Multiple signaling pathways mediate ghrelin-induced proliferation of hippocampal neural stem cells

Journal of Endocrinology

Volumn 218, Issue 1, 2013, Pages 49-59

  Chung, Hyunju ^a   Li, Endan ^b   Kim, Yumi ^b   Kim, Sehee ^b   Park, Seungjoon ^b  

^a Kyung Hee University College of Medicine   (South Korea)

^b Kyung Hee University Hospital   (South Korea)

Author keywords

Ghrelin; Hippocampus; Progenitor; Proliferation; Signaling pathways

Indexed keywords

GHRELIN; GHRELIN RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; JANUS KINASE 2; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; S6 KINASE; STAT3 PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; MOLECULAR MECHANICS; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

GHRELIN; HIPPOCAMPUS; PROGENITOR; PROLIFERATION; SIGNALING PATHWAYS;

ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ENZYME INHIBITORS; GHRELIN; HIPPOCAMPUS; HORMONE ANTAGONISTS; MAP KINASE SIGNALING SYSTEM; NEURAL STEM CELLS; NEUROGENESIS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, INBRED F344; RECEPTORS, GHRELIN; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84878799121     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0045     Document Type: Article

References (56)

1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J & Eriksson PS 2000 Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. Journal of Neuroscience 20 2896-2903.
2. Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, Elsworth JD, Roth RH, Sleeman MW, Picciotto MR, Tschop MH et al. 2006 Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. Journal of Clinical Investigation 116 3229-3239. (doi:10.1172/JCI29867)
3. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, Gotoh Y, Peltz G, Gong L, Kawase T, Alvarez-Buylla A et al. 2007 b-Catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25 2827-2836. (doi:10.1634/stemcells. 2007-0177)
4. Adams MM, Shi L, Linville MC, Forbes ME, Long AB, Bennett C, Newton IG, Carter CS, Sonntag WE, Riddle DR et al. 2008 Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Experimental Neurology 211 141-149. (doi:10.1016/j.expneurol. 2008.01.016)
5. Andrews ZB 2011 The extra-hypothalamic actions of ghrelin on neuronal function. Trends in Neurosciences 34 31-40. (doi:10.1016/j.tins.2010. 10.001)
6. Baldanzi G, Filigheddu N, Cutrupi S, Catapano F, Bonissoni S, Fubini A, Malan D, Baj G, Granata R, Broglio F et al. 2002 Ghrelin and des-acyl ghrelin inhibit cell death in cardiomyocytes and endothelial cells through ERK1/2 and PI 3-kinase/AKT. Journal of Cell Biology 159 1029-1037. (doi:10.1083/jcb.200207165)
7. Brewer GJ, Torricelli JR, Evege EK, Price PJ 1993 Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serumfree medium combination. Journal of Neuroscience Research 35 567-576. (doi:10.1002/jnr.490350513)
8. Butler CR & Zeman AZ 2008 Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment. Brain 131 2243-2263. (doi:10.1093/brain/awn127)
9. Carlini VP, Varas MM, Cragnolini AB, Schioth HB, Scimonelli TN & de Barioglio SR 2004Differential role of the hippocampus,amygdala, and dorsal raphe nucleus in regulating feeding, memory, and anxiety-like behavioral responses to ghrelin. Biochemical and Biophysical Research Communications 313 635-641. (doi:10.1016/j.bbrc.2003.11.150)
10. Chung H, Kim E, Lee DH, Seo S, Ju S, Lee D, Kim H & Park S 2007 Ghrelin inhibits apoptosis in hypothalamic neuronal cells during oxygenglucose deprivation. Endocrinology 148 148-159. (doi:10.1210/en. 2006-0991)
