Changes in NG2 cells and oligodendrocytes in a new model of intraspinal hemorrhage

Experimental Neurology

Volumn 255, Issue , 2014, Pages 113-126

  Sahinkaya, F Rezan ^a   Milich, Lindsay M ^a   McTigue, Dana M ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Blood; Gliogenesis; Inflammation; Iron; Myelin; Progenitor; Spinal cord injury

Indexed keywords

COLLAGENASE; FERRITIN; IRON; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; STAT3 PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRDU ASSAY; CELL COUNT; CELL DYNAMICS; CELL LOSS; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; CONTUSION; DYNAMICS; FEMALE; GLIA CELL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INTRASPINAL HEMORRHAGE; LOCOMOTION; MACROPHAGE ACTIVATION; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD HEMORRHAGE; VASCULAR DISEASE;

BLOOD; GLIOGENESIS; INFLAMMATION; IRON; MYELIN; PROGENITOR; SPINAL CORD INJURY;

ANIMALS; ANTIGENS; AXONS; CELL COUNT; CELL DIFFERENTIATION; FEMALE; HEMORRHAGE; NEURAL STEM CELLS; OLIGODENDROGLIA; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD DISEASES; SPINAL CORD INJURIES;

EID: 84897860802     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.02.025     Document Type: Article

References (69)

