Endothelial nitric oxide synthase regulates white matter changes via the BDNF/TrKB pathway after stroke in mice

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Cui, Xu ^a   Chopp, Michael ^a,b   Zacharek, Alex ^a   Ning, Ruizhuo ^a   Ding, Xiaoshuang ^a   Roberts, Cynthia ^a   Chen, Jieli ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; SYNAPTOPHYSIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL CULTURE; BRAIN INFARCTION; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE FIBER GROWTH; NONHUMAN; OLIGODENDROGLIA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STEM CELL; WHITE MATTER;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, KNOCKOUT; MYELIN SHEATH; NEURITES; NITRIC OXIDE SYNTHASE TYPE III; OLIGODENDROGLIA; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; STROKE; SYNAPSES;

EID: 84893384300     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080358     Document Type: Article

References (60)

1. Persson LA (1981) Growth of nerve-cell body and myelinogenesis in mouse trigemnal ganglion and root: a combined cytofluorometric and morphometric study. J Neurocytol 10: 169-182.
2. Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34: 51-61. (Pubitemid 351378086)
3. Sozmen EG, Kolekar A, Havton LA, Carmichael ST (2009) A white matter stroke model in the mouse: axonal damage, progenitor responses and MRI correlates. J Neurosci Methods 180: 261-272.
4. Endres M, Laufs U, Liao JK, Moskowitz MA (2004) Targeting eNOS for stroke protection. Trends Neurosci 27: 283-289. (Pubitemid 38529957)
5. Chen J, Zacharek A, Zhang C, Jiang H, Li Y, et al. (2005) Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 25: 2366-2375. (Pubitemid 40322278)
6. Chen J, Cui X, Zacharek A, Roberts C, Chopp M (2009) eNOS mediates TO90317 treatment-induced angiogenesis and functional outcome after stroke in mice. Stroke 40: 2532-2538.
7. Chen MJ, Ivy AS, Russo-Neustadt AA (2006) Nitric oxide synthesis is required for exercise-induced increases in hippocampal BDNF and phosphatidylinositol 39 kinase expression. Brain Res Bull 68: 257-268. (Pubitemid 41827729)
8. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, et al. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578. (Pubitemid 28270451)
9. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736. (Pubitemid 32695243)
10. Cui X, Chopp M, Shehadaha A, Zachareka A, Nicholsc NK, et al. (2012) Therapeutic benefit of treatment of stroke with Simvastatin and human umbilical cord blood cells: neurogenesis, synaptic plasticity and axon growth. Cell Transplant.
11. Runyan SA, Phelps PE (2009) Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro. Exp Neurol 216: 95-104.
12. Djalali S, Holtje M, Grosse G, Rothe T, Stroh T, et al. (2005) Effects of brainderived neurotrophic factor (BDNF) on glial cells and serotonergic neurones during development. J Neurochem 92: 616-627. (Pubitemid 40189464)
13. Xiao J, Wong AW, Willingham MM, van den Buuse M, Kilpatrick TJ, et al. (2010) Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neurosignals 18: 186-202.
14. Liu Z, Li Y, Zhang RL, Cui Y, Chopp M (2011) Bone marrow stromal cells promote skilled motor recovery and enhance contralesional axonal connections after ischemic stroke in adult mice. Stroke 42: 740-744.
15. Linares D, Taconis M, Mana P, Correcha M, Fordham S, et al. (2006) Neuronal nitric oxide synthase plays a key role in CNS demyelination. J Neurosci 26: 12672-12681. (Pubitemid 44904562)
16. Wiencken AE, Casagrande VA (1999) Endothelial nitric oxide synthetase (eNOS) in astrocytes: another source of nitric oxide in neocortex. Glia 26: 280-290. (Pubitemid 29257190)
17. Dinerman JL, Dawson TM, Schell MJ, Snowman A, Snyder SH (1994) Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc Natl Acad Sci U S A 91: 4214-4218. (Pubitemid 24143403)
18. Farr TD, Whishaw IQ (2002) Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke. Stroke 33: 1869-1875. (Pubitemid 34761078)
19. Frisen J, Verge VM, Fried K, Risling M, Persson H, et al. (1993) Characterization of glial trkB receptors: differential response to injury in the central and peripheral nervous systems. Proc Natl Acad Sci U S A 90: 4971-4975. (Pubitemid 23182957)