11. Chung H, Seo S, Moon M & Park S 2008 Phosphatidylinositol-3- kinase/Akt/glycogen synthase kinase-3b and ERK1/2 pathways mediate protective effects of acylated and unacylated ghrelin against oxygenglucose deprivation-induced apoptosis in primary rat cortical neuronal cells. Journal of Endocrinology 198 511-521. (doi:10.1677/JOE-08-0160)
12. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, Matsukura S, Kangawa K & Nakazato M 2000 Ghrelin, a novel growthhormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141 4255-4261. (doi:10.1210/en.141.11.4255)
13. Delhanty PJ, van der Eerden BC, van der Velde M, Gauna C, Pols HA, Jahr H, Chiba H, van der Lely AJ & van Leeuwen JP 2006 Ghrelin and unacylated ghrelin stimulate human osteoblast growth via mitogenactivated protein kinase (MAPK)/phosphoinositide 3-kinase (PI3K) pathways in the absence of GHS-R1a. Journal of Endocrinology 188 37-47. (doi:10.1677/joe.1.06404)
14. Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, Horvath B, Gaskin FS, Nonaka N, Jaeger LB, Banks WA et al. 2006 Ghrelin controls hippocampal spine synapse density and memory performance. Nature Neuroscience 9 381-388. (doi:10.1038/nn1656)
15. Fontan-Lozano A, Saez-Cassanelli JL, Inda MC, de los Santos-Arteaga M, Sierra-Dominguez SA, Lopez-Lluch G, Delgado-Garcia JM, Carrion AM 2007 Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. Journal of Neuroscience 27 10185-10195. (doi:10.1523/JNEUROSCI.2757-07.2007)
16. Garza JC, Guo M, Zhang W & Lu XY 2008 Leptin increases adult hippocampal neurogenesis in vivo and in vitro. Journal of Biological Chemistry 283 18238-18247. (doi:10.1074/jbc.M800053200)
17. Ghigo E, Broglio F, Arvat E, Maccario M, Papotti M & Muccioli G 2005 Ghrelin: more than a natural GH secretagogue and/or an orexigenic factor. Clinical Endocrinology 62 1-17. (doi:10.1111/j.1365-2265.2004. 02160.x)
18. Grote HE & Hannan AJ 2007 Regulators of adult neurogenesis in the healthy and diseased brain. Clinical and Experimental Pharmacology & Physiology 34 533-545. (doi:10.1111/j.1440-1681.2007.04610.x)
19. Gu F, Hata R, Ma YJ, Tanaka J, Mitsuda N, Kumon Y, Hanakawa Y, Hashimoto K, Nakajima K & Sakanaka M 2005 Suppression of Stat3 promotes neurogenesis in cultured neural stem cells. Journal of Neuroscience Research 81 163-171. (doi:10.1002/jnr.20561)
20. Guan XM, Yu H, Palyha OC, McKee KK, Feighner SD, Sirinathsinghji DJ, Smith RG, van der Ploeg LH & Howard AD 1997 Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Research Molecular Brain Research 48 23-29. (doi:10.1016/S0169-328X(97)00071-5)
21. Han J, Wang B, Xiao Z, Gao Y, Zhao Y, Zhang J, Chen B, Wang X & Dai J 2008 Mammalian target of rapamycin (mTOR) is involved in the neuronal differentiation of neural progenitors induced by insulin. Molecular and Cellular Neuroscience 39 118-124. (doi:10.1016/j.mcn. 2008.06.003)
22. Hao Y, Creson T, Zhang L, Li P, Du F, Yuan P, Gould TD, Manji HK & Chen G 2004 Mood stabilizer valproate promotes ERK pathwaydependent cortical neuronal growth and neurogenesis. Journal of Neuroscience 24 6590-6599. (doi:10.1523/JNEUROSCI.5747-03.2004)
23. Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, Rosenblum CI, Hamelin M, Hreniuk DL, Palyha OC, Anderson J et al. 1996 A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 273 974-977. (doi:10.1126/science.273.5277.974)
