Bone marrow stromal cells protect oligodendrocytes from oxygen-glucose deprivation injury

Journal of Neuroscience Research

Volumn 86, Issue 7, 2008, Pages 1501-1510

  Zhang, Jing ^a   Li, Yi ^a   Zheng, Xuguang ^a   Gao, Qi ^a   Liu, Zhongwu ^a   Qu, Runjiang ^a   Borneman, Jade ^b   Elias, Stanton B ^a   Chopp, Michael ^a,c  

^a HENRY FORD HOSPITAL   (United States)

^b Cognate BioServices Inc ^*  (United States)

^c OAKLAND UNIVERSITY   (United States)

Author keywords

Bone marrow stromal cells; Oligodendrocytes; Oxygen glucose deprivation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; GLUCOSE; MESSENGER RNA; OXYGEN; PROTEIN P75; PROTEIN SERINE THREONINE KINASE;

ANAEROBIC METABOLISM; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL HYPOXIA; CELL LINE; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; MOUSE; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REOXYGENATION; STROMA CELL; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; ANIMALS; ANOXIA; APOPTOSIS; BONE MARROW CELLS; CELL SURVIVAL; CELLS, CULTURED; CHROMONES; COCULTURE TECHNIQUES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLUCOSE; IN SITU NICK-END LABELING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; MORPHOLINES; OLIGODENDROGLIA; RECEPTORS, GROWTH FACTOR; STROMAL CELLS;

EID: 43149126106     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21617     Document Type: Article

References (79)