20. Matthias GKaE (2008) eNOS And Stroke: Prevention, Treatment And Recovery 537-550 p.
21. Laufs U, Endres M, Stagliano N, Amin-Hanjani S, Chui DS, et al. (2000) Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J Clin Invest 106: 15-24. (Pubitemid 30437236)
22. Bouloumie A, Schini-Kerth VB, Busse R (1999) Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardiovasc Res 41: 773-780. (Pubitemid 29130642)
23. Yuhanna IS, MacRitchie AN, Lantin-Hermoso RL, Wells LB, Shaul PW (1999) Nitric oxide (NO) upregulates NO synthase expression in fetal intrapulmonary artery endothelial cells. Am J Respir Cell Mol Biol 21: 629-636. (Pubitemid 129586598)
24. Zheng J, Bird IM, Melsaether AN, Magness RR (1999) Activation of the mitogen-activated protein kinase cascade is necessary but not sufficient for basic fibroblast growth factor- and epidermal growth factor-stimulated expression of endothelial nitric oxide synthase in ovine fetoplacental artery endothelial cells. Endocrinology 140: 1399-1407. (Pubitemid 29104246)
25. Hernandez R, Martinez-Lara E, Del Moral ML, Blanco S, Canuelo A, et al. (2004) Upregulation of endothelial nitric oxide synthase maintains nitric oxide production in the cerebellum of thioacetamide cirrhotic rats. Neuroscience 126: 879-887. (Pubitemid 38780893)
26. Gabbott PL, Bacon SJ (1996) Localisation of NADPH diaphorase activity and NOS immunoreactivity in astroglia in normal adult rat brain. Brain Res 714: 135-144. (Pubitemid 26120801)
27. Barna M, Komatsu T, Reiss CS (1996) Activation of type III nitric oxide synthase in astrocytes following a neurotropic viral infection. Virology 223: 331-343. (Pubitemid 26319593)
28. Ben Achour S, Pascual O (2012) Astrocyte-neuron communication: functional consequences. Neurochem Res 37: 2464-2473.
29. Theodosis DT, Poulain DA, Oliet SH (2008) Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88: 983-1008.
30. Halassa MM, Fellin T, Haydon PG (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13: 54-63. (Pubitemid 46186152)
31. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640. (Pubitemid 41059337)
32. Amin-Hanjani S, Stagliano NE, Yamada M, Huang PL, Liao JK, et al. (2001) Mevastatin, an HMG-CoA reductase inhibitor, reduces stroke damage and upregulates endothelial nitric oxide synthase in mice. Stroke 32: 980-986.
33. Gertz K, Priller J, Kronenberg G, Fink KB, Winter B, et al. (2006) Physical activity improves long-term stroke outcome via endothelial nitric oxide synthasedependent augmentation of neovascularization and cerebral blood flow. Circ Res 99: 1132-1140. (Pubitemid 44729938)
34. Endres M, Laufs U, Huang Z, Nakamura T, Huang P, et al. (1998) Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 95: 8880-8885. (Pubitemid 28350583)
35. Cui X, Chopp M, Zacharek A, Zhang C, Roberts C, et al. (2009) Role of endothelial nitric oxide synthetase in arteriogenesis after stroke in mice. Neuroscience 159: 744-750.
36. Calhoun ME, Jucker M, Martin LJ, Thinakaran G, Price DL, et al. (1996) Comparative evaluation of synaptophysin-based methods for quantification of synapses. J Neurocytol 25: 821-828. (Pubitemid 27032366)
37. Alix JJ, Domingues AM (2011) White matter synapses: form, function, and dysfunction. Neurology 76: 397-404.
38. Bakiri Y, Karadottir R, Cossell L, Attwell D (2011) Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum. J Physiol 589: 559-573.
39. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4: 399-415. (Pubitemid 37280178)
40. Dziewulska D, Rafalowska J, Podlecka A, Szumanska G (2004) Remote morphological changes in the white matter after ischaemic stroke. Folia Neuropathol 42: 75-80. (Pubitemid 38979242)
41. Alix JJ (2006) Recent biochemical advances in white matter ischaemia. Eur Neurol 56: 74-77.
42. Pantoni L, Garcia JH, Gutierrez JA (1996) Cerebral white matter is highly vulnerable to ischemia. Stroke 27: 1641-1646; discussion 1647.
43. McIver SR, Muccigrosso M, Gonzales ER, Lee JM, Roberts MS, et al. (2010) Oligodendrocyte degeneration and recovery after focal cerebral ischemia. Neuroscience 169: 1364-1375.
44. Shi X, Kang Y, Hu Q, Chen C, Yang L, et al. (2010) A long-term observation of olfactory ensheathing cells transplantation to repair white matter and functional recovery in a focal ischemia model in rat. Brain Res 1317: 257-267.
45. Johnston MV (2009) Plasticity in the developing brain: implications for rehabilitation. Dev Disabil Res Rev 15: 94-101.
46. Pozzo-Miller LD, Gottschalk W, Zhang L, McDermott K, Du J, et al. (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J Neurosci 19: 4972-4983. (Pubitemid 29270132)
47. Madinier A, Bertrand N, Rodier M, Quirie A, Mossiat C, et al. (2013) Ipsilateral versus contralateral spontaneous post-stroke neuroplastic changes: involvement of BDNF? Neuroscience 231: 169-181.
48. Liu HS, Shen H, Harvey BK, Castillo P, Lu H, et al. (2011) Post-treatment with amphetamine enhances reinnervation of the ipsilateral side cortex in stroke rats. Neuroimage 56: 280-289.
49. Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F (2004) Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience 125: 129-139. (Pubitemid 38402166)
50. Medina DL, Sciarretta C, Calella AM, Von Bohlen Und Halbach O, Unsicker K, et al. (2004) TrkB regulates neocortex formation through the Shc/PLCgamma-mediated control of neuronal migration. EMBO J 23: 3803-3814. (Pubitemid 39389711)
51. Bergami M, Santi S, Formaggio E, Cagnoli C, Verderio C, et al. (2008) Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 183: 213-221.
52. Kovalchuk Y, Holthoff K, Konnerth A (2004) Neurotrophin action on a rapid timescale. Curr Opin Neurobiol 14: 558-563. (Pubitemid 39349616)
53. Juric DM, Miklic S, Carman-Krzan M (2006) Monoaminergic neuronal activity up-regulates BDNF synthesis in cultured neonatal rat astrocytes. Brain Res 1108: 54-62. (Pubitemid 44278004)
54. Rudge JS, Pasnikowski EM, Holst P, Lindsay RM (1995) Changes in neurotrophic factor expression and receptor activation following exposure of hippocampal neuron/astrocyte cocultures to kainic acid. J Neurosci 15: 6856-6867.
55. Kim H, Li Q, Hempstead BL, Madri JA (2004) Paracrine and autocrine functions of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in brain-derived endothelial cells. J Biol Chem 279: 33538-33546. (Pubitemid 39063002)
56. Wang H, Ward N, Boswell M, Katz DM (2006) Secretion of brain-derived neurotrophic factor from brain microvascular endothelial cells. Eur J Neurosci 23: 1665-1670.
57. Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642. (Pubitemid 36930455)
58. Du Y, Fischer TZ, Lee LN, Lercher LD, Dreyfus CF (2003) Regionally specific effects of BDNF on oligodendrocytes. Dev Neurosci 25: 116-126. (Pubitemid 37100207)
59. Du Y, Lercher LD, Zhou R, Dreyfus CF (2006) Mitogen-activated protein kinase pathway mediates effects of brain-derived neurotrophic factor on differentiation of basal forebrain oligodendrocytes. J Neurosci Res 84: 1692-1702. (Pubitemid 44892603)
60. Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26: 10967-10983. (Pubitemid 44772187)