24. Hwang S,Moon M, Kim S, Hwang L, Ahn KJ, Park S 2009 Neuroprotective effect of ghrelin is associated with decreased expression of prostate apoptosis response-4. Endocrine Journal 56 609-617. (doi:10.1507/ endocrj.K09E-072)
25. Jiang H, Betancourt L & Smith RG 2006 Ghrelin amplifies dopamine signaling by cross talk involving formation of growth hormone secretagogue receptor/dopamine receptor subtype 1 heterodimers. Molecular Endocrinology 20 1772-1785. (doi:10.1210/me.2005-0084)
26. Jiang H, Li LJ, Wang J & Xie JX 2008 Ghrelin antagonizes MPTP-induced neurotoxicity to the dopaminergic neurons in mouse substantia nigra. Experimental Neurology 212 532-537. (doi:10.1016/j.expneurol.2008. 05.006)
27. Johansson I, Destefanis S, Aberg ND, Aberg MA, Blomgren K, Zhu C, Ghe C, Granata R, Ghigo E, Muccioli G et al. 2008 Proliferative and protective effects of growth hormone secretagogues on adult rat hippocampal progenitor cells. Endocrinology 149 2191-2199. (doi:10.1210/en. 2007-0733)
28. Kojima M, Kangawa K 2005 Ghrelin: structure and function. Physiological Reviews 85 495-522. (doi:10.1152/physrev.00012.2004)
29. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H & Kangawa K 1999 Ghrelin is a growth hormone-releasing acylated peptide from stomach. Nature 402 656-660. (doi:10.1038/45230)
30. Learish RD, Bruss MD & Haak-Frendscho M 2000 Inhibition of mitogenactivated protein kinase kinase blocks proliferation of neural progenitor cells. Brain Research Developmental Brain Research 122 97-109. (doi:10.1016/S0165-3806(00)00064-X)
31. Lee J, Seroogy KB & Mattson MP 2002 Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. Journal of Neurochemistry 80 539-547. (doi:10.1046/j.0022- 3042.2001.00747.x)
32. Lee J, Lim E, Kim Y, Li E & Park S 2010a Ghrelin attenuates kainic acidinduced neuronal cell death in the mouse hippocampus. Journal of Endocrinology 205 263-270. (doi:10.1677/JOE-10-0040)
33. Lee JY, Chung H, Yoo YS, Oh YJ, Oh TH, Park S & Yune TY 2010b Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 151 3815-3826. (doi:10.1210/en. 2009-1416)
34. Li L, Xu B, Zhu Y, Chen L, Sokabe M & Chen L 2010 DHEA prevents Ab25-35-impaired survival of newborn neurons in the dentate gyrus through a modulation of PI3K-Akt-mTOR signaling. Neuropharmacology 59 323-333. (doi:10.1016/j.neuropharm.2010.02.009)
35. Li E, Chung H, Kim Y, Kim DH, Ryu JH, Sato T, Kojima M & Park S 2013 Ghrelin directly stimulates adult hippocampal neurogenesis: implications for learning and memory. Endocrine Journal. In press (doi:10.1507/endocrj.EJ13-0008)
36. Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky SA, Anderson JG, Jung S, Birnbaum S, Yanagisawa M, Elmquist JK, Nestler EJ et al. 2008 The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nature Neuroscience 11 752-753. (doi:10.1038/nn.2139)
37. Miao Y, Xia Q, Hou Z, Zheng Y, Pan H, Zhu S 2007 Ghrelin protects cortical neuron against focal ischemia/reperfusion in rats. Biochemical and Biophysical Research Communications 359 795-800. (doi:10.1016/ j.bbrc.2007.05.192)
38. Ming GL & Song H 2005 Adult neurogenesis in the mammalian central nervous system. Annual Review of Neuroscience 28 223-250. (doi:10.1146/annurev.neuro.28.051804.101459)
39. Moon M, Kim HG, Hwang L, Seo JH, Kim S, Hwang S, Kim S, Lee D, Chung H, Oh MS et al. 2009a Neuroprotective effect of ghrelin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease by blocking microglial activation. Neurotoxicity Research 15 332-347. (doi:10.1007/s12640-009-9037-x)