1. Almad A., McTigue D.M. Chronic expression of PPAR-δ by oligodendrocyte lineage cells in the injured rat spinal cord. J. Comp. Neurol. 2010, 518:785-799.
2. Azari M.F., Profyris C., Karnezis T., Bernard C.C., Small D.H., Cheema S.S., Ozturk E., Hatzinisiriou I., Petratos S. Leukemia inhibitory factor arrests oligodendrocyte death and demyelination in spinal cord injury. J. Neuropathol. Exp. Neurol. 2006, 65:914-929.
3. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
4. Benton R.L., Hagg T. Vascular pathology as a potential therapeutic target in SCI. Transl. Stroke Res. 2011, 2:556-574.
5. Blight A. Mechanical factors in experimental spinal cord injury. J. Am. Paraplegia Soc. 1988, 11:26-34.
6. Blight A.R., Decrescito V. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. NSC 1986, 19:321-341.
7. Bullock R., Mendelow A.D., Teasdale G.M., Graham D.I. Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol. Res. 1984, 6:184-188.
8. Busch S.A., Horn K.P., Cuascut F.X., Hawthorne A.L., Bai L., Miller R.H., Silver J. Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J. Neurosci. 2010, 30:255-265.
9. Butzkueven H., Zhang J.-G., Soilu-Hanninen M., Hochrein H., Chionh F., Shipham K.A., Emery B., Turnley A.M., Petratos S., Ernst M., Bartlett P.F., Kilpatrick T.J. LIF receptor signaling limits immune-mediated demyelination by enhancing oligodendrocyte survival. Nat. Med. 2002, 8:613-619.
10. Choo A.M.-T., Liu J., Liu Z., Dvorak M., Tetzlaff W., Oxland T.R. Modeling spinal cord contusion, dislocation, and distraction: characterization of vertebral clamps, injury severities, and node of Ranvier deformations. J. Neurosci. Methods 2009, 181:6-17.
11. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 1997, 3:73-76.
12. Dell'Albani P., Kahn M.A., Cole R., Condorelli D.F., Giuffrida-Stella A.M., de Vellis J. Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J. Neurosci. Res. 1998, 54:191-205.
13. Frost E.E., Zhou Z., Krasnesky K., Armstrong R.C. Initiation of oligodendrocyte progenitor cell migration by a PDGF-A activated extracellular regulated kinase (ERK) signaling pathway. Neurochem. Res. 2008, 34:169-181.
14. Gensel J.C., Nakamura S., Guan Z., van Rooijen N., Ankeny D.P., Popovich P.G. Macrophages promote axon regeneration with concurrent neurotoxicity. J. Neurosci. 2009, 29:3956-3968.
15. Griffiths I.R., Burns N., Crawford A.R. Early vascular changes in the spinal grey matter following impact injury. Acta Neuropathol. 1978, 41:33-39.
16. Guardiola-Diaz H.M., Ishii A., Bansal R. Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation. Glia 2011, 60:476-486.
17. Han S., Arnold S.A., Sithu S.D., Mahoney E.T., Geralds J.T., Tran P., Benton R.L., Maddie M.A., D'Souza S.E., Whittemore S.R., Hagg T. Rescuing vasculature with intravenous angiopoietin-1 and alpha v beta 3 integrin peptide is protective after spinal cord injury. Brain 2010, 133:1026-1042.
18. Herrera J.J., Sundberg L.M., Zentilin L., Giacca M., Narayana P.A. Sustained expression of vascular endothelial growth factor and angiopoietin-1 improves blood-spinal cord barrier integrity and functional recovery after spinal cord injury. J. Neurotrauma 2010, 27:2067-2076.
19. Hill C. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 2001, 171:153-169.
20. Horky L.L., Galimi F., Gage F.H., Horner P.J. Fate of endogenous stem/progenitor cells following spinal cord injury. J. Comp. Neurol. 2006, 498:525-538.
21. Hu J.G., Fu S.L., Wang Y.X., Li Y., Jiang X.Y., Wang X.F., Qiu M.S., Lu P.H., Xu X.M. Platelet-derived growth factor-AA mediates oligodendrocyte lineage differentiation through activation of extracellular signal-regulated kinase signaling pathway. Neuroscience 2008, 151:138-147.
22. Hughes E.G., Kang S.H., Fukaya M., Bergles D.E. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 2013, 16:668-676. (Available at: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=23624515&retmode=ref&cmd=prlinks).
23. Ishii A., Furusho M., Bansal R. Sustained activation of ERK1/2 MAPK in oligodendrocytes and Schwann cells enhances myelin growth and stimulates oligodendrocyte progenitor expansion. J. Neurosci. 2013, 33:175-186.
24. Juliet P.A.R., Frost E.E., Balasubramaniam J., Del Bigio M.R. Toxic effect of blood components on perinatal rat subventricular zone cells and oligodendrocyte precursor cell proliferation, differentiation and migration in culture. J. Neurochem. 2009, 109:1285-1299.
25. - regulates microglia and macrophage glutamate excitotoxicity in vivo. Exp. Neurol. 2012, 233:333-341.
26. Kurland D., Hong C., Aarabi B., Gerzanich V., Simard J.M. Hemorrhagic progression of a contusion after traumatic brain injury: a review. J. Neurotrauma 2012, 29:19-31.
27. MacLellan C.L., Silasi G., Poon C.C., Edmundson C.L., Buist R., Peeling J., Colbourne F. Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J. Cereb. Blood Flow Metab. 2008, 28:516-525.
28. MacLellan C.L., Silasi G., Auriat A.M., Colbourne F. Rodent models of intracerebral hemorrhage. Stroke 2010, 41:S95-S98.
29. Maikos J.T., Shreiber D.I. Immediate damage to the blood-spinal cord barrier due to mechanical trauma. J. Neurotrauma 2007, 24:492-507.
30. Mautes A.E., Weinzierl M.R., Donovan F., Noble L.J. Vascular events after spinal cord injury: contribution to secondary pathogenesis. Phys. Ther. 2000, 80:673-687.
31. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 2001, 21:3392-3400.
32. McTigue D.M., Tripathi R., Wei P. NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions. J. Neuropathol. Exp. Neurol. 2006, 65:406-420.
33. Noble L.J., Wrathall J.R. Correlative analyses of lesion development and functional status after graded spinal cord contusive injuries in the rat. Exp. Neurol. 1989, 103:34-40.
34. Noble L.J., Wrathall J.R. Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 1989, 482:57-66.
35. Pineau I., Lacroix S. Proinflammatory cytokine synthesis in the injured mouse spinal cord: multiphasic expression pattern and identification of the cell types involved. J. Comp. Neurol. 2007, 500:267-285.
