Ghrelin administration enhances neurogenesis but impairs spatial learning and memory in adult mice

Neuroscience

Volumn 257, Issue , 2014, Pages 175-185

  Zhao, Z ^a,b   Liu, H ^a,c   Xiao, K ^a   Yu, M ^a   Cui, L ^a   Zhu, Q ^a   Zhao, R ^b   Li, G D ^d   Zhou, Y ^a  

^a QINGDAO UNIVERSITY MEDICAL COLLEGE   (China)

^b Affiliated Hospital of Medical College   (China)

^c BINZHOU MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adult neurogenesis; Ghrelin; Hippocampus; Learning; Memory circuits

Indexed keywords

GHRELIN; PROTEIN C FOS;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LEARNING DISORDER; MALE; MEMORY; MEMORY DISORDER; MOUSE; NERVE TRACT; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPATIAL LEARNING;

5-BROMO-2′ DEOXYURIDIEN; ADULT NEUROGENESIS; BRDU; DENTATE GYRUS; DG; GHRELIN; HIPPOCAMPUS; LEARNING; MEMORY CIRCUITS; PARAFORMALDEHYDE; PFA; SGZ; SUBGRANULAR ZONE; TARGET QUADRANT; TQ;

ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; EXPLORATORY BEHAVIOR; GHRELIN; HIPPOCAMPUS; LEARNING; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROPEPTIDES; ONCOGENE PROTEINS V-FOS; PHOSPHOPYRUVATE HYDRATASE; TIME FACTORS;

EID: 84890131140     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.10.063     Document Type: Article

References (64)

