Multifaces of neuropeptide Y in the brain - Neuroprotection, neurogenesis and neuroinflammation

Neuropeptides

Volumn 46, Issue 6, 2012, Pages 299-308

  Malva, J O ^b   Xapelli, S ^d,e   Baptista, S ^c   Valero, J ^a   Agasse, F ^a   Ferreira, R ^a   Silva, A P ^c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^e UNIVERSITY OF LISBON   (Portugal)

Author keywords

Microglia; Neurogenesis; Neuroinflammation; Neuropeptide Y; Neuroprotection; Stem cells

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; METHAMPHETAMINE; NEUROPEPTIDE Y; TRIMETHYLTIN;

ALZHEIMER DISEASE; APOPTOSIS; ASTROCYTE; BASAL CELL; BLOOD BRAIN BARRIER; BRAIN INFARCTION SIZE; CALCIUM TRANSPORT; CEREBROSPINAL FLUID; DENTATE GYRUS; EPILEPTIC DISCHARGE; EXCITOTOXICITY; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL STRATUM LUCIDUM; HUMAN; LAMINA PROPRIA; METHAMPHETAMINE DEPENDENCE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROBLAST; NEUROPROTECTION; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PARKINSON DISEASE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RETINA; REVIEW; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; BRAIN CHEMISTRY; CELL DEATH; DENTATE GYRUS; HIPPOCAMPUS; HUMANS; INFLAMMATION; NEUROGENESIS; NEUROPEPTIDE Y; NEUROPROTECTIVE AGENTS; OLFACTORY MUCOSA; RETINA;

EID: 84869883047     PISSN: 01434179     EISSN: 15322785     Source Type: Journal    
DOI: 10.1016/j.npep.2012.09.001     Document Type: Review

References (185)

1. Abbott N.J., Patabendige A.A., Dolman D.E., Yusof S.R., Begley D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37:13-25.
2. Agasse F., Bernardino L., Kristiansen H., Christiansen S.H., Ferreira R., Silva B., Grade S., Woldbye D.P., Malva J.O. Neuropeptide Y promotes neurogenesis in murine subventricular zone. Stem Cells 2008, 26:1636-1645.
3. Aimone J.B., Wiles J., Gage F.H. Computational influence of adult neurogenesis on memory encoding. Neuron 2009, 61:187-202.
4. Alberio T., Lopiano L., Fasano M. Cellular models to investigate biochemical pathways in Parkinson's disease. FEBS J. 2012, 279:1146-1155.
5. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 1969, 137:433-457.
6. Alvaro A.R., Rosmaninho-Salgado J., Santiago A.R., Martins J., Aveleira C., Santos P.F., Pereira T., Gouveia D., Carvalho A.L., Grouzmann E., Ambrósio A.F., Cavadas C. NPY in rat retina is present in neurons, in endothelial cells and also in microglial and Muller cells. Neurochem. Int. 2007, 50:757-763.
7. Alvaro A.R., Martins J., Costa A.C., Fernandes E., Carvalho F., Ambrósio A.F., Cavadas C. Neuropeptide Y protects retinal neural cells against cell death induced by ecstasy. Neuroscience 2008, 152:97-105.
8. Alvaro A.R., Martins J., Araujo I.M., Rosmaninho-Salgado J., Ambrosio A.F., Cavadas C. Neuropeptide Y stimulates retinal neural cell proliferation - involvement of nitric oxide. J. Neurochem. 2008, 105:2501-2510.
9. Amador-Arjona A., Elliott J., Miller A., Ginbey A., Pazour G.J., Enikolopov G., Roberts A.J., Terskikh A.V. Primary cilia regulate proliferation of amplifying progenitors in adult hippocampus: implications for learning and memory. J. Neurosci. 2011, 31:9933-9944.
10. Amantea D., Nappi G., Bernardi G., Bagetta G., Corasaniti M.T. Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J. 2009, 276:13-26.
11. Baptista S., Bento A.R., Goncalves J., Bernardino L., Summavielle T., Lobo A., Fontes-Ribeiro C., Malva J.O., Agasse F., Silva A.P. Neuropeptide Y promotes neurogenesis and protection against methamphetamine-induced toxicity in mouse dentate gyrus-derived neurosphere cultures. Neuropharmacology 2012, 62:2413-2423.
12. Barros L.F., Hermosilla T., Castro J. Necrotic volume increase and the early physiology of necrosis. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2001, 130:401-409.
13. Bauer J., Bradl M., Hickley W.F., Forss-Petter S., Breitschopf H., Linington C., Wekerle H., Lassmann H. T-cell apoptosis in inflammatory brain lesions: destruction of T cells does not depend on antigen recognition. Am. J. Pathol. 1998, 153:715-724.