1. Anitha M, Gondha C, Sutliff R, Parsadanian A, Mwangi S, Sitaraman SV, Srinivasan S. 2006. GDNF rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the PI3K/Akt pathway. J Clin Invest 116:344-356.
2. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM, Bresnahan JC, Hempstead BL, Yoon SO. 2002. Pro-NGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 36:375-386.
3. Beckman JS, Koppenol WH. 1996. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am J Physiol 271:0424-C1437.
4. Bhave SV, Ghoda L, Hoffman PL. 1999. Brain-derived neurotrophic factor mediates the anti-apoptotic effect of NMDA in cerebellar granule neurons: signal transduction cascades and site of ethanol action. J Neurosci 19:3277-3286.
5. Braydich-Stolle L, Kostereva N, Dym M, Hofmann MC. 2007. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 304:34-45.
6. Brazil DP, Park J, Hemmings BA. 2002. PKB binding proteins. Getting in on the Akt. Cell 111:293-303.
7. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
8. Cantley LC. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
9. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV. 1996. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719.
10. Casha S, Yu WR, Fehlings MG. 2001. Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 103:203-218.
11. Chen J, Li Y, Wang L, Zhang Z, Lu D, Lu M, Chopp M. 2001. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 32:1005-1011.
12. Chen J, Li Y, Katakowski M, Chen X, Wang L, Lu D, Lu M, Gautam SC, Chopp M. 2003. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73:778-786.
13. Chen X, Katakowski M, Li Y, Lu D, Wang L, Zhang L, Chen J, Xu Y, Gautam S, Mahmood A, Chopp M. 2002a. Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: growth factor production. J Neurosci Res 69:687-691.
14. Chen X, Li Y, Wang L, Katakowski M, Zhang L, Chen J, Xu Y, Gautam SC, Chopp M. 2002b. Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22:275-279.
15. Chopp M, Li Y. 2002. Treatment of neural injury with marrow stromal cells. Lancet Neurol 1:92-100.
16. Coffer PJ, Jin J, Woodgett JR. 1998. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 335:1-13.
17. Coulson EJ, Reid K, Murray SS, Cheema SS, Bartlett PF. 2000. Role of neurotrophin receptor p75NTR in mediating neuronal cell death following injury. Clin Exp Pharmacol Physiol 27:537-541.
18. Dirnagl U, Iadecola C, Moskowitz MA. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
19. Dive C, Gregory CD, Phipps DJ, Evans DL, Milner AE, Wyllie AH. 1992. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim Biophys Acta 1133:275-285.
20. Dolcet X, Egea J, Soler RM, Martin-Zanca D, Comella JX. 1999. Activation of phosphatidylinositol 3-kinase, but not extracellular-regulated kinases, is necessary to mediate brain-derived neurotrophic factor-induced motoneuron survival. J Neurochem 73:521-531.
21. Focke PJ, Swetlik AR, Schilz JL, Epstein ML. 2003. GDNF and insulin cooperate to enhance the proliferation and differentiation of enteric crest-derived cells. J Neurobiol 55:151-164.
22. Foulstone EJ, Tavare JM, Gunn-Moore FJ. 1999. Sustained phosphorylation and activation of protein kinase B correlates with brain-derived neurotrophic factor and insulin stimulated survival of cerebellar granule cells. Neurosci Lett 264:125-128.
23. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. 2000. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101:660-667.
24. Gao Q, Li Y, Chopp M. 2005. Bone marrow stromal cells increase astrocyte survival via up-regulation of phosphoinositide 3-kinase/threonine protein kinase and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathways and stimulate astrocyte trophic factor gene expression after anaerobic insult. Neuroscience 136:123-134.
25. Gresle MM, Jarrott B, Jones NM, Callaway JK. 2006. Injury to axons and oligodendrocytes following endothelin-1-induced middle cerebral artery occlusion in conscious rats. Brain Res 1110:13-22.
26. Hajduch E, Litherland GJ, Hundal HS. 2001. Protein kinase B (PKB/ Akt) - a key regulator of glucose transport? FEBS Lett 492:199-203.
27. Hauck SM, Kinkl N, Deeg CA, Swiatek-de Lange M, Schoffmann S, Ueffing M. 2006. GDNF family ligands trigger indirect neuroprotective signaling in retinal glial cells. Mol Cell Biol 26:2746-2757.