1. Albarran-Zeckler R.G., Brantley A.F., Smith R.G. Growth hormone secretagogue receptor (GHS-R1a) knockout mice exhibit improved spatial memory and deficits in contextual memory. Behav Brain Res 2012, 232:13-19.
2. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 1965, 124:319-335.
3. Andrews Z.B., Erion D., Beiler R., Liu Z.W., Abizaid A., Zigman J., Elsworth J.D., Savitt J.M., DiMarchi R., Tschoep M., Roth R.H., Gao X.B., Horvath T.L. Ghrelin promotes and protects nigrostriatal dopamine function via a UCP2-dependent mitochondrial mechanism. J Neurosci 2009, 29:14057-14065.
4. Bruel-Jungerman E., Laroche S., Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 2005, 21:513-521.
5. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001, 435:406-417.
6. Carlini V.P., Ghersi M., Schioth H.B., de Barioglio S.R. Ghrelin and memory: differential effects on acquisition and retrieval. Peptides 2010, 31:1190-1193.
7. Carlini V.P., Martini A.C., Schioth H.B., Ruiz R.D., Fiol de Cuneo M., De Barioglio S.R. Decreased memory for novel object recognition in chronically food-restricted mice is reversed by acute ghrelin administration. Neuroscience 2008, 153:929-934.
8. Carlini V.P., Monzon M.E., Varas M.M., Cragnolini A.B., Schioth H.B., Scimonelli T.N., de Barioglio S.R. Ghrelin increases anxiety-like behavior and memory retention in rats. Biochem Biophys Res Commun 2002, 299:739-743.
9. Carlini V.P., Varas M.M., Cragnolini A.B., Schioth H.B., Scimonelli T.N., de Barioglio S.R. Differential role of the hippocampus, amygdala, and dorsal raphe nucleus in regulating feeding, memory, and anxiety-like behavioral responses to ghrelin. Biochem Biophys Res Commun 2004, 313:635-641.
10. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
11. Carvajal P., Carlini V.P., Schioth H.B., de Barioglio S.R., Salvatierra N.A. Central ghrelin increases anxiety in the open field test and impairs retention memory in a passive avoidance task in neonatal chicks. Neurobiol Learn Mem 2009, 91:402-407.
12. Chung H., Kim E., Lee D.H., Seo S., Ju S., Lee D., Kim H., Park S. Ghrelin inhibits apoptosis in hypothalamic neuronal cells during oxygen-glucose deprivation. Endocrinology 2007, 148:148-159.
13. Clark R.E., Broadbent N.J., Squire L.R. Hippocampus and remote spatial memory in rats. Hippocampus 2005, 15:260-272.
14. Davis J.F., Choi D.L., Clegg D.J., Benoit S.C. Signaling through the ghrelin receptor modulates hippocampal function and meal anticipation in mice. Physiol Behav 2011, 103:39-43.
15. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
16. Deng W., Saxe M.D., Gallina I.S., Gage F.H. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 2009, 29:13532-13542.
17. Diano S., Farr S.A., Benoit S.C., McNay E.C., da Silva I., Horvath B., Gaskin F.S., Nonaka N., Jaeger L.B., Banks W.A., Morley J.E., Pinto S., Sherwin R.S., Xu L., Yamada K.A., Sleeman M.W., Tschop M.H., Horvath T.L. Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 2006, 9:381-388.
18. Dresler M., Kluge M., Genzel L., Schussler P., Steiger A. Nocturnal administration of ghrelin does not promote memory consolidation. Pharmacopsychiatry 2010, 43:277-278.
19. Dupret D., Revest J.M., Koehl M., Ichas F., De Giorgi F., Costet P., Abrous D.N., Piazza P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 2008, 3:e1959.
20. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat Med 1998, 4:1313-1317.
21. Esposito M.S., Piatti V.C., Laplagne D.A., Morgenstern N.A., Ferrari C.C., Pitossi F.J., Schinder A.F. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005, 25:10074-10086.
22. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
23. Ge S., Goh E.L., Sailor K.A., Kitabatake Y., Ming G.L., Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439:589-593.
24. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999, 2:260-265.
25. Gu Y., Arruda-Carvalho M., Wang J., Janoschka S.R., Josselyn S.A., Frankland P.W., Ge S. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 2012, 15:1700-1706.
26. Hansson C., Haage D., Taube M., Egecioglu E., Salome N., Dickson S.L. Central administration of ghrelin alters emotional responses in rats: behavioural, electrophysiological and molecular evidence. Neuroscience 2011, 180:201-211.
27. Harms L.R., Eyles D.W., McGrath J.J., Mackay-Sim A., Burne T.H. Developmental vitamin D deficiency alters adult behaviour in 129/SvJ and C57BL/6J mice. Behav Brain Res 2008, 187:343-350.
28. Howard A.D., Feighner S.D., Cully D.F., Arena J.P., Liberator P.A., Rosenblum C.I., Hamelin M., Hreniuk D.L., Palyha O.C., Anderson J., Paress P.S., Diaz C., Chou M., Liu K.K., McKee K.K., Pong S.S., Chaung L.Y., Elbrecht A., Dashkevicz M., Heavens R., Rigby M., Sirinathsinghji D.J., Dean D.C., Melillo D.G., Patchett A.A., Nargund R., Griffin P.R., DeMartino J.A., Gupta S.K., Schaeffer J.M., Smith R.G., Van der Ploeg L.H. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 1996, 273:974-977.
29. Jessberger S., Clark R.E., Broadbent N.J., Clemenson G.D., Consiglio A., Lie D.C., Squire L.R., Gage F.H. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 2009, 16:147-154.
