Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus

Neurobiology of Disease

Volumn 26, Issue 1, 2007, Pages 174-188

  Howell, Owain W ^a   Silva, Sharmalene ^a   Scharfman, Helen E ^b   Sosunov, Alexander A ^c   Zaben, Malik ^a   Shatya, Anan ^a   Mckhann II, Guy ^c   Herzog, Herbert ^d   Laskowski, Alexandra ^a   Gray, William P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b HELEN HAYES HOSPITAL   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Cell culture; Dentate gyrus; Epilepsy; Nestin; Neurogenesis; NPY; Progenitor cell; Stem cell; Subcallosal zone; Subventricular zone

Indexed keywords

NESTIN; NEUROPEPTIDE Y; NEUROPEPTIDE Y1 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; HIPPOCAMPUS; MOUSE; NERVE CELL; NEUROENDOCRINOLOGY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; ANTIMETABOLITES; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT PROTEINS; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDE Y; RATS; RATS, WISTAR; SEIZURES; STEM CELLS; TUBULIN;

EID: 33947375670     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.12.014     Document Type: Article

References (62)

1. Altman J., and Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124 (1965) 319-335
2. Baraban S.C., Hollopeter G., Erickson J.C., Schwartzkroin P.A., and Palmiter R.D. Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J. Neurosci. 17 (1997) 8927-8936
3. Battista D., Ferrari C.C., Gage F.H., and Pitossi F.J. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur. J. Neurosci. 23 (2006) 83-93
4. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., and Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10432-10437
5. Capela A., and Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35 (2002) 865-875
6. D'Sa C., and Duman R.S. Antidepressants and neuroplasticity. Bipolar Disord. 4 (2002) 183-194
7. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 (1999) 703-716
8. El Bahh B., Auvergne R., Lere C., Brana C., Le Gal La Salle G., and Rougier A. Decreased epileptic susceptibility correlates with neuropeptide Y overexpression in a model of tolerance to excitotoxicity. Brain Res. 894 (2001) 209-217
9. Encinas J.M., Vaahtokari A., and Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 8233-8238
10. Erickson J.C., Clegg K.E., and Palmiter R.D. Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381 (1996) 415-421
11. Filippov V., Kronenberg G., Pivneva T., Reuter K., Steiner B., Wang L.P., Yamaguchi M., Kettenmann H., and Kempermann G. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol. Cell. Neurosci. 23 (2003) 373-382
12. Fukuda S., Kato F., Tozuka Y., Yamaguchi M., Miyamoto Y., and Hisatsune T. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23 (2003) 9357-9366
13. Gates M.A., Thomas L.B., Howard E.M., Laywell E.D., Sajin B., Faissner A., Gotz B., Silver J., and Steindler D.A. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 361 (1995) 249-266
14. Gray W.P., and Sundstrom L.E. Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res. 790 (1998) 52-59
15. Gross C.G. Neurogenesis in the adult brain: death of a dogma. Nat. Rev., Neurosci. 1 (2000) 67-73
16. Hagihara H., Hara M., Tsunekawa K., Nakagawa Y., Sawada M., and Nakano K. Tonic-clonic seizures induce division of neuronal progenitor cells with concomitant changes in expression of neurotrophic factors in the brain of pilocarpine-treated mice. Brain Res. Mol. Brain Res. 139 (2005) 258-266
17. Hansel D.E., Eipper B.A., and Ronnett G.V. Neuropeptide Y functions as a neuroproliferative factor. Nature 410 (2001) 940-944
18. Hansel D.E., Eipper B.A., and Ronnett G.V. Regulation of olfactory neurogenesis by amidated neuropeptides. J. Neurosci. Res. 66 (2001) 1-7
19. Howell O.W., Scharfman H.E., Herzog H., Sundstrom L.E., Beck-Sickinger A., and Gray W.P. Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 86 (2003) 646-659
20. Howell O.W., Doyle K., Goodman J.H., Scharfman H.E., Herzog H., Pringle A., Beck-Sickinger A.G., and Gray W.P. Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem. 93 (2005) 560-570
21. Huttmann K., Sadgrove M., Wallraff A., Hinterkeuser S., Kirchhoff F., Steinhauser C., and Gray W.P. Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur. J. Neurosci. 18 (2003) 2769-2778
22. Imura T., Nakano I., Kornblum H.I., and Sofroniew M.V. Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 53 (2006) 277-293
23. Jessberger S., Romer B., Babu H., and Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp. Neurol. 196 (2005) 342-351
24. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
25. 1 receptor knock-out mice. Focus on immunohistochemical localization(1). Neuroscience 111 (2002) 443-532
26. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., and Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467 (2003) 455-463
27. Lee M.K., Rebhun L.I., and Frankfurter A. Posttranslational modification of class III beta-tubulin. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 7195-7199
28. Lois C., and Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 264 (1994) 1145-1148
29. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11 (1993) 173-189
30. Maekawa M., Takashima N., Arai Y., Nomura T., Inokuchi K., Yuasa S., and Osumi N. Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10 (2005) 1001-1014