14. Bedoui S., Miyake S., Lin Y., Miyamoto K., Oki S., Kawamura N., Beck-Sickinger A., von Horsten S., Yamamura T. Neuropeptide Y (NPY) supresses experimental autoimmune encephalomyelitis: NPY1 receptor-specific inhibition of autoreactive Th1 responses in vivo. J. Immunol. 2003, 17:3451-3458.
15. Bedoui S., von Horsten S., Gebhardt T. A role for neuropeptide Y (NPY) in phagocytosis: implications for innate and adaptive immunity. Peptides 2007, 28:373-376.
16. Bedoui S., Kromer A., Gebhardt T., Jacobs R., Raber K., Dimitrijevic T., Heine J., von Horsten S. Neuropeptide Y receptor-specifically modulates human neutrophil function. J. Neuroimmunol. 2008, 195:88-95.
17. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
18. Biebl M., Cooper C.M., Winkler J., Kuhn H.G. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 2000, 291:17-20.
19. 2+ influx into cultured dorsal root ganglion neurones of the rat via a Y2 receptor. Br. J. Pharmacol. 1991, 103:1781-1789.
20. Block M.L., Zecca L., Hong J.-S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurol. 2007, 8:57-69.
21. Bonaguidi M.A., Wheeler M.A., Shapiro J.S., Stadel R.P., Sun G.J., Ming G.L., Song H. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011, 145:1142-1155.
22. Breton-Provencher V., Lemasson M., Peralta M.R., Saghatelyan A. Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J. Neurosci. 2009, 29:15245-15257.
23. Bruel-Jungerman E., Lucassen P.J., Francis F. Cholinergic influences on cortical development and adult neurogenesis. Behav. Brain Res. 2011, 221:379-388.
24. Buja L.M., Eigenbrodt M.L., Eigenbrodt E.H. Apoptosis and necrosis. Basic types and mechanisms of cell death. Arch. Pathol. Lab. Med. 1993, 117:1208-1214.
25. Buxbaum J.N., Ye Z., Reixach N., Friske L., Levy C., Das P., Golde T., Masliah E., Roberts A.R., bartfai T. Transthyretin protects Alzheimer's mice from the behavioral and biochemical effects of Abeta toxicity. Proc. Natl. Acad. Sci U. S. A. 2008, 105:2681-2686.
26. Cadet J.L., Krasnova I.N. Molecular bases of methamphetamine-induced neurodegeneration. Int. Rev. Neurobiol. 2009, 88:101-119.
27. Cannizzaro C., Tel B.C., Rose S., Zeng B.Y., Jenner P. Increased neuropeptide Y mRNA expression in striatum in Parkinson's disease. Brain Res. Mol. Brain Res. 2003, 110:169-176.
28. Charles N.A., Holland E.C., Gilbertson R., Glass R., Kettenmann H. The brain tumor microenvironment. Glia 2011, 59:1169-1180.
29. Chavarria A., Alcocer-Varela J. Is damage in central nervous system due to inflammation?. Autoimmun. Rev. 2004, 3:251-260.
30. Chen S.H., Cheung R.T. Peripheral and central administration of neuropeptide Y in a rat middle cerebral artery occlusion stroke model reduces cerebral blood flow and increases infarct volume. Brain Res. 2002, 927:138-143.
31. Chen S.H., Cheung R.T. Intracerebroventricular injection of a neuropeptide Y-Y1 receptor agonist increases while BIBP3226, a Y1 antagonist, reduces the infarct volume following transient middle cerebral artery occlusion in rats. Neuroscience 2003, 116:119-126.
32. Chen S.H., Cheung R.T. Neuropeptide Y-Y1 receptor agonist worsens while antagonist improves survival of cultured Y1-expressing neuronal cells following oxygen and glucose deprivation. J. Biomed. Sci. 2004, 11:781-788.
33. Chen S.H., Cheung R.T. Neuropeptide Y and its receptor analogs differentially modulate the immunoreactivity for neuronal or endothelial nitric oxide synthase in the rat brain following focal ischemia with reperfusion. J. Biomed. Sci. 2005, 12:267-278.
34. Chen S.H., Fung P.C., Cheung R.T. Neuropeptide Y-Y1 receptor modulates nitric oxide level during stroke in the rat. Free Radic. Biol. Med. 2002, 32:776-784.
35. Cheung R.T., Cechetto D.F. Neuropeptide changes following excitotoxic lesion of the insular cortex in rats. J. Comp. Neurol. 1995, 362:535-550.
36. Cheung R.T., Cechetto D.F. Colchicine affects cortical and amygdalar neurochemical changes differentially after middle cerebral artery occlusion in rats. J. Comp. Neurol. 1997, 387:27-41.
37. Cheung R.T., Cechetto D.F. Neuropeptide Y-Y1 receptor antisense oligodeoxynucleotide increases the infarct volume after middle cerebral artery occlusion in rats. Neuroscience 2000, 98:771-777.