30. Karl C., Couillard-Despres S., Prang P., Munding M., Kilb W., Brigadski T., Plotz S., Mages W., Luhmann H., Winkler J., Bogdahn U., Aigner L. Neuronal precursor-specific activity of a human doublecortin regulatory sequence. J Neurochem 2005, 92:264-282.
31. Kee N., Teixeira C.M., Wang A.H., Frankland P.W. Imaging activation of adult-generated granule cells in spatial memory. Nat Protoc 2007, 2:3033-3044.
32. 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.
33. Kempermann G., Gage F.H. Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 1999, 9:321-332.
34. Kempermann G., Gage F.H. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 2002, 16:129-136.
35. Koehl M., Abrous D.N. A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 2011, 33:1101-1114.
36. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660.
37. Li E., Chung H., Kim Y., Kim D.H., Ryu J.H., Sato T., Kojima M., Park S. Ghrelin directly stimulates adult hippocampal neurogenesis: implications for learning and memory. Endocr J 2013, 60:781-789.
38. Ming G.L., Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005, 28:223-250.
39. Mitchell V., Bouret S., Beauvillain J.C., Schilling A., Perret M., Kordon C., Epelbaum J. Comparative distribution of mRNA encoding the growth hormone secretagogue-receptor (GHS-R) in microcebus murinus (Primate, lemurian) and rat forebrain and pituitary. J Comp Neurol 2001, 429:469-489.
40. Moon M., Kim S., Hwang L., Park S. Ghrelin regulates hippocampal neurogenesis in adult mice. Endocr J 2009, 56:525-531.
41. Mu Y., Lee S.W., Gage F.H. Signaling in adult neurogenesis. Curr Opin Neurobiol 2010, 20:416-423.
42. Palasz A., Krzystanek M., Worthington J., Czajkowska B., Kostro K., Wiaderkiewicz R., Bajor G. Nesfatin-1, a unique regulatory neuropeptide of the brain. Neuropeptides 2012, 46:105-112.
43. Sato M., Nakahara K., Goto S., Kaiya H., Miyazato M., Date Y., Nakazato M., Kangawa K., Murakami N. Effects of ghrelin and des-acyl ghrelin on neurogenesis of the rat fetal spinal cord. Biochem Biophys Res Commun 2006, 350:598-603.
44. Sato T., Fukue Y., Teranishi H., Yoshida Y., Kojima M. Molecular forms of hypothalamic ghrelin and its regulation by fasting and 2-deoxy-d-glucose administration. Endocrinology 2005, 146:2510-2516.
45. Shi L., Bian X., Qu Z., Ma Z., Zhou Y., Wang K., Jiang H., Xie J. Peptide hormone ghrelin enhances neuronal excitability by inhibition of Kv7/KCNQ channels. Nat Commun 2013, 4:1435.
46. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
47. Snyder J.S., Hong N.S., McDonald R.J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
48. Song L., Zhu Q., Liu T., Yu M., Xiao K., Kong Q., Zhao R., Li G.D., Zhou Y. Ghrelin modulates lateral amygdala neuronal firing and blocks acquisition for conditioned taste aversion. PLoS One 2013, 8:e65422.
49. Spitznagel M.B., Benitez A., Updegraff J., Potter V., Alexander T., Glickman E., Gunstad J. Serum ghrelin is inversely associated with cognitive function in a sample of non-demented elderly. Psychiatry Clin Neurosci 2010, 64:608-611.
50. Tashiro A., Sandler V.M., Toni N., Zhao C., Gage F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 2006, 442:929-933.
51. Thuret S., Toni N., Aigner S., Yeo G.W., Gage F.H. Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 2009, 19:658-669.
52. Tschop M., Weyer C., Tataranni P.A., Devanarayan V., Ravussin E., Heiman M.L. Circulating ghrelin levels are decreased in human obesity. Diabetes 2001, 50:707-709.
53. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999, 96:13427-13431.
54. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 2002, 415:1030-1034.
55. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25:8680-8685.
56. Vukovic J., Borlikova G.G., Ruitenberg M.J., Robinson G.J., Sullivan R.K., Walker T.L., Bartlett P.F. Immature doublecortin-positive hippocampal neurons are important for learning but not for remembering. J Neurosci 2013, 33:6603-6613.
57. Wellman P.J., Hollas C.N., Elliott A.E. Systemic ghrelin sensitizes cocaine-induced hyperlocomotion in rats. Regul Pept 2008, 146:33-37.
58. Wojtowicz J.M., Kee N. BrdU assay for neurogenesis in rodents. Nat Protoc 2006, 1:1399-1405.
59. Zhang C.L., Zou Y., He W., Gage F.H., Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008, 451:1004-1007.
60. Zhang W., Hu Y., Lin T.R., Fan Y., Mulholland M.W. Stimulation of neurogenesis in rat nucleus of the solitary tract by ghrelin. Peptides 2005, 26:2280-2288.
61. Zhang W., Lin T.R., Hu Y., Fan Y., Zhao L., Stuenkel E.L., Mulholland M.W. Ghrelin stimulates neurogenesis in the dorsal motor nucleus of the vagus. J Physiol 2004, 559:729-737.
62. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.
63. 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. J Neurosci 2006, 26:3-11.
64. Zhou Y., Takahashi E., Li W., Halt A., Wiltgen B., Ehninger D., Li G.D., Hell J.W., Kennedy M.B., Silva A.J. Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 2007, 27:13843-13853.