28. Imai H, Masayasu H, Dewar D, Graham DI, Macrae IM. 2001. Ebselen protects both gray and white matter in a rodent model of focal cerebral ischemia. Stroke 32:2149-2154.
29. Itakura M, Yamamori S, Kuwahara R, Sekiguchi M, Takahashi M. 2005. Two distinct regulatory mechanisms of neurotransmitter release by phosphatidylinositol 3-kinase. J Neurochem 94:502-509.
30. Kulik G, Klippel A, Weber MJ. 1997. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 17:1595-1606.
31. Lee J, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Kimura T, Nakano T, Ogura A, Shinohara T. 2007. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 134:1853-1859.
32. Lee R, Kermani P, Teng KK, Hempstead BL. 2001. Regulation of cell survival by secreted proneurotrophins. Science 294:1945-1948.
33. Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX, Zhang Z. 2000. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 20:1311-1319.
34. Li Y, Chen J, Wang L, Zhang L, Lu M, Chopp M. 2001. Intracerebral transplantation of bone marrow stromal cells in a 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. Neurosci Lett 316:67-70.
35. Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M. 2002. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59:514-523.
36. Li Y, Chen J, Zhang CL, Wang L, Lu D, Katakowski M, Gao Q, Shen LH, Zhang J, Lu M, Chopp M. 2005. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49:407-417.
37. Li Y, McIntosh K, Chen J, Zhang C, Gao Q, Borneman J, Raginski K, Mitchell J, Shen L, Zhang J, Lu D, Chopp M. 2006. Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp Neurol 198:313-325.
38. Lin DC, Quevedo C, Brewer NE, Bell A, Testa JR, Grimes ML, Miller FD, Kaplan DR. 2006. APPL1 associates with TrkA and GIPC1 and is required for nerve growth factor-mediated signal transduction. Mol Cell Biol 26:8928-8941.
39. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 - Delta Delta C(T) method. Methods 25:402-408.
40. Lyons SA, Kettenmann H. 1998. Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J Cereb Blood Flow Metab 18:521-530.
41. Mahmood A, Lu D, Wang L, Li Y, Lu M, Chopp M. 2001. Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells. Neurosurgery 49:1196-1203; discussion1203-1194.
42. Mahmood A, Lu D, Chopp M. 2004. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21:33-39.
43. Matute C, Alberdi E, Domercq M, Sanchez-Gomez MV, Perez-Samartin A, Rodriguez-Antiguedad A, Perez-Cerda F. 2007. Excitotoxic damage to white matter. J Anat 210:693-702.
44. McCarran WJ, Goldberg MP. 2007. White matter axon vulnerability to AMPA/kainate receptor-mediated ischemic injury is developmentally regulated. J Neurosci 27:4220-4229.
45. Mielke JG, Taghibiglou C, Wang YT. 2006. Endogenous insulin signaling protects cultured neurons from oxygen-glucose deprivation-induced cell death. Neuroscience 143:165-173.
46. Mockridge JW, Benton EC, Andreeva LV, Latchman DS, Marber MS, Heads RJ. 2000. IGF-1 regulates cardiac fibroblast apoptosis induced by osmotic stress. Biochem Biophys Res Commun 273:322-327.
47. Mograbi B, Bocciardi R, Bourget I, Busca R, Rochet N, Farahi-Far D, Juhel T, Rossi B. 2001. Glial cell line-derived neurotrophic factor-stimulated phosphatidylinositol 3-kinase and Akt activities exert opposing effects on the ERK pathway: importance for the rescue of neuroectodermic cells. J Biol Chem 276:45307-45319.
48. Nicholson DW, Thomberry NA. 1997. Caspases: killer proteases. Trends Biochem Sci 22:299-306.
49. Paez PM, Garcia CI, Davio C, Campagnoni AT, Soto EF, Pasquini JM. 2004. Apotransferrin promotes the differentiation of two oligodendroglial cell lines. Glia 46:207-217.
50. Pantoni L, Garcia JH, Gutierrez JA. 1996. Cerebral white matter is highly vulnerable to ischemia. Stroke 27:1641-1646; discussion 1647.
51. Politi LE, Rotstein NP, Salvador G, Giusto NM, Insua MF. 2001. Insulin-like growth factor-I is a potential trophic factor for amacrine cells. J Neurochem 76:1199-1211.
52. Rahbek UL, Dissing S, Thomassen C, Hansen AJ, Tritsaris K. 2005. Nerve growth factor activates aorta endothelial cells causing PI3K/Akt-and ERK-dependent migration. Pflugers Arch 450:355-361.
53. Rajagopal R, Chen ZY, Lee FS, Chao MV. 2004. Transactivation of Trk neurotrophin receptors by G-protein-coupled receptor ligands occurs on intracellular membranes. J Neurosci 24:6650-6658.