36. Pleasant J.M., Carlson S.W., Mao H., Scheff S.W., Yang K.H., Saatman K.E. Rate of neurodegeneration in the mouse controlled cortical impact model is influenced by impactor tip shape: implications for mechanistic and therapeutic studies. J. Neurotrauma 2011, 28:2245-2262.
37. Popovich P.G., Hickey W.F. Bone marrow chimeric rats reveal the unique distribution of resident and recruited macrophages in the contused rat spinal cord. J. Neuropathol. Exp. Neurol. 2001, 60:676-685.
38. Popovich P.G., Horner P.J., Mullin B.B., Stokes B.T. A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp. Neurol. 1996, 142:258-275.
39. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
40. Popovich P.G., Guan Z., McGaughy V., Fisher L., Hickey W.F., Basso D.M. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J. Neuropathol. Exp. Neurol. 2002, 61:623-633.
41. Popovich P.G., Lemeshow S., Gensel J.C., Tovar C.A. Independent evaluation of the effects of glibenclamide on reducing progressive hemorrhagic necrosis after cervical spinal cord injury. Exp. Neurol. 2011, 1-8.
42. Powers B.E., Sellers D.L., Lovelett E.A., Cheung W., Aalami S.P., Zapertov N., Maris D.O., Horner P.J. Remyelination reporter reveals prolonged refinement of spontaneously regenerated myelin. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4075-4080.
43. Prunell G.F., Svendgaard N.-A., Alkass K., Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J. Neurosurg. 2005, 102:1046-1054.
44. Psachoulia K., Jamen F., Young K.M., Richardson W.D. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. NGB 2010, 5:57.
45. Rabchevsky A.G., Sullivan P.G., Scheff S.W. Temporal-spatial dynamics in oligodendrocyte and glial progenitor cell numbers throughout ventrolateral white matter following contusion spinal cord injury. Glia 2007, 55:831-843.
46. Rathore K.I., Kerr B.J., Redensek A., Lopez-Vales R., Jeong S.Y., Ponka P., David S. Ceruloplasmin protects injured spinal cord from iron-mediated oxidative damage. J. Neurosci. 2008, 28:12736-12747. (Available at: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=19036966&retmode=ref&cmd=prlinks).
47. Rhodes K.E., Raivich G., Fawcett J.W. The injury response of oligodendrocyte precursor cells is induced by platelets, macrophages and inflammation-associated cytokines. Neuroscience 2006, 140:87-100.
48. Rosenberg G.A., Mun-Bryce S., Wesley M., Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke 1990, 21:801-807.
49. Sauerbeck A., Schonberg D.L., Laws J.L., McTigue D.M. Systemic iron chelation results in limited functional and histological recovery after traumatic spinal cord injury in rats. Exp. Neurol. 2013, 248:1-9.
50. Schonberg D.L., McTigue D.M. Iron is essential for oligodendrocyte genesis following intraspinal macrophage activation. Exp. Neurol. 2009, 218:64-74.
51. Schonberg D.L., Popovich P.G., McTigue D.M. Oligodendrocyte generation is differentially influenced by toll-like receptor (TLR) 2 and TLR4-mediated intraspinal macrophage activation. J. Neuropathol. Exp. Neurol. 2007, 66:1124-1135.
52. Schonberg D.L., Goldstein E.Z., Sahinkaya F.R., Wei P., Popovich P.G., McTigue D.M. Ferritin stimulates oligodendrocyte genesis in the adult spinal cord and can be transferred from macrophages to NG2 cells in vivo. J. Neurosci. 2012, 32:5374-5384.
53. Sellers D.L., Maris D.O., Horner P.J. Postinjury niches induce temporal shifts in progenitor fates to direct lesion repair after spinal cord injury. J. Neurosci. 2009, 29:6722-6733.
54. Simard J.M., Gerzanich V. When replication teaches more than the original experiment - the saga of the unknown unknown. Exp. Neurol. 2011, 1-2.
55. Simard J.M., Tsymbalyuk O., Ivanov A., Ivanova S., Bhatta S., Geng Z., Woo S.K., Gerzanich V. Endothelial sulfonylurea receptor 1-regulated NCCa-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury. J. Clin. Invest. 2007, 117:2105-2113.
56. Simard J.M., Woo S.K., Norenberg M.D., Tosun C., Chen Z., Ivanova S., Tsymbalyuk O., Bryan J., Landsman D., Gerzanich V. Brief suppression of Abcc8 prevents autodestruction of spinal cord after trauma. Sci. Transl. Med. 2010, 2. (28ra29-28ra29).
57. Simard J.M., Popovich P.G., Tsymbalyuk O., Gerzanich V. Spinal cord injury with unilateral versus bilateral primary hemorrhage - effects of glibenclamide. Exp. Neurol. 2012, 1-7.
58. Simard J.M., Popovich P.G., Tsymbalyuk O., Caridi J., Gullapalli R.P., Kilbourne M.J., Gerzanich V. MRI evidence that glibenclamide reduces acute lesion expansion in a rat model of spinal cord injury 2013, 51:823-827.
59. Sun F., Lin C.-L.G., McTigue D., Shan X., Tovar C.A., Bresnahan J.C., Beattie M.S. Effects of axon degeneration on oligodendrocyte lineage cells: dorsal rhizotomy evokes a repair response while axon degeneration rostral to spinal contusion induces both repair and apoptosis. Glia 2010, 58:1304-1319.
60. Tator C.H., Koyanagi I. Vascular mechanisms in the pathophysiology of human spinal cord injury. J. Neurosurg. 1997, 86:483-492.
61. Todorich B., Pasquini J.M., Garcia C.I., Paez P.M., Connor J.R. Oligodendrocytes and myelination: the role of iron. Glia 2009, 57:467-478.
62. Tripathi R., McTigue D.M. Prominent oligodendrocyte genesis along the border of spinal contusion lesions. Glia 2007, 55:698-711.
63. Tripathi R.B., McTigue D.M. Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats. J. Comp. Neurol. 2008, 510:129-144.
64. Warden P., Bamber N.I., Li H., Esposito A., Ahmad K.A., Hsu C.Y., Xu X.M. Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp. Neurol. 2001, 168:213-224.
65. Watanabe M., Toyama Y., Nishiyama A. Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J. Neurosci. Res. 2002, 69:826-836.
66. Yu C.-G., Yezierski R.P., Joshi A., Raza K., Li Y., Geddes J.W. Involvement of ERK2 in traumatic spinal cord injury. J. Neurochem. 2010, 113:131-142.
67. Zai L.J., Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005, 50:247-257.
68. Zhang X., Surguladze N., Slagle-Webb B., Cozzi A., Connor J.R. Cellular iron status influences the functional relationship between microglia and oligodendrocytes. Glia 2006, 54:795-804.
69. Zhu X., Hill R.A., Nishiyama A. NG2 cells generate oligodendrocytes and gray matter astrocytes in the spinal cord. NGB 2008, 4:19.