38. Cheung A., Newland P.L., Zaben M., Attard G.S., Gray W.P. Intracellular nitric oxide mediates neuroproliferative effect of neuropeptide y on postnatal hippocampal precursor cells. J. Biol. Chem. 2012, 287:20187-20196.
39. Choi D.W. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci. Lett. 1985, 58:293-297.
40. Choi J., Koh S. Role of brain inflammation in epileptogenesis. Yonsei Med. J. 2008, 49:1-18.
41. Choi D.W., Koh J.Y., Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J. Neurosci. 1988, 8:185-196.
42. Corona A.W., Fenn A.M., Godbout J.P. Cognitive and behavioral consequences of impaired immunoregulation in aging. J. Neuroimm. Pharmacol. 2012, 7:7-23.
43. Corvino, V., Marchese, E., Giannetti, S., Lattanzi, W., Bonvissuto, D., Biamonte, F., Mongiovi, A.M., Michetti, F., Geloso, M.C., 2012. The neuroprotective and neurogenic effects of neuropeptide Y administration in an animal model of hippocampal neurodegeneration and temporal lobe epilepsy induced by trimethyltin. J. Neurochem. [Epub ahead of print]. http://dx.doi.org/10.1111/j.1471-4159.2012.07770.x.
44. Croce N., Dinallo V., Ricci V., Federici G., Caltagirone C., Bernardini S., Angelucci F. Neuroprotective effect of neuropeptide Y against beta-amyloid 25-35 toxicity in SH-SY5Y neuroblastoma cells is associated with increased neurotrophin production. Neurodegener. Dis. 2011, 8:300-309.
45. Curtis M.A., Kam M., Nannmark U., Anderson M.F., Axell M.Z., Wikkelso C., Holtas S., van Roon-Mom W.M., Bjork-Eriksson T., Nordborg C., Frisen J., Dragunow M., Faull R.L., Eriksson P.S. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
46. Czeh M., Gressens P., Kaindl A.M. The yin and yang of microglia. Dev. Neurosci. 2011, 33:199-209.
47. Danton G.H., Dietrich W.D. Inflammatory mechanisms after ischemia and stroke. J. Neuropathol. Exp. Neurol. 2003, 62:127-136.
48. De La Fuente M., Del Río M., Víctor V.M., Medina S. Neuropeptide Y effects on murine natural killer activity: changes with ageing and cAMP involvement. Regul. Pept. 2001, 101:73-79.
49. De Mello Reis R.A., Schitine C.S., Kofalvi A., Grade S., Cortes L., Gardino P.F., Malva J.O., Mello F.G. Functional identification of cell phenotypes differentiating from mice retinal neurospheres using single cell calcium imaging. Cell. Mol. Neurobiol. 2011, 31:835-846.
50. Decressac M., Prestoz L., Veran J., Cantereau A., Jaber M., Gaillard A. Neuropeptide Y stimulates proliferation, migration and differentiation of neural precursors from the subventricular zone in adult mice. Neurobiol. Dis. 2009, 34:441-449.
51. Decressac M., Wright B., David B., Tyers P., Jaber M., Barker R.A., Gaillard A. Exogenous neuropeptide Y promotes in vivo hippocampal neurogenesis. Hippocampus 2011, 21:233-238.
52. Decressac M., Pain S., Chabeauti P.Y., Frangeul L., Thiriet N., Herzog H., Vergote J., Chalon S., Jaber M., Gaillard A. Neuroprotection by neuropeptide Y in cell and animal models of Parkinson's disease. Neurobiol. Aging 2012, 33:2125-2137.
53. Diaz D., Valero J., Airado C., Baltanas F.C., Weruaga E., Alonso J.R. Sexual dimorphic stages affect both proliferation and serotonergic innervation in the adult rostral migratory stream. Exp. Neurol. 2009, 216:357-364.
54. Dimitrijevic, M., Stanojevic, S., 2011. The intriguing mission of NPY in the immune system. Amino Acids [Epub ahead of print].
55. Doetsch F., García-Verdugo J.M., Álvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17:5046-5061.
56. Domin H., Kajta M., Smialowska M. Neuroprotective effects of MTEP, a selective mGluR5 antagonists and neuropeptide Y on the kainate-induced toxicity in primary neuronal cultures. Pharmacol. Rep. 2006, 58:846-858.
57. Doring A., Yong V.W. The good, the bad and the ugly. Macrophages/microglia with a focus on myelin repair. Front. Biosci. (Schol. Ed.) 2011, 3:846-856.
58. Ferreira R., Xapelli S., Santos T., Silva A.P., Cristóvão A., Cortes L., Malva J.O. Neuropeptide Y modulation of interleukin-1 beta (IL-1{beta})-induced nitric oxide production in microglia. J. Biol. Chem. 2010, 285:41921-41934.
