Targeting nitric oxide in the subacute restorative treatment of ischemic stroke

Expert Opinion on Investigational Drugs

Volumn 22, Issue 7, 2013, Pages 843-851

  Zhang, Rui Lan ^a   Zhang, Zheng Gang ^a   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

Angiogenesis; CGMP; Neurogenesis; Nitric Oxide; PDE5 inhibitor; Stroke

Indexed keywords

ANGIOPOIETIN 2; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; SILDENAFIL; TADALAFIL; VARDENAFIL; VASCULOTROPIN;

ANGIOGENESIS; ASTROCYTE; ASTROCYTOSIS; BLOOD VESSEL PERMEABILITY; BRAIN ISCHEMIA; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; COMPETITIVE INHIBITION; CONVALESCENCE; DENTATE GYRUS; DISEASE EXACERBATION; DISEASE SEVERITY; ENDOTHELIUM CELL; HEART VENTRICLE HYPERTROPHY; HUMAN; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; OLIGODENDROGLIA; PHENOTYPE; PROTEIN ASSEMBLY; PROTEIN BLOOD LEVEL; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; STROKE PATIENT; SUBVENTRICULAR ZONE; UPREGULATION;

ANIMALS; BRAIN ISCHEMIA; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; DRUG EVALUATION, PRECLINICAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGENESIS; NEURONS; NITRIC OXIDE; NITRIC OXIDE DONORS; PHOSPHODIESTERASE 5 INHIBITORS; STROKE;

EID: 84879125007     PISSN: 13543784     EISSN: 17447658     Source Type: Journal    
DOI: 10.1517/13543784.2013.793672     Document Type: Review

References (101)

