Review: Could neurotransmitters influence neurogenesis and neurorepair after stroke?

Neuropathology and Applied Neurobiology

Volumn 39, Issue 7, 2013, Pages 722-735

  Sanchez Mendoza E ^a   Bellver Landete, V ^a   Merino, J J ^a   Gonzalez M P ^a   Martinez Murillo R ^b   Oset Gasque, M J ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO CAJAL   (Spain)

Author keywords

Brain ischaemia; Glutamate; Neural progenitor cells (NPCs); Neurogenesis; Neurorepair; Neurotransmitters

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID; NEUROTRANSMITTER;

CELL TYPE; CEREBROVASCULAR ACCIDENT; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; REVIEW; SUBVENTRICULAR ZONE;

BRAIN ISCHAEMIA; GLUTAMATE; NEURAL PROGENITOR CELLS (NPCS); NEUROGENESIS; NEUROREPAIR; NEUROTRANSMITTERS;

ANIMALS; BRAIN INJURIES; BRAIN ISCHEMIA; HUMANS; NEUROGENESIS; NEURONS; NEUROTRANSMITTER AGENTS; STROKE;

EID: 84886776958     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12082     Document Type: Review

References (92)

1. Castillo J, Alvarez-Sabin J, Dávalos A, Diez-Tejedor E, Lizasoain I, Martínez-Vila E, Vivancos J, Zarranz JJ. Consensus review. Pharmacological neuroprotection in cerebral ischemia: is it still a therapeutic option? Neurologia 2003; 18: 368-384
2. Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J. Measurement of motor recovery after stroke: outcome assessment and sample size requirements. Stroke 1992; 23: 1084-1089
3. Calautti C, Baron JC. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 2003; 34: 1553-1566
4. Hermann DM, Chopp M. Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation. Lancet Neurol 2012; 11: 369-380
5. Cramer SC, Chopp M. Recovery recapitulates ontogeny. Trends Neurosci 2000; 23: 265-271
6. Sohur US, Arlotta P, Macklis J. Developmental controls are re-expressed during induction of neurogenesis in the neocortex of young adult mice. Front Neurosci 2012; 6: 12
7. Lichtenwalner RJ, Parent JM. Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 2006; 26: 1-20
8. Carmichael ST. Targets for neural repair therapies after stroke. Stroke 2010; 41 (10 Suppl.): S124-126
9. Agasse F, Bernardino L, Malva J. SVZ cells as a tool for brain repair. In Interaction between Neurons and Glia in Aging and Disease. Eds JO Malva, AC Rego, RA Cunha, CR Oliveira. New York: Springer, 2007; 81-108
10. Quiñones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 2006; 494: 415-434
11. García-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 1998; 36: 234-248
12. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005; 85: 523-569
13. Sánchez-Mendoza E, Bellver-Landete V, González MP, Merino JJ, Martínez-Murillo R, Oset-Gasque MJ. Brain repair after ischemic stroke: role of neurotransmitters in post-ischemic neurogenesis. Rev Neurol 2012; 55: 533-542
14. Bagley JA, Belluscio L. Dynamic imaging reveals that brain-derived neurotrophic factor can independently regulate motility and direction of neuroblasts within the rostral migratory stream. Neuroscience 2010; 169: 1449-1461
15. Bath KG, Lee FS. Neurotrophic factor control of adult SVZ neurogenesis. Dev Neurobiol 2010; 70: 339-349
16. Jean YY, Lercher LD, Dreyfus CF. Glutamate elicits release of BDNF from basal forebrain astrocytes in a process dependent on metabotropic receptors and the PLC pathway. Neuron Glia Biol 2008; 4: 35-42
17. Pathania M, Yan LD, Bordey A. A symphony of signals conducts early and late stages of adult neurogenesis. Neuropharmacology 2010; 58: 865-876
18. Jeong Y, Mangelsdorf DJ. Nuclear receptor regulation of stemness and stem cell differentiation. Exp Mol Med 2009; 41: 525-537
19. Sun G, Yu RT, Evans RM, Shi Y. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci U S A 2007; 104: 15282-15287
20. Qu Q, Sun G, Li W, Yang S, Ye P, Zhao C, Yu RT, Gage FH, Evans RM, Shi Y. Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat Cell Biol 2010; 12: 31-40
21. Qu Q, Shi Y. Neural stem cells in the developing and adult brains. J Cell Physiol 2009; 221: 5-9
22. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8: 963-970