59. Ferreira R., Santos T., Viegas M., Cortes L., Bernardino L., Vieira O.V., Malva J.O. Neuropeptide Y inhibits interleukin-1β-induced phagocytosis by microglial cells. J. Neuroinflammation 2011, 8:169.
60. Ferreira R., Santos T., Cortes L., Cochaud S., Agasse F., Silva A.P., Xapelli S., Malva J.O. Neuropeptide Y inhibits interleukin-1 beta-induced microglia motility. J. Neurochem. 2012, 120:93-105.
61. Ferri K.F., Kroemer G. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 2001, 3:E255-E263.
62. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell Neurosci. 2003, 23:373-382.
63. Forster E., Jossin Y., Zhao S., Chai X., Frotscher M., Goffinet A.M. Recent progress in understanding the role of Reelin in radial neuronal migration, with specific emphasis on the dentate gyrus. Eur. J. Neurosci. 2006, 23:901-909.
64. Frank M.G., Barrientos R.M., Biedenkapp J.C., Rudy J.W., Watkins L.R., Maier S.F. MRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol. Aging 2006, 27:717-722.
65. García-Verdugo J.M., Doetsch F., Wichterle H., Lim D.A., Alvarez-Buylla A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J. Neurobiol. 1998, 36:234-248.
66. Garden G., Möller T. Microglia biology in health and disease. J. Neuroimmune Pharmacol. 2006, 1:127-137.
67. Garthwaite G., Garthwaite J. Neurotoxicity of excitatory amino acid receptor agonists in rat cerebellar slices: dependence on calcium concentration. Neurosci. Lett. 1986, 66:193-198.
68. Geloso, M.C., Corvino, V., Michetti, F., 2011. Trimethyltin-induced hippocampal degeneration as a tool to investigate neurodegenerative processes. Neurochem. Int. [Epub ahead of print].
69. Gerald C., Walker M.W., Criscione L., Gustafson E.L., Batzl-Hartmann C., Smith K.E., Vaysse P., Durkin M.M., Laz T.M., Linemeyer D.L., Schaffhauser A.O., Whitebread S., Hofbauer K.G., Taber R.I., Branchek T.A., Weinshank R.L. A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 1996, 382:168-171.
70. Gheusi G., Ortega-Perez I., Murray K., Lledo P.M. A niche for adult neurogenesis in social behavior. Behav. Brain Res. 2009, 200:315-322.
71. Giannelli S.G., Demontis G.C., Pertile G., Rama P., Broccoli V. Adult human Muller glia cells are a highly efficient source of rod photoreceptors. Stem Cells 2011, 29:344-356.
72. Goncalves J., Baptista S., Martins T., Milhazes N., Borges F., Ribeiro C.F., Malva J.O., Silva A.P. Methamphetamine-induced neuroinflammation and neuronal dysfunction in the mice hippocampus: preventive effect of indomethacin. Eur. J. Neurosci. 2010, 31:315-326.
73. Graeber M.B., Li W., Rodriguez M.L. Role of microglia in CNS inflammation. FEBS Lett. 2011, 585:3798-3805.
74. Gray W.P. Neuropeptide Y signalling on hippocampal stem cells in health and disease. Mol. Cell. Endocrinol. 2008, 288:52-62.
75. Greber S., Schwarzer C., Sperk G. Neuropeptide Y inhibits potassium-stimulated glutamate release through Y2 receptors in rat hippocampal slices in vitro. Br. J. Pharmacol. 1994, 113:737-740.
76. Gubert F., Zaverucha-do-Valle C., Pimentel-Coelho P.M., Mendez-Otero R., Santiago M.F. Radial glia-like cells persist in the adult rat brain. Brain Res. 2009, 1258:43-52.
77. Gustafson E.L., Smith K.E., Durkin M.M., Walker M.W., Gerald C., Weinshank R., Branchek T.A. Distribution of the neuropeptide Y Y2 receptor mRNA in rat central nervous system. Brain Res. Mol. Brain Res. 1997, 46:223-235.
78. Han Y.G., Spassky N., Romaguera-Ros M., Garcia-Verdugo J.M., Aguilar A., Schneider-Maunoury S., Alvarez-Buylla A. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 2008, 11:277-284.
79. Hansel D.E., Eipper B.A., Ronnett G.V. Regulation of olfactory neurogenesis by amidated neuropeptides. J. Neurosci. Res. 2001, 66:1-7.
80. Hansel D.E., Eipper B.A., Ronnett G.V. Neuropeptide Y functions as a neuroproliferative factor. Nature 2001, 410:940-944.
81. Hara M.R., Snyder S.H. Cell signaling and neuronal death. Annu. Rev. Pharmacol. Toxicol. 2007, 47:117-141.
82. Hara Y., Nomura T., Yoshizaki K., Frisen J., Osumi N. Impaired hippocampal neurogenesis and vascular formation in ephrin-A5-deficient mice. Stem Cells 2010, 28:974-983.