1. Zivin JA. Acute stroke therapy with tissue plasminogen activator (tPA) since it was approved by the U.S. Food and Drug Administration (FDA). Ann Neurol 2009;66(1):6-10
2. del Zoppo GJ. Inflammation and the neurovascular unit in the setting of focal cerebral ischemia. Neuroscience 2009;158(3):972-82
3. Armstead WM, Ganguly K, Kiessling JW, et al. Signaling, delivery and age as emerging issues in the benefit/risk ratio outcome of tPA For treatment of CNS ischemic disorders. J Neurochem 2010;113(2):303-12
4. Fisher M, Bastan B. Treating acute ischemic stroke. Curr Opin Drug Discov Devel 2008;11(5):626-32
5. Chavez JC, Hurko O, Barone FC, Feuerstein GZ, et al. Pharmacologic interventions for stroke: looking beyond the thrombolysis time window into the penumbra with biomarkers, not a stopwatch. Stroke 2009;40(10):e558-63
6. Ginsberg MD. Current status of neuroprotection for cerebral ischemia: synoptic overview. Stroke 2009;40(3 Suppl):S111-14
7. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003;4(5):399-415
8. Zhang R, Wang L, Zhang L, et al. Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ Res 2003;92(3):308-13
9. Zhang R, Wang Y, Zhang L, et al. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 2002;33(11):2675-80
10. Chen J, Zhang ZG, Li Y, et al. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 2003;53(6):743-51
11. Lu D, Goussev A, Chen J, et al. Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J Neurotrauma 2004;21(1):21-32
12. Shyu WC, Lin SZ, Yang HI, et al. Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 2004;110(13):1847-54
13. Wang L, Zhang Z, Wang Y, et al. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004;35(7):1732-7
14. Jin K, Sun Y, Xie L, et al. Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 2004;24(4):399-408
15. Taguchi A, Soma T, Tanaka H, et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 2004;114(3):330-8
16. Willing AE, Vendrame M, Mallery J, et al. Mobilized peripheral blood cells administered intravenously produce functional recovery in stroke. Cell Transplant 2003;12(4):449-54
17. Garthwaite J, Southam E, Boulton CL, et al. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo [4,3-a]quinoxalin-1-one. Mol Pharmacol 1995;48:2:184-8
18. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999;22(9):391-7
19. Corbin JD, Francis SH. Cyclic GMP phosphodiesterase-5: target of sildenafil. J Biol Chem 1999;274(20):13729-32
20. Bednar MM. The role of sildenafil in the treatment of stroke. Curr Opin Investig Drugs 2008;9(7):754-9
21. Terpolilli NA, Moskowitz MA, Plesnila N. Nitric oxide: considerations for the treatment of ischemic stroke. J Cereb Blood Flow Metab 2012;32(7):1332-46
22. Eliasson MJ, Huang Z, Ferrante RJ, et al. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 1999;19(14):5910-18
23. Olmez I, Ozyurt H. Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 2012;60(2):208-12
24. Shi ZQ, Sunico CR, McKercher SR, et al. S-nitrosylated SHP-2 contributes to NMDA receptor-mediated excitotoxicity in acute ischemic stroke. Proc Natl Acad Sci USA 2013;110(8):3137-42
25. Stamler JS. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 1994;78(6):931-6
26. ENOS Trial Investigators. Glyceryl trinitrate vs. control, and continuing vs. stopping temporarily prior antihypertensive therapy, in acute stroke: rationale and design of the Efficacy of Nitric Oxide in Stroke (ENOS) trial (ISRCTN99414122). Int J Stroke 2006;1(4):245-9
27. Amaro S, Chamorro A. Translational stroke research of the combination of thrombolysis and antioxidant therapy. Stroke 2011;42(5):1495-9
28. Zhang ZG, Zhang L, Jiang Q, et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 2000;106(7):829-38
29. Krupinski J, Kaluza J, Kumar P, et al. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 1994;25(9):1794-8
30. Garcia J, Cox J, Hudgins W. Ultrastructure of the microvasculature in experimental cerebral infarction. Acta Neuropathol 1971;18(4):273-85
31. Zhang ZG, Zhang L, Tsang W, et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002;22(4):379-92
32. Thored P, Wood J, Arvidsson A, et al. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 2007;38(11):3032-9
33. Zhang L, Zhang Z, Zhang RL, et al. Tadalafil, a long-acting type 5 phosphodiesterase isoenzyme inhibitor, improves neurological functional recovery in a rat model of embolic stroke. Brain Res 2006;1118(1):192-8
34. DiNapoli VA, Huber JD, Houser K, et al. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol Aging 2008;29(5):753-64
35. Tanne D, Gorman MJ, Bates VE, et al. Intravenous tissue plasminogen activator for acute ischemic stroke in patients aged 80 years and older: the tPA stroke survey experience. Stroke 2000;31(2):370-5