31. Marksteiner J., Sperk G., and Maas D. Differential increases in brain levels of neuropeptide Y and vasoactive intestinal polypeptide after kainic acid-induced seizures in the rat. Naunyn-Schmiedeberg's Arch. Pharmacol. 339 (1989) 173-177
32. Mazarati A., Lu X., Kilk K., Langel U., Wasterlain C., and Bartfai T. Galanin Type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur. J. Neurosci. 19 (2004) 3235-3244
33. Menn B., Garcia-Verdugo J.M., Yaschine C., Gonzalez-Perez O., Rowitch D., and Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J. Neurosci. 26 (2006) 7907-7918
34. Mercer A., Ronnholm H., Holmberg J., Lundh H., Heidrich J., Zachrisson O., Ossoinak A., Frisen J., and Patrone C. PACAP promotes neural stem cell proliferation in adult mouse brain. J. Neurosci. Res. 76 (2004) 205-215
35. Nakagawa E., Aimi Y., Yasuhara O., Tooyama I., Shimada M., McGeer P.L., and Kimura H. Enhancement of progenitor cell division in the dentate gyrus triggered by initial limbic seizures in rat models of epilepsy. Epilepsia 41 (2000) 10-18
36. Namba T., Mochizuki H., Onodera M., Mizuno Y., Namiki H., and Seki T. The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur. J. Neurosci. 22 (2005) 1928-1941
37. Navarro-Quiroga I., Hernandez-Valdes M., Lin S.L., and Naegele J.R. Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J. Comp. Neurol. 497 (2006) 833-845
38. Ohta S., Gregg C., and Weiss S. Pituitary adenylate cyclase-activating polypeptide regulates forebrain neural stem cells and neurogenesis in vitro and in vivo. J. Neurosci. Res. 84 (2006) 1177-1186
39. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
40. Parent J.M., Valentin V.V., and Lowenstein D.H. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J. Neurosci. 22 (2002) 3174-3188
41. Parent J.M., von dem Bussche N., and Lowenstein D.H. Prolonged seizures recruit caudal subventricular zone glial progenitors into the injured hippocampus. Hippocampus 16 (2006) 321-328
42. Peretto P., Giachino C., Aimar P., Fasolo A., and Bonfanti L. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J. Comp. Neurol. 487 (2005) 407-427
43. Pirttila T.J., Lukasiuk K., Hakansson K., Grubb A., Abrahamson M., and Pitkanen A. Cystatin C modulates neurodegeneration and neurogenesis following status epilepticus in mouse. Neurobiol. Dis. 20 (2005) 241-253
44. Pleasure S.J., Collins A.E., and Lowenstein D.H. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 20 (2000) 6095-6105
45. Radley J.J., and Jacobs B.L. Pilocarpine-induced status epilepticus increases cell proliferation in the dentate gyrus of adult rats via a 5-HT1A receptor-dependent mechanism. Brain Res. 966 (2003) 1-12
46. Rietze R., Poulin P., and Weiss S. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J. Comp. Neurol. 424 (2000) 397-408
47. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., and Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003) 805-809
48. Scharfman H.E., and Gray W.P. Plasticity of neuropeptide Y in the dentate gyrus after seizures, and its relevance to seizure-induced neurogenesis. Exs (2006) 193-211
49. Scott B.W., Wang S., Burnham W.M., De Boni U., and Wojtowicz J.M. Kindling-induced neurogenesis in the dentate gyrus of the rat. Neurosci. Lett. 248 (1998) 73-76
50. Seaberg R.M., and van der Kooy D. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22 (2002) 1784-1793
51. Seaberg R.M., Smukler S.R., and van der Kooy D. Intrinsic differences distinguish transiently neurogenic progenitors from neural stem cells in the early postnatal brain. Dev. Biol. 278 (2005) 71-85
52. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
53. Seri B., Garcia-Verdugo J.M., Collado-Morente L., McEwen B.S., and Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478 (2004) 359-378
54. Seri B., Herrera D.G., Gritti A., Ferron S., Collado L., Vescovi A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain. Cereb. Cortex 16 Suppl. 1 (2006) i103-i111
55. Shimoda Y., Tajima Y., Osanai T., Katsume A., Kohara M., Kudo T., Narimatsu H., Takashima N., Ishii Y., Nakamura S., Osumi N., and Sanai Y. Pax6 controls the expression of Lewis X epitope in the embryonic forebrain by regulating alpha 1,3-fucosyltransferase IX expression. J. Biol. Chem. 277 (2002) 2033-2039
56. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
57. Tramontin A.D., Garcia-Verdugo J.M., Lim D.A., and Alvarez-Buylla A. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb. Cortex 13 (2003) 580-587
58. Tropepe V., Coles B.L., Chiasson B.J., Horsford D.J., Elia A.J., McInnes R.R., and van der Kooy D. Retinal stem cells in the adult mammalian eye. Science 287 (2000) 2032-2036
59. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
60. Wei L.C., Shi M., Chen L.W., Cao R., Zhang P., and Chan Y.S. Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res. Dev. Brain Res. 139 (2002) 9-17
61. Yoshimura S., Takagi Y., Harada J., Teramoto T., Thomas S.S., Waeber C., Bakowska J.C., Breakefield X.O., and Moskowitz M.A. FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5874-5879
62. Zucchini S., Barbieri M., and Simonato M. Alterations in seizure susceptibility and in seizure-induced plasticity after pharmacologic and genetic manipulation of the fibroblast growth factor-2 system. Epilepsia 46 Suppl. 5 (2005) 52-58