83. Hastings N.B., Gould E. Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 1999, 413:146-154.
84. Henry C.J., Huang Y., Wynne A.M., Godbout J.P. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav. Immun. 2009, 23:309-317.
85. Holler J., Zakrzewicz A., Kaufmann A., Wilhelm J., Fuchs-Moll G., Dietrich H., Padberg W., Kuncová J., Kummer W., Grau V. Neuropeptide Y is expressed by rat mononuclear blood leukocytes and strongly down-regulated during inflammation. J. Immunol. 2008, 181:6906-6912.
86. Horner K.A., Westwood S.C., Hanson G.R., Keefe K.A. Multiple high doses of methamphetamine increase the number of preproneuropeptide Y mRNA-expressing neurons in the striatum of rat via a dopamine D1 receptor-dependent mechanism. J. Pharmacol. Exp. Ther. 2006, 319:414-421.
87. Howell O.W., Scharfman H.E., Herzog H., Sundstrom L.E., Beck-Sickinger A., Gray W.P. Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 2003, 86:646-659.
88. Howell O.W., Doyle K., Goodman J.H., Scharfman H.E., Herzog H., Pringle A., Beck-Sickinger A.G., Gray W.P. Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem. 2005, 93:560-570.
89. Howell O.W., Silva S., Scharfman H.E., Sosunov A.A., Zaben M., Shatya A., McKhann G., Herzog H., Laskowski A., Gray W.P. Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol. Dis. 2007, 26:174-188.
90. Husum H., Aznar S., Hoyer-Hansen S., Larsen M.H., Mikkelsen J.D., Moller A., Mathe A.A., Wortwein G. Exacerbated loss of cell survival, neuropeptide Y-immunoreactive (IR) cells, and serotonin-IR fiber lengths in the dorsal hippocampus of the aged flinders sensitive line "depressed" rat: Implications for the pathophysiology of depression?. J. Neurosci. Res. 2006, 84:1292-1302.
91. Ide Y., Fujiyama F., Okamoto-Furuta K., Tamamaki N., Kaneko T., Hisatsune T. Rapid integration of young newborn dentate gyrus granule cells in the adult hippocampal circuitry. Eur. J. Neurosci. 2008, 28:2381-2392.
92. Iwai N., Zhou Z., Roop D.R., Behringer R.R. Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem cells 2008, 26:1298-1306.
93. Jia C., Hegg C.C. NPY mediates ATP-induced neuroproliferation in adult mouse olfactory epithelium. Neurobiol. Dis. 2010, 38:405-413.
94. Jurgens H.A., Johnson R.W. Dysregulated neuronal-microglial cross-talk during aging, stress and inflammation. Exp. Neurol. 2012, 233:40-48.
95. Kanekar S., Jia C., Hegg C.C. Purinergic receptor activation evokes neurotrophic factor neuropeptide Y release from neonatal mouse olfactory epithelial slices. J. Neurosci. Res. 2009, 87:1424-1434.
96. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat. Immunol. 2010, 11:373-384.
97. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 2007, 10:355-362.
98. Kerever A., Schnack J., Vellinga D., Ichikawa N., Moon C., Arikawa-Hirasawa E., Efird J.T., Mercier F. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 2007, 25:2146-2157.
99. Koning N., Uitdehaag B.M.J., Huitinga I., Hoek R.M. Restoring immune suppression in the multiple sclerosis brain. Prog. Neurobiol. 2009, 89:359-368.
100. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat. Med. 2000, 6:513-519.
101. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 2003, 467:455-463.
102. Lagace D.C., Whitman M.C., Noonan M.A., Ables J.L., DeCarolis N.A., Arguello A.A., Donovan M.H., Fischer S.J., Farnbauch L.A., Beech R.D., DiLeone R.J., Greer C.A., Mandyam C.D., Eisch A.J. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 2007, 27:12623-12629.
103. Larsen P.J., Sheikh S.P., Jakobsen C.R., Schwartz T.W., Mikkelsen J.D. Regional distribution of putative NPY Y1 receptors and neurons expressing Y1mRNA in forebrain areas of the central nervous system. Eur. J. Neurosci. 1993, 5:1622-1637.
104. Lee S.W., Clemenson G.D., Gage F.H. New neurons in an aged brain. Behav. Brain Res. 2011, 227:497-507.
105. Leung C.T., Coulombe P.A., Reed R.R. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 2007, 10:720-726.
106. Llorens-Martin M., Torres-Aleman I., Trejo J.L. Mechanisms mediating brain plasticity: IGF1 and adult hippocampal neurogenesis. Neuroscientist 2009, 15:134-148.