23. Agasse F, Roger M, Coronas V. Neurogenic and intact or apoptotic non-neurogenic areas of adult brain release diffusible molecules that differentially modulate the development of subventricular zone cell cultures. Eur J Neurosci 2004; 19: 1459-1468
24. Agasse F, Bernardino L, Kristiansen H, Christiansen SH, Ferreira R, Silva B, Grade S, Woldbye DP, Malva JO. Neuropeptide Y promotes neurogenesis in murine subventricular zone. Stem Cells 2008; 26: 1636-1645
25. Li WL, Yu SP, Ogle ME, Ding XS, Wei L. Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice. Dev Neurobiol 2008; 68: 1474-1486
26. Zhang RL, Zhang ZG, Chopp M. Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology 2008; 55: 345-352
27. Chang HC, Yang YR, Wang SG, Wang RY. Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion. Behav Brain Res 2009; 205: 450-455
28. Sánchez-Mendoza E, Burguete MC, Castelló-Ruiz M, González MP, Roncero C, Salom JB, Arce C, Cañadas S, Torregrosa G, Alborch E, Oset-Gasque MJ. Transient focal cerebral ischemia significantly alters not only EAATs but also VGLUTs expression in rats: relevance of changes in reactive astroglia. J Neurochem 2010; 113: 1343-1355
29. Zhang RL, Chopp M, Gregg SR, Toh Y, Roberts C, Letourneau Y, Buller B, Jia L, P Nejad Davarani S, Zhang ZG. Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse. J Cereb Blood Flow Metab 2009; 29: 1240-1250
30. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularisation after stroke. Stroke 2007; 38: 3032-3039
31. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 2006; 26: 125-134
32. Bernardino L, Agasse F, Silva B, Ferreira R, Grade S, Malva JO. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 2008; 26: 2361-2371
33. Leker RR, Lasri V, Chernoguz D. Growth factors improve neurogenesis and outcome after focal cerebral ischemia. J Neural Transm 2009; 116: 1397-1402
34. Madri JA. Modeling the neurovascular niche: implications for recovery from CNS injury. J Physiol Pharmacol 2009; 60 (Suppl. 4): 95-104
35. Harms KM, Li L, Cunningham LA. Murine neural stem/progenitor cells protect neurons against ischemia by HIF-1alpha-regulated VEGF signaling. PLoS ONE 2010; 5: e9767
36. Merino JJ, Gutiérrez-Fernández M, Rodríguez-Frutos B, Alvarez-Grech J, Alcalde ME, Vallejo-Cremades MT, Díez-Tejedor E. CXCR4/SDF-1α-chemokine regulates neurogenesis and/or angiogenesis within the vascular niche of ischemic rats; however, does SDF-1α play a role in repair? Int J Stroke 2011; 6: 466-467
37. Schabitz WR, Berger C, Kollmar R, Seitz M, Tanay E, Kiessling M, Schwab S, Sommer C. Effect of brain-derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 2004; 35: 992-997
38. Saarelainen T, Lukkarinen JA, Koponen S, Grohn OH, Jolkkonen J, Koponen E, Haapasalo A, Alhonen L, Wong G, Koistinaho J, Kauppinen RA, Castrén E. Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons show increased susceptibility to cortical injury after focal cerebral ischemia. Mol Cell Neurosci 2000; 16: 87-96
39. Grade S, Weng YC, Snapyan M, Kriz J, Malva JO, Saghatelyan A. Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum. PLoS ONE 2013; 8: e55039
40. Hayashi T, Abe K, Suzuki H, Itoyama Y. Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 1997; 28: 2039-2044
41. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004; 35: 1732-1737
42. Chen J, Zhang C, Jiang H, Li Y, Zhang L, Robin A, Katakowski M, Lu M, Chopp M. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab 2005; 25: 281-290
43. Reitmeir R, Kilic E, Kilic U, Bacigaluppi M, ElAli A, Salani G, Pluchino S, Gassmann M, Hermann DM. Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity. Brain 2011; 134 (Pt 1): 84-99
44. Reitmeir R, Kilic E, Reinboth BS, Guo Z, ElAli A, Zechariah A, Kilic U, Hermann DM. Vascular endothelial growth factor induces contralesional corticobulbar plasticity and functional neurological recovery in the ischemic brain. Acta Neuropathol (Berl) 2012; 123: 273-284
45. Cali C, Marchaland J, Regazzi R, Bezzi P. SDF 1-alpha (CXCL12) triggers glutamate exocytosis from astrocytes on a millisecond time scale: imaging analysis at the single-vesicle level with TIRF microscopy. J Neuroimmunol 2008; 198: 82-91
46. Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci 2006; 26: 13007-13016
47. Hurtado-Chong A, Yusta-Boyo MJ, Vergaño-Vera E, Bulfone A, de Pablo F, Vicario-Abejón C. IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci 2009; 30: 742-755
48. Bondy CA, Cheng CM. Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol 2004; 490: 25-31
49. Kalluri HS, Dempsey RJ. IGFBP-3 inhibits the proliferation of neural progenitor cells. Neurochem Res 2011; 36: 406-411
50. Naylor M, Bowen KK, Sailor KA, Dempsey RJ, Vemuganti R. Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus. Neurochem Int 2005; 47: 565-572
51. Coronas V, Bantubungi K, Fombonne J, Krantic S, Schiffmann SN. Roger M Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J Neurochem 2004; 91: 1292-1301
52. Gu W, Gu C, Jiang W, Wester P. Neurotransmitter synthesis in poststroke cortical neurogenesis in adult rats. Stem Cell Res 2009; 4: 148-154
53. Banasr M, Hery M, Printemps R, Daszuta A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 2004; 29: 450-460
54. Kim Y, Wang WZ, Comte I, Pastrana E, Tran PB, Brown J, Miller RJ, Doetsch F, Molnár Z, Szele FG. Dopamine stimulation of postnatal murine subventricular zone neurogenesis via the D3 receptor. J Neurochem 2010; 114: 750-760
55. Platel JC, Stamboulian S, Nguyen I, Bordey A. Neurotransmitter signaling in postnatal neurogenesis: the first leg. Brain Res Rev 2010; 63: 60-71
56. Nakamichi N, Takarada T, Yoneda Y. Neurogenesis mediated by gamma-amino-butyric acid and glutamate signaling. J Pharmacol Sci 2009; 110: 133-149
57. Platel JC, Lacar B, Bordey A. GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J Mol Histol 2007; 38: 602-610
58. Platel JC, Dave KA, Bordey A. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol 2008; 586: 3739-3743
59. Platel JC, Heintz T, Young S, Gordon V, Bordey A. Tonic activation of GLUK5 kainate receptors decreases neuroblast migration in whole-mounts of the subventricular zone. J Physiol 2008; 586: 3783-3793
60. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 2010; 65: 859-872
61. Castiglione M, Calafiore M, Costa L, Sortino MA, Nicoletti F, Copani A. Group metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology 2008; 55: 560-567
62. Di Giorgi-Gerevini V, Melchiorri D, Battaglia G, Ricci-Vitiani L, Ciceroni C, Busceti CL, Biagioni F, Iacovelli L, Canudas AM, Parati E, De Maria R, Nicoletti F. Endogenous activation of metabotropic glutamate receptors supports the proliferation and survival of neural progenitor cells. Cell Death Differ 2005; 12: 1124-1133
63. Jansson LC, Louhivuori L, Wigren HK, Nordström T, Louhivuori V, Castrén ML, Åkerman KE. Effect of glutamate receptor antagonists on migrating neural progenitor cells. Eur J Neurosci 2013; 37: 1369-1382
64. Baker SA, Baker KA, Hagg T. Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur J Neurosci 2004; 20: 575-579
65. Cova L, Armentero MT, Zennaro E, Calzarossa C, Bossolasco P, Busca G, Lambertenghi Deliliers G, Polli E, Nappi G, Silani V, Blandini F. Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson's disease. Brain Res 2010; 1311: 12-27
66. O'Keeffe GC, Barker RA, Caldwell MA. Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 2009; 8: 2888-2894
67. Hitoshi S, Maruta N, Higashi M, Kumar A, Kato N, Ikenaka K. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 2007; 85: 3574-3585
68. Soumier A, Banasr M, Goff LK, Daszuta A. Region- and phase-dependent effects of 5-HT(1A) and 5-HT(2C) receptor activation on adult neurogenesis. Eur Neuropsychopharmacol 2010; 20: 336-345
69. Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, Nunes M, Goldman SA, Nedergaard M. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 2007; 302: 356-366
70. Young SZ, Taylor MM, Bordey A. Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur J Neurosci 2011; 33: 1123-1132
71. Centonze D, Rossi S, Tortiglione A, Picconi B, Prosperetti C, De Chiara V, Bernardi G, Calabresi P. Synaptic plasticity during recovery from permanent occlusion of the middle cerebral artery. Neurobiol Dis 2007; 27: 44-53