36. Manolio TA, Kronmal RA, Burke GL, et al. Short-term predictors of incident stroke in older adults. The Cardiovascular Health Study. Stroke 1996;27(9):1479-86
37. Wang L, Zhang ZG, Zhang RL, Chopp M. 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 2005;25(9):1150-8
38. Beck H, Plate KH. Angiogenesis after cerebral ischemia. Acta Neuropathol 2009;117(5):481-96
39. Petcu EB, Smith RA, Miroiu RI, Opris MM. Angiogenesis in old-aged subjects after ischemic stroke: a cautionary note for investigators. J Angiogenes Res 2010;2:26
40. Ding G, Jiang Q, Li L, et al. Longitudinal magnetic resonance imaging of sildenafil treatment of embolic stroke in aged rats. Stroke 2011;42(12):3537-41
41. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 2002;90(3):284-8
42. Sahara M, Sata M, Morita T, et al. A phosphodiesterase-5 inhibitor vardenafil enhances angiogenesis through a protein kinase G-dependent hypoxiainducible factor-1/vascular endothelial growth factor pathway. Arterioscler Thromb Vasc Biol 2010;30(7):1315-24
43. Zhang Z, Chopp M. Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc Med 2002;12(2):62-6
44. Jiang Q, Zhang ZG, Ding GL, et al. Investigation of neural progenitor cell induced angiogenesis after embolic stroke in rat using MRI. Neuroimage 2005;28(3):698-707
45. Ding G, Jiang Q, Li L, et al. Angiogenesis detected after embolic stroke in rat brain using magnetic resonance T2*WI. Stroke 2008;39(5):1563-8
46. Li L, Jiang Q, Zhang L, et al. Angiogenesis and improved cerebral blood flow in the ischemic boundary area detected by MRI after administration of sildenafil to rats with embolic stroke. Brain Res 2007;1132(1):185-92
47. Slevin M, Krupinski J, Slowik A, et al. Serial measurement of vascular endothelial growth factor and transforming growth factor-beta1 in serum of patients with acute ischemic stroke. Stroke 2000;31(8):1863-70
48. Krupinski J, Kaluza J, Kumar P, et al. Prognostic value of blood vessel density in ischaemic stroke [letter; comment]. Lancet 1993;342(8873):742
49. Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci 2006;26(50):13007-16
50. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 2004;41(5):683-6
51. Carreira BP, Morte MI, Inacio A, et al. Nitric oxide stimulates the proliferation of neural stem cells bypassing the epidermal growth factor receptor. Stem Cells 2010;28(7):1219-30
52. Gomez-Pinedo U, Rodrigo R, Cauli O, et al. cGMP modulates stem cells differentiation to neurons in brain in vivo. Neuroscience 2010;165(4):1275-83
53. Tegenge MA, Rockel TD, Fritsche E, Bicker G. Nitric oxide stimulates human neural progenitor cell migration via cGMP-mediated signal transduction. Cell Mol Life Sci 2011;68(12):2089-99
54. Morshead CM, Craig CG, van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 1998;125(12):2251-61
55. Zhang RL, Zhang ZG, Chopp M. Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology 2008;55(3):345-52
56. Jin K, Wang X, Xie L, et al. Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci USA 2006;103(35):13198-202
57. Macas J, Nern C, Plate KH, Momma S. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 2006;26(50):13114-19
58. Minger SL, Ekonomou A, Carta EM, et al. Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med 2007;2(1):69-74
59. Curtis MA, Kam M, Faull RL. Neurogenesis in humans. Eur J Neurosci 2011;33(6):1170-4
60. Alvarez-Buylla A, Kohwi M, Nguyen TM, Merkle FT. The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb Symp Quant Biol 2008;73:357-65
61. Zhang R, Zhang L, Zhang Z, et al. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 2001;50(5):602-11
62. Chen J, Li Y, Zhang R, et al. Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res 2004;1005(1-2):21-8
63. Packer MA, Stasiv Y, Benraiss A, et al. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 2003;100(16):9566-71
64. Moreno-Lopez B, Romero-Grimaldi C, Noval JA, et al. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 2004;24(1):85-95
65. Luo CX, Jin X, Cao CC, et al. Bidirectional regulation of neurogenesis by neuronal nitric oxide synthase derived from neurons and neural stem cells. Stem Cells 2010;28(11):2041-52
66. Sun Y, Jin K, Childs JT, et al. Neuronal nitric oxide synthase and ischemia-induced neurogenesis. J Cereb Blood Flow Metab 2005;25(4):485-92
67. Luo CX, et al. Reduced neuronal nitric oxide synthase is involved in ischemia-induced hippocampal neurogenesis by up-regulating inducible nitric oxide synthase expression. J Neurochem 2007;103(5):1872-82
68. Chen J, et al. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 2005;25(9):2366-75
69. Zhu DY, et al. Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 2003;23(1):223-9
70. Zhang RL, Zhang Z, Zhang L, et al. Delayed treatment with sildenafil enhances neurogenesis and improves functional recovery in aged rats after focal cerebral ischemia. J Neurosci Res 2006;83(7):1213-19