107. Loane D.J., Byrnes K.R. Role of microglia in neurotrauma. Neurotherapeutics 2010, 7:366-377.
108. Lois C., Álvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
109. Lois C., García-Verdugo J.M., Álvarez-Buylla A. Chain migration of neuronal precursors. Science 1996, 271:978-981.
110. Majno G., Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 1995, 146:3-15.
111. Mayer E.J., Hughes E.H., Carter D.A., Dick A.D. Nestin positive cells in adult human retina and in epiretinal membranes. Br. J. Ophthalmol. 2003, 87:1154-1158.
112. Mayer E.J., Carter D.A., Ren Y., Hughes E.H., Rice C.M., Halfpenny C.A., Scolding N.J., Dick A.D. Neural progenitor cells from postmortem adult human retina. Br. J. Ophthalmol. 2005, 89:102-106.
113. Milenkovic I., Weick M., Wiedemann P., Reichenbach A., Bringmann A. Neuropeptide Y-evoked proliferation of retinal glial (Muller) cells. Graefe's Arch. Clin. Exp. Ophthalmol. 2004, 242:944-950.
114. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
115. Mirzadeh Z., Merkle F.T., Soriano-Navarro M., Garcia-Verdugo J.M., Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008, 3:265-278.
116. Mu Y., Lee S.W., Gage F.H. Signaling in adult neurogenesis. Curr. Opin. Neurobiol. 2010, 20:416-423.
117. Nadler J.V., Tu B., Timofeeva O., Jiao Y., Herzog H. Neuropeptide Y in the recurrent mossy fiber pathway. Peptides 2007, 28:357-364.
118. Neveu I., Remy S., Naveilhan P. The neuropeptide Y receptors, Y1 and Y2, are transiently and differentially expressed in the developing cerebellum. Neuroscience 2002, 113:767-777.
119. Nunes A.F., Saraiva M.J., Sousa M.M. Transthyretin knockouts are a new mouse model for increased neuropeptide Y. FASEB J. 2006, 20:166-168.
120. Nunes A.F., Montero M., Franquinho F., Santos S.D., Malva J., Zimmer J., Sousa M.M. Transthyretin knockout mice display decreased susceptibility to AMPA-induced neurodegeneration. Neurochem. Int. 2009, 55:454-457.
121. Oboti L., Schellino R., Giachino C., Chamero P., Pyrski M., Leinders-Zufall T., Zufall F., Fasolo A., Peretto P. Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice. Front. Neurosci. 2011, 5:113.
122. Olah M., Biber K., Vinet J., Boddeke H.W. Microglia phenotype diversity. CNS Neurol. Disord. Drug Targets 2011, 10:108-118.
123. Olson A.K., Eadie B.D., Ernst C., Christie B.R. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 2006, 16:250-260.
124. Park H.R., Lee J. Neurogenic contributions made by dietary regulation to hippocampal neurogenesis. Ann. N. Y. Acad. Sci. 2011, 1229:23-28.
125. Parker R.M.C., Herzog H. Regional distribution of Y-receptor subtype mRNAs in rat brain. Eur. J. Neurosci. 1999, 11:1431-1448.
126. Perry V.H., Nicoll J.A.R., Holmes C. Microglia in neurodegenerative disease. Nat. Rev. Neurol. 2010, 6:193-201.
127. Persidsky Y., Ramirez S., Haorah J., Kanmogne G. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J. Neuroimm. Pharmacol. 2006, 1:223-236.
128. Platel J.C., Gordon V., Heintz T., Bordey A. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 2009, 57:66-78.
129. Plumpe T., Ehninger D., Steiner B., Klempin F., Jessberger S., Brandt M., Romer B., Rodriguez G.R., Kronenberg G., Kempermann G. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 2006, 7:77.
130. 2+ entry. J. Neurosci. 1997, 17:8169-8177.
131. Quinones-Hinojosa A., Sanai N., Soriano-Navarro M., Gonzalez-Perez O., Mirzadeh Z., Gil-Perotin S., Romero-Rodriguez R., Berger M.S., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 2006, 494:415-434.
132. Reitz C., Brayne C., Mayeux R. Epidemiology of Alzheimer disease. Nat. Rev. Neurol. 2011, 7:137-152.
133. Rivest S. Molecular insights on the cerebral innate immune system. Brain Behav. Immun. 2003, 17:13-19.
134. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 2002, 22:2679-2689.
135. Rodrigo C., Zaben M., Lawrence T., Laskowski A., Howell O.W., Gray W.P. NPY augments the proliferative effect of FGF2 and increases the expression of FGFR1 on nestin positive postnatal hippocampal precursor cells, via the Y1 receptor. J. Neurochem. 2010, 113:615-627.
136. Rose J.B., Crews L., Rockenstein E., Adame A., Mante M., Hersh L.B., Gage F.H., Spencer B., Potkar R., Marr R.A., Masliah E. Neuropeptide Y fragments derived from neprilysin processing are neuroprotective in a transgenic model of Alzheimer's disease. J. Neurosci. 2009, 29:1115-1125.