72. Lai B, Mao XO, Xie L, Jin K, Greenberg DA. Electrophysiological neurodifferentiation of subventricular zone-derived precursor cells following stroke. Neurosci Lett 2008; 442: 305-308
73. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB. Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex. Exp Neurol 2006; 199: 113-121
74. Campos F, Sobrino T, Ramos-Cabrer P, Castellanos M, Blanco M, Rodriguez-Yañez M, Serena J, Leira R, Castillo J. High blood glutamate oxaloacetate transaminase levels are associated with good functional outcome in acute ischemic stroke. J Cereb Blood Flow Metab 2011; 31: 1387-1393
75. Campos F, Sobrino T, Ramos-Cabrer P, Castillo J. Oxaloacetate: a novel neuroprotective for acute ischemic stroke. Int J Biochem Cell Biol 2012; 44: 262-265
76. Rossini PM, Calautti C, Pauri F, Baron JC. Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2003; 2: 493-502
77. Mohajerani MH, Aminoltejari K, Murphy TH. Targeted mini-strokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc Natl Acad Sci U S A 2011; 31: 108-122
78. Overman JJ, Carmichael ST. Plasticity in the Injured brain: more than molecules matter. Neuroscientist 2013. doi:10.1177/1073858413491146
79. Arranz AM, Gottlieb M, Pérez-Cerdá F, Matute C. Increased expression of glutamate transporters in subcortical white matter after transient focal cerebral ischemia. Neurobiol Dis 2010; 37: 156-165
80. Leone DP, Srinivasan K, Brakebusch C, McConnell SK. The rho GTPase Rac1 is required for proliferation and survival of progenitors in the developing forebrain. Dev Neurobiol 2010; 70: 659-678
81. Ponimaskin E, Voyno-Yasenetskaya T, Richter DW, Schachner M, Dityatev A. Morphogenic signaling in neurons via neurotransmitter receptors and small GTPases. Mol Neurobiol 2007; 35: 278-287
82. Shin JJ, Fricker-Gates RA, Perez FA, Leavitt BR, Zurakowski D, Macklis JD. Transplanted neuroblasts differentiate appropriately into projection neurons with correct neurotransmitter and receptor phenotype in neocortex undergoing targeted projection neuron degeneration. J Neurosci 2000; 20: 7404-7416
83. Czupryn A, Zhou YD, Chen X, McNay D, Anderson MP, Flier JS, Macklis JD. Transplanted hypothalamic neurons restore leptin signaling and ameliorate obesity in db/db mice. Science 2011; 334: 1133-1137
84. Madinier A, Bertrand N, Rodier M, Quirié A, Mossiat C, Prigent-Tessier A, Marie C, Garnier P. Ipsilateral versus contralateral spontaneous post-stroke neuroplastic changes: involvement of BDNF? Neuroscience 2013; 231: 169-181
85. Ozdinler PH, Macklis JD. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 2006; 9: 1371-1381
86. Wang PY, Petralia RS, Wang YX, Wenthold RJ, Brenowitz SD. Functional NMDA receptors at axonal growth cones of young hippocampal neurons. J Neurosci 2011; 31: 9289-9297
87. Bacigaluppi M, Pluchino S, Peruzzotti-Jametti L, Kilic E, Kilic U, Salani G, Brambilla E, West MJ, Comi G, Martino G, Hermann DM. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 2009; 132: 2239-2251
88. Andres RH, Horie N, Slikker W, Keren-Gill H, Zhan K, Sun G, Manley NC, Pereira MP, Sheikh LA, McMillan EL, Schaar BT, Svendsen CN, Bliss TM, Steinberg GK. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 2011; 134 (Pt 6): 1777-1789
89. Fernández-Gómez FJ, Hernández F, Argandoña L, Galindo MF, Segura T, Jordán J. Farmacología de la neuroprotección en el ictus isquémico agudo. Rev Neurol 2008; 47: 253-260
90. Darsalia V, Allison SJ, Cusulin C, Monni E, Kuzdas D, Kallur T, Lindvall O, Kokaia Z. Cell number and timing of transplantation determine survival of human neural stem cell grafts in stroke-damaged rat brain. J Cereb Blood Flow Metab 2011; 31: 235-242
91. Ishibashi S, Sakaguchi M, Kuroiwa T, Yamasaki M, Kanemura Y, Shizuko I, Shimazaki T, Onodera M, Okano H, Mizusawa H. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 2004; 78: 215-223
92. Wang YQ, Cui HR, Yang SZ, Sun HP, Qiu MH, Feng XY, Sun FY. VEGF enhance cortical newborn neurons and their neurite development in adult rat brain after cerebral ischemia. Neurochem Int 2009; 55: 629-636