40. Moon M, Kim S, Hwang L, Park S 2009b Ghrelin regulates hippocampal neurogenesis in adultmice. Endocrine Journal 56 525-531. (doi:10.1507/ endocrj.K09E-089)
41. Naleid AM, Grace MK, Cummings DE & Levine AS 2005 Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides 26 2274-2279. (doi:10.1016/j.peptides.2005.04.025)
42. Nogueiras R, Tovar S, Mitchell SE, Rayner DV, Archer ZA, Dieguez C & Williams LM 2004 Regulation of growth hormone secretagogue receptor gene expression in the arcuate nuclei of the rat by leptin and ghrelin. Diabetes 53 2552-2558. (doi:10.2337/diabetes.53.10.2552)
43. Park YJ, Lee YJ, Kim SH, Joung DS, Kim BJ, So I, Park DJ & Cho BY 2008 Ghrelin enhances the proliferating effect of thyroid stimulating hormone in FRTL-5 thyroid cells. Molecular and Cellular Endocrinology 285 19-25. (doi:10.1016/j.mce.2008.01.003)
44. Peltier J, O'Neill A & Schaffer DV 2007 PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Developmental Neurobiology 67 1348-1361. (doi:10.1002/dneu.20506)
45. Ryu JK, Choi HB, Hatori K, Heisel RL, Pelech SL, McLarnon JG & Kim SU 2003 Adenosine triphosphate induces proliferation of human neuralstem cells: role of calcium and p70 ribosomal protein S6 kinase. Journal of Neuroscience Research 72 352-362. (doi:10.1002/jnr.10507)
46. Sato M, Nakahara K, Goto S, Kaiya H, Miyazato M, Date Y, Nakazato M, Kangawa K &MurakamiN 2006 Effects of ghrelin and des-acyl ghrelin on neurogenesis of the rat fetal spinal cord. Biochemical and Biophysical Research Communications 350 598-603. (doi:10.1016/j.bbrc.2006.09.088)
47. Song G, Ouyang G & Bao S 2005 The activation of Akt/PKB signaling pathway and cell survival. Journal of Cellular and Molecular Medicine 9 59-71. (doi:10.1111/j.1582-4934.2005.tb00337.x)
48. Squire LR & Zola SM 1996 Ischemic brain damage and memory impairment: a commentary. Hippocampus 6 546-552. (doi:10.1002/ (SICI)1098-1063(1996)6:5!546::AID-HIPO7O3.0.CO;2-G)
49. Thielemans L, Peeters PJ, Jonckheere H, Luyten W, de Hooqt R, Coulie B & Aerssens J 2007 The hepatocarcinoma cell line HepG2 does not express a GHS-R1a-type ghrelin receptor. Journal of Receptor and Signal Transduction Research 27 309-322. (doi:10.1080/10799890701519587)
50. Van der Lely AJ, Tschop M, Heiman ML & Ghigo E 2004 Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocrine Reviews 25 426-457. (doi:10.1210/er.2002-0029)
51. Weeber EJ & Sweatt JD 2002 Molecular neurobiology of human cognition. Neuron 33 845-848. (doi:10.1016/S0896-6273(02)00634-7)
52. Yoshimatsu T, Kawaguchi D, Oishi K, Takeda K, Akira S, Masuyama N & Gotoh Y 2006 Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133 2553-2563. (doi:10.1242/dev.02419)
53. Zhang W, Lin TR, Hu Y, Fan Y, Zhao L, Stuenkel EL & MulhollandMW2004 Ghrelin stimulates neurogenesis in the dorsal motor nucleus of the vagus. Journal of Physiology 559 729-737. (doi:10.1113/jphysiol.2004. 064121)
54. Zhang W, Hu Y, Lin TR, Fan Y & Mulholland MW 2005 Stimulation of neurogenesis in rat nucleus of the solitary tract by ghrelin. Peptides 26 2280-2288. (doi:10.1016/j.peptides.2005.04.023)
55. Zhao C, DengW& Gage FH 2008 Mechanisms and functional implications of adult neurogenesis. Cell 132 645-660. (doi:10.1016/j.cell.2008. 01.033)
56. Zhou L, Del Villar K, Dong Z, Miller CA 2004 Neurogenesis response to hypoxia-inducedcell death:map kinase signal transductionmechanisms. Brain Research 1021 8-19. (doi:10.1016/j.brainres.2004.05.115