137. Russo I., Barlati S., Bosetti F. Effects of neuroinflammation on the regenerative capacity of brain stem cells. J Neurochem. 2011, 116:947-956.
138. Saijo K., Glass C.K. Microglial cell origin and phenotypes in health and disease. Nat. Rev. Immunol. 2011, 11:775-787.
139. Salero E., Blenkinsop T.A., Corneo B., Harris A., Rabin D., Stern J.H., Temple S. Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives. Cell Stem Cell 2012, 10:88-95.
140. Scaffidi P., Misteli T., Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195.
141. Scharfman H.E., Gray W.P. Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its relevance to seizure-induced neurogenesis. Exs. 2006, 95:193-211.
142. Schoenfeld T.J., Gould E. Stress, stress hormones, and adult neurogenesis. Exp. Neurol. 2011, 233:12-21.
143. Schwarz H., Villiger P.M., von Kempis J., Lotz M. Neuropeptide Y is Na inducible gene in the human immune system. J. Neuroimmunol. 1994, 51:53-61.
144. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300.
145. Sierra A., Gottfried-Blackmore A.C., McEwen B.S., Bulloch K. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 2007, 55:412-424.
146. Silva A.P., Carvalho A.P., Carvalho C.M., Malva J.O. Modulation of intracellular calcium changes and glutamate release by neuropeptide Y1 and Y2 receptors in the rat hippocampus: differential effects in CA1, CA3 and dentate gyrus. J. Neurochem. 2001, 79:286-296.
147. Silva A.P., Cavadas C., Grouzmann E. Neuropeptide Y and its receptors as potential therapeutic drug targets. Clin. Chim. Acta 2002, 326:3-25.
148. Silva A.P., Carvalho A.P., Carvalho C.M., Malva J.O. Functional interaction between neuropeptide Y receptors and modulation of calcium channels in the rat hippocampus. Neuropharmacology 2003, 44:282-292.
149. Silva A.P., Pinheiro P.S., Carvalho A.P., Carvalho C.M., Jakobsen B., Zimmer J., Malva J.O. Activation of neuropeptide Y receptors is neuroprotective against excitotoxicity in organotypic hippocampal slice cultures. FASEB J. 2003, 17:1118-1120.
150. Silva A.P., Xapelli S., Grouzmann E., Cavadas C. The putative neuroprotective role of neuropeptide Y in the central nervous system. Curr. Drug. Targets CNS Neurol. Disord. 2005, 4:331-347.
151. Smialowska M., Wieronska J.M., Szewczyk B. Neuroprotective effect of NPY on kainate neurotoxicity in the hippocampus. Pol. J. Pharmacol. 2003, 55:979-986.
152. Smialowska M., Domin H., Zieba B., Kozniewska E., Michalik R., Piotrowski P., Kajta M. Neuroprotective effects of neuropeptide Y-Y2 and Y5 receptor agonists in vitro and in vivo. Neuropeptides 2009, 43:235-249.
153. Sorensen G., Woldbye D.P. Mice lacking neuropeptide Y show increased sensitivity to cocaine. Synapse 2012, 66:840-843.
154. Sorensen G., Jensen M., Weikop P., Dencker D., Christiansen S.H., Loland C.J., Begtsen C.H., Petersen J.H., Fink-Jensen A., Wortwein G., Woldbye D.P. Neuropeptide Y Y5 receptor antagonism attenuates cocaine-induced effects in mice. Psychopharmacology (Berl) 2012, 222:565-577.
155. Stanic D., Paratcha G., Ledda F., Herzog H., Kopin A.S., Hokfelt T. Peptidergic influences on proliferation, migration, and placement of neural progenitors in the adult mouse forebrain. Proc. Nat. Acad. Sci. U. S. A. 2008, 105:3610-3615.
156. Streit W.J., Walter S.A., Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 1999, 57:563-581.
157. 2+ channels in acutely isolated neurons from the rat arcuate nucleus. J. Neurophysiol. 1999, 81:1391-1403.
158. Swanson R.A., Duan S. Regulation of glutamate transporter function. Neuroscientist 1999, 5:280-282.
159. Szeto H.H. Mitochondria-targeted peptide antioxidants: novel neuroprotective agents. AAPS J. 2006, 8:E521-E531.
160. Tatemoto K., Cariquist M., Mutt V. Neuropeptide Y - a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 1982, 296:659-660.
161. Thiriet N., Deng X., Solinas M., Ladenheim B., Curtis W., Goldberg S.R., Palmiter R.D., Cadet J.L. Neuropeptide Y protects against methamphetamine-induced neuronal apoptosis in the mouse striatum. J. Neurosci. 2005, 25:5273-5279.
