklin R, Stevens S, Heldin CH, Compston A, et al. (1998) Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 121 (Pt12): 2221-2228.
31. Polito A, Reynolds R (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207: 707-716.
32. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009) Epidermal Growth Factor Induces the Progeny of Subventricular Zone Type B Cells to Migrate and Differentiate into Oligodendrocytes. Stem Cells 27: 2032-2043.
33. van der Kooij MA, Groenendaal F, Kavelaars A, Heijnen CJ, van Bel F (2009) Combination of deferoxamine and erythropoietin: therapy for hypoxia-ischemia-induced brain injury in the neonatal rat? Neurosci Lett 451: 109-113.
34. Mizuno K, Hida H, Masuda T, Nishino H, Togari H (2008) Pretreatment with low doses of erythropoietin ameliorates brain damage in periventricular leukomalacia by targeting late oligodendrocyte progenitors: a rat model. Neonatology 94: 255-266.
35. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, et al. (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33: 366-374.
36. Jiang Q, Zhang ZG, Ding GL, Silver B, Zhang L, et al. (2006) MRI detects white matter reorganization after neural progenitor cell treatment of stroke. Neuroimage 32: 1080-1089.
37. Li L, Jiang Q, Ding G, Zhang L, Zhang ZG, et al. (2009) MRI identification of white matter reorganization enhanced by erythropoietin treatment in a rat model of focal ischemia. Stroke 40: 936-941.
38. Mandai K, Matsumoto M, Kitagawa K, Matsushita K, Ohtsuki T, et al. (1997) Ischemic damage and subsequent proliferation of oligodendrocytes in focal cerebral ischemia. Neuroscience 77: 849-861.
39. Gotts JE, Chesselet MF (2005) Migration and fate of newly born cells after focal cortical ischemia in adult rats. J Neurosci Res 80: 160-171.
40. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB (2006) Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex. Exp Neurol 199: 113-121.
41. Zhao JW, Raha-Chowdhury R, Fawcett JW, Watts C (2009) Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur J Neurosci 29: 1853-1869.
42. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22.
43. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, et al. (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161: 169-186.
44. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR (1997) A rat model of focal embolic cerebral ischemia. Brain Res 766: 83-92.
45. Santra M, Zhang X, Santra S, Jiang F, Chopp M (2006) Ectopic doublecortin gene expression suppresses the malignant phenotype in glioblastoma cells. Cancer Res 66: 11726-11735.
46. Wiznerowicz M, Trono D (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 77: 8957-8961.
47. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates: New York: Academic.
48. Chen J, Li Y, Wang L, Zhang Z, Lu D, et al. (2001) Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32: 1005-1011.
49. Hernandez TD, Schallert T (1988) Seizures and recovery from experimental brain damage. Exp Neurol 102: 318-324.
50. Lee J, Gravel M, Zhang R, Thibault P, Braun PE (2005) Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J Cell Biol 170: 661-673.
51. Pfeiffer SE, Warrington AE, Bansal R (1993) The oligodendrocyte and its many cellular processes. Trends Cell Biol 3: 191-197.
52. Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, et al. (2006) Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 26: 5996-6003.
53. Verity AN, Bredesen D, Vonderscher C, Handley VW, Campagnoni AT (1993) Expression of myelin protein genes and other myelin components in an oligodendrocytic cell line conditionally immortalized with a temperature-sensitive retrovirus. J Neurochem 60: 577-587