71. Zhang RL, Chopp M, Roberts C, et al. Sildenafil enhances neurogenesis and oligodendrogenesis in ischemic brain of middle-aged mouse. PLoS One 2012;7(10):e48141
72. Sun F, Wang X, Mao X, et al. Ablation of neurogenesis attenuates recovery of motor function after focal cerebral ischemia in middle-aged mice. PLoS One 2012;7(10):e46326
73. Wang X, Mao X, Xie L, et al. Conditional depletion of neurogenesis inhibits long-term recovery after experimental stroke in mice. PLoS One 2012;7(6):e38932
74. Ueno Y, Chopp M, Zhang L, et al. Axonal outgrowth and dendritic plasticity in the cortical peri-infarct area after experimental stroke. Stroke 2012;43(8):2221-8
75. Zhang L, Chopp M, Zhang RL, et al. Erythropoietin amplifies stroke-induced oligodendrogenesis in the rat. PLoS One 2010;5(6):e11016
76. Carmichael ST. Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 2006;59(5):735-42
77. Shen Q, Wang Y, Kokovay E, et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008;3(3):289-300
78. Tavazoie M, Van der Veken L, Silva-Vargas V, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008;3(3):279-88
79. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000;425(4):479-94
80. Morris DC, Davies K, Zhang Z, Chopp M. Measurement of cerebral microvessel diameters after embolic stroke in rat using quantitative laser scanning confocal microscopy. Brain Res 2000;876(1-2):31-6
81. Zhang ZG, Tsang W, Zhang L, et al. Up-regulation of neuropilin-1 in neovasculature after focal cerebral ischemia in the adult rat. J Cereb Blood Flow Metab 2001;21(5):541-9
82. Lin TN, Wang CK, Cheung WM, Hsu CY. Induction of angiopoietin and Tie receptor mRNA expression after cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 2000;20(2):387-95
83. Jin K, Zhu Y, Sun Y, et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002;99(18):11946-50
84. Teng H, Zhang ZG, Wang L, et al. Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke. J Cereb Blood Flow Metab 2008;28(4):764-71
85. Wang L, Chopp M, Gregg SR, et al. Neural progenitor cells treated with EPO induce angiogenesis through the production of VEGF. J Cereb Blood Flow Metab 2008;28(7):1361-8
86. Roitbak T, Li L, Cunningham LA. Neural stem/progenitor cells promote endothelial cell morphogenesis and protect endothelial cells against ischemia via HIF-1alpha-regulated VEGF signaling. J Cereb Blood Flow Metab 2008;28(9):1530-42
87. Liu XS, Zhang ZG, Zhang RL, et al. Stroke induces gene profile changes associated with neurogenesis and angiogenesis in adult subventricular zone progenitor cells. J Cereb Blood Flow Metab 2007;27(3):564-74
88. Katakowski M, et al. Phosphoinositide 3-kinase promotes adult subventricular neuroblast migration after stroke. J Neurosci Res 2003;74(4):494-501
89. Vojtek AB, Taylor J, DeRuiter SL, et al. Akt regulates basic helix-loop-helix transcription factor-coactivator complex formation and activity during neuronal differentiation. Mol Cell Biol 2003;23(13):4417-27
90. Kawasaki K, Smith RS, Jr., Hsieh CM, et al. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol Cell Biol 2003;23(16):5726-37
91. Kageyama R, Ohtsuka T, Hatakeyama J, et al. Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 2005;306(2):343-8
92. Parras CM, Galli R, Britz O, et al. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 2004;23(22):4495-505
93. Schlossmann J, Feil R, Hofmann F. Signaling through NO and cGMP-dependent protein kinases. Ann Med 2003;35(1):21-7
94. Feil R, Lohmann SM, de Jonge H, et al. Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice. Circ Res 2003;93(10):907-16
95. Takimoto E, Champion HC, Li M, et al. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 2005;11(2):214-22
96. Pyriochou A, Zhou Z, Koika V, et al. The phosphodiesterase 5 inhibitor sildenafil stimulates angiogenesis through a protein kinase G/MAPK pathway. J Cell Physiol 2007;211(1):197-204
97. Feuerstein GZ, Zaleska MM, Krams M, Mitchell J, Kilgannon JH, et al. Missing steps in the STAIR case: a Translational Medicine perspective on the development of NXY-059 for treatment of acute ischemic stroke. J Cereb Blood Flow Metab 2008;28(1):217-19
98. Madden JA. Role of the vascular endothelium and plaque in acute ischemic stroke. Neurology 2012;79(13 Suppl 1):S58-62
99. Roberts BW, Mitchell J, Kilgannon JH, et al. Nitric oxide donor agents for the treatment of ischemia/reperfusion injury in human subjects: a systematic review. Shock 2013;39(3):229-39
100. Silver B, Grover KM, Arcila X, et al. Recovery in a patient with locked-in syndrome. Can J Neurol Sci 2006;33(2):246-9
101. Silver B, McCarthy S, Lu M, et al. Sildenafil treatment of subacute ischemic stroke: a safety study at 25-mg daily for 2 weeks. J Stroke Cerebrovasc Dis 2009;18(5):381-3