162. Thiriet N., Agasse F., Nicoleau C., Guegan C., Vallette F., Cadet J.L., Jaber M., Malva J.O., Coronas V. NPY promotes chemokinesis and neurogenesis in the rat subventricular zone. J. Neurochem. 2011, 116:1018-1027.
163. Tropepe V., Coles B.L., Chiasson B.J., Horsford D.J., Elia A.J., McInnes R.R., van der Kooy D. Retinal stem cells in the adult mammalian eye. Science 2000, 287:2032-2036.
164. Turrin N., Rivest S. Molecular and cellular immune mediators of neuroprotection. Mol. Neurobiol. 2006, 34:221-242.
165. Valero J., Weruaga E., Murias A.R., Recio J.S., Curto G.G., Gomez C., Alonso J.R. Changes in cell migration and survival in the olfactory bulb of the pcd/pcd mouse. Dev. Neurobiol. 2007, 67:839-859.
166. Valero J., Eiriz M.F., Santos T., Neiva I., Ferreira R., Malva J.O. Microglia: the bodyguard and the hunter of the adult neurogenic niche. Advances in Stem Cell Research 2012, 245-279. Humana Press. H. Baharvand, N. Aghdami (Eds.).
167. Vezzani A., Sperk G. Overexpression of NPY and Y2 receptors in epileptic brain tissue: an endogenous neuroprotective mechanism in temporal lobe epilepsy?. Neuropeptides 2004, 38:245-252.
168. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7:31-40.
169. Wang Q., Yu S., Simonyi A., Sun G.Y., Sun A.Y. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 2005, 31:3-16.
170. Wee Yong V. Inflammation in neurological disorders: a help or a hindrance?. Neuroscientist 2010, 16:408-420.
171. Westwood S.C., Hanson G.R. Effects of stimulants of abuse on extrapyramidal and limbic neuropeptide Y systems. J. Pharmacol. Exp. Ther. 1999, 288:1160-1166.
172. Wheway J., Herzog H., Mackay F. The Y1 receptor for NPY: a key modulator of the adaptive immune system. Peptides 2007, 28:453-458.
173. Whitman M.C., Fan W., Rela L., Rodriguez-Gil D.J., Greer C.A. Blood vessels form a migratory scaffold in the rostral migratory stream. J. Comp. Neurol. 2009, 516:94-104.
174. Whitney N.P., Eidem T.M., Peng H., Huang Y., Zheng J.C. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J. Neurochem. 2009, 108:1343-1359.
175. Woldbye D.P., Kokaia M. Neuropeptide Y and seizures: effects of exogenously applied ligands. Neuropeptides 2004, 38:253-260.
176. Wu Y.F., Li S.B. Neuropeptide Y expression in mouse hippocampus and its role in neuronal excitotoxicity. Acta Pharmacol. Sin. 2005, 26:63-68.
177. Xapelli S., Agasse F., Ferreira R., Silva A.P., Malva J.O. Neuropeptide Y as an endogenous antiepileptic, neuroprotective and proneurogenic peptide. Recent Pat. CNS Drug Discov. 2006, 1:315-324.
178. Xapelli S., Silva A.P., Ferreira R., Malva J.O. Neuropeptide Y can rescue neurons from cell death following the application of an excitotoxic insult with kainate in rat organotypic hippocampal slice cultures. Peptides 2007, 28:288-294.
179. Xapelli S., Bernardino L., Ferreira R., Grade S., Silva A.P., Salgado J.R., Cavadas C., Grouzmann E., Poulsen F.R., Jakobsen B., Oliveira C.R., Zimmer J., Malva J.O. Interaction between neuropeptide Y (NPY) and brain-derived neurotrophic factor in NPY-mediated neuroprotection against excitotoxicity: a role for microglia. Eur. J. Neurosci. 2008, 27:2089-2102.
180. Yamamoto B.K., Raudensky J. The role of oxidative stress, metabolic compromise, and inflammation in neuronal injury produced by amphetamine-related drugs of abuse. J. Neuroimm. Pharmacol. 2008, 3:203-217.
181. Ye S.M., Johnson R.W. An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 2001, 9:183-192.
182. Yoneyama M., Shiba T., Hasebe S., Ogita K. Adult neurogenesis is regulated by endogenous factors produced during neurodegeneration. J. Pharmacol. Sci. 2011, 115:425-432.
183. Yoshihara T., Honma S., Mitome M., Honma K. Methamphetamine stimulates the release of neuropeptide Y and noradrenaline from the paraventricular nucleus in rats. Brain Res. 1996, 707:119-121.
184. Zhang H., Wang F.W., Yao L.L., Hao A.J. Microglia - friend or foe. Front. Biosci. (Schol. Ed.) 2011, 3:869-883.
185. Zhao C., Teng E.M., Summers R.G., Ming G.L., Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus I. J. Neurosci. 2006, 26:3-11.