54. Shah A, Swain WA, Richardson D, Edwards J, Stewart DJ, Richardson CM, Swinson DE, Patel D, Jones JL, O'Byrne KJ. 2005. Phospho-akt expression is associated with a favorable outcome in non-small cell lung cancer. Clin Cancer Res 11:2930-2936.
55. Shibata M, Hisahara S, Hara H, Yamawaki T, Fukuuchi Y, Yuan J, Okano H, Miura M. 2000. Caspases determine the vulnerability of oligodendrocytes in the ischemic brain. J Clin Invest 106:643-653.
56. Shiojima I, Walsh K. 2002. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90:1243-1250.
57. Syroid DE, Maycox PJ, Soilu-Hanninen M, Petratos S, Bucci T, Burrola P, Murray S, Cheema S, Lee KF, Lemke G, Kilpatrick TJ. 2000. Induction of postnatal Schwann cell death by the low-affinity neurotrophin receptor in vitro and after axotomy. J Neurosci 20:5741-5747.
58. Thompson RJ, Zhou N, MacVicar BA. 2006. Ischemia opens neuronal gap junction hemichannels. Science 312:924-927.
59. Tsui CC, Shankland SJ, Pierchala BA. 2006. Glial cell line-derived neurotrophic factor and its receptor ret is a novel ligand-receptor complex critical for survival response during podocyte injury. J Am Soc Nephrol 17:1543-1552.
60. Ulrich E, Duwel A, Kauffmann-Zeh A, Gilbert C, Lyon D, Rudkin B, Evan G, Martin-Zanca D. 1998. Specific TrkA survival signals interfere with different apoptotic pathways. Oncogene 16:825-832.
61. Vaillant AR, Mazzoni I, Tudan C, Boudreau M, Kaplan DR, Miller FD. 1999. Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal sur-vival. J Cell Biol 146:955-966.
62. Veit C, Genze F, Menke A, Hoeffert S, Gress TM, Gierschik P, Giehl K. 2004. Activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase is required for glial cell line-derived neurotrophic factor-induced migration and invasion of pancreatic carcinoma cells. Cancer Res 64:5291-5300.
63. 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.
64. Villegas SN, Njaine B, Linden R, Carri NG. 2006. Glial-derived neurotrophic factor (GDNF) prevents ethanol (EtOH) induced B92 glial cell death by both PI3K/AKT and MEK/ERK signaling pathways. Brain Res Bull 71:116-126.
65. Vivanco I, Sawyers CL. 2002. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2:489-501.
66. Vlahos CJ, Matter WF, Hui KY, Brown RF. 1994. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269:5241-5248.
67. Wang HJ, Cao JP, Yu JK, Gao DS. 2007. Role of PI3-K/Akt pathway and its effect on glial cell line-derived neurotrophic factor in midbrain dopamine cells. Acta Pharmacol Sin 28:166-172.
68. 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.
69. Wang L, Gang Zhang Z, Lan Zhang R, Chopp M. 2005. Activation of the PI3-K/Akt pathway mediates cGMP enhanced-neurogenesis in the adult progenitor cells derived from the subventricular zone. J Cereb Blood Flow Metab 25:1150-1158.
70. NTR apoptotic signaling pathway using a novel cellular model. J Biol Chem 276:33812-33820.
71. Wilkins A, Majed H, Layfield R, Compston A, Chandran S. 2003. 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 23:4967-4974.
72. Xie Y, Tisi MA, Yeo TT, Longo FM. 2000. Nerve growth factor (NGF) loop 4 dimeric mimetics activate ERK and AKT and promote NGF-like neurotrophic effects. J Biol Chem 275:29868-29874.
73. Yamaguchi A, Tamatani M, Matsuzaki H, Namikawa K, Kiyama H, Vitek MP, Mitsuda N, Tohyama M. 2001. Akt activation protects hippocampal neurons from apoptosis by inhibiting transcriptional activity of p53. J Biol Chem 276:5256-5264.
74. Yoon SO, Casaccia-Bonnefil P, Carter B, Chao MV. 1998. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J Neurosci 18:3273-3281.
75. Yoshioka A, Yamaya Y, Saiki S, Kanemoto M, Hirose G, Beesley J, Pleasure D. 2000. Non-N-methyl-D-aspartate glutamate receptors mediate oxygen-glucose deprivation-induced oligodendroglial injury. Brain Res 854:207-215.
76. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A. 2005. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106:1755-1761.
77. Zhang J, Li Y, Chen J, Yang M, Katakowski M, Lu M, Chopp M. 2004. Expression of insulin-like growth factor 1 and receptor in ischemic rats treated with human marrow stromal cells. Brain Res 1030:19-27.
78. Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M. 2005. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 195:16-26.
79. Zhang J, Li Y, Lu M, Cui Y, Chen J, Noffsinger L, Elias SB, Chopp M. 2006. Bone marrow stromal cells reduce axonal loss in experimental autoimmune encephalomyelitis mice. J Neurosci Res 84:587-595.