Impaired hippocampal neurogenesis and its enhancement with ghrelin in 5XFADl

Journal of Alzheimer's Disease

Volumn 41, Issue 1, 2014, Pages 233-241

  Moon, Minho ^a   Cha, Moon Yong ^a   Mook Jung, Inhee ^a  

^a Seoul National University College of Medicine   (South Korea)

Author keywords

5XFAD mice; adult neurogenesis; Alzheimer's disease; amyloid plaque; ghrelin; hippocampus

Indexed keywords

ANTIBODY; CALRETININ; DOUBLECORTIN; GHRELIN; HISTONE H3; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; NEUROPROTECTIVE AGENT;

5XFAD MOUSE; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONGITUDINAL STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; ANIMAL; DENTATE GYRUS; DISEASE MODEL; DRUG EFFECTS; GENETICS; GLIOSIS; HUMAN; MALE; METABOLISM; MICROGLIA; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLAQUE, AMYLOID; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; GHRELIN; GLIOSIS; HIPPOCAMPUS; HUMANS; LONGITUDINAL STUDIES; MALE; MICE, TRANSGENIC; MICROGLIA; NEURAL STEM CELLS; NEUROGENESIS; NEUROPROTECTIVE AGENTS; PLAQUE, AMYLOID;

EID: 84902298760     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-132417     Document Type: Article

References (59)

1. Sakono M, Zako T (2010) Amyloid oligomers: Formation and toxicity of Abeta oligomers. FEBS J 277, 1348-1358.
2. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8, 79-84.
3. Mu Y, Gage FH (2011) Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol Neurodegener 6, 85.
4. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer's disease: At the crossroads. Exp Neurol 223, 267-281.
5. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28, 223-250.
6. Chuang TT (2010) Neurogenesis in mouse models of Alzheimer's disease. Biochim Biophys Acta 1802, 872-880.
7. Moon M, Hong HS, Nam DW, Baik SH, Song H, Kook SY, Kim YS, Lee J, Mook-Jung I (2012) Intracellular amyloid-beta accumulation in calcium-binding protein-deficient neurons leads to amyloid-beta plaque formation in animal model of Alzheimer's disease. J Alzheimers Dis 29, 615-628.
8. Kim KH, Moon M, Yu SB, Mook-Jung I, Kim JI (2012) RNA-Seq analysis of frontal cortex and cerebellum from 5XFAD mice at early stage of disease pathology. J Alzheimers Dis 29, 793-808.
9. Moon M, Song H, Hong HJ, Nam DW, Cha MY, Oh MS, Yu J, Hoon R, Mook-Jung I (2013) Vitamin D-binding protein interacts with Abeta and suppresses Abeta-mediated pathology. Cell Death Differ 20, 630-638.
10. Hong I, Kang T, Yoo Y, Park R, Lee J, Lee S, Kim J, Song B, Kim SY, Moon M, Yun KN, Kim JY, Mook-Jung I, Park YM, Choi S (2013) Quantitative proteomic analysis of the hippocampus in the 5XFAD mouse model at early stages of Alzheimer's disease pathology. J Alzheimers Dis36, 321-334.
11. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: Potential factors in amyloid plaque formation. J Neurosci 26, 10129-10140.
12. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O (2012) Motor deficits. Neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Abeta aggregation in the 5XFAD mouse model of Alzheimer's disease. Neurobiol Aging 33 196, e129-e140.
13. Schaeffer EL, Novaes BA, da Silva ER, Skaf HD, Mendes-Neto AG (2009) Strategies to promote differentiation of newborn neurons into mature functional cells in Alzheimer brain. Prog Neuropsychopharmacol Biol Psychiatry33, 1087-1102.
14. Moon M, Choi JG, Nam DW, Hong HS, Choi YJ, Oh MS, Mook-Jung I (2011) Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-beta1-42 oligomer-injected mice. J Alzheimers Dis 23, 147-159.
15. Sato M, Nakahara K, Goto S, Kaiya H, Miyazato M, Date Y, Nakazato M, Kangawa K, Murakami N (2006) Effects of ghrelin and des-acyl ghrelin on neurogenesis of the rat fetal spinal cord. Biochem Biophys Res Commun 350, 598-603.
16. 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.
17. Zhang W, Lin TR, Hu Y, Fan Y, Zhao L, Stuenkel EL, Mulholland MW (2004) Ghrelin stimulates neurogenesis in the dorsal motor nucleus of the vagus. J Physiol 559, 729-737.
18. Li E, Kim Y, Kim S, Sato T, Kojima M, Park S (2014) Ghre-lin stimulates proliferation, migration and differentiation of neural progenitors from the subventricular zone in the adult mice. Exp Neurol 252, 75-84.
19. Johansson I, Destefanis S, Aberg ND, Aberg MA, Blomgren K, Zhu C, Ghe C, Granata R, Ghigo E, Muccioli G, Eriksson PS, Isgaard J (2008) Proliferative and protective effects of growth hormone secretagogues on adult rat hippocampal progenitor cells. Endocrinology 149, 2191-2199.
20. Moon M, Kim S, Hwang L, Park S (2009) Ghrelin regulates hippocampal neurogenesis in adult mice. Endocr J 56, 525-531.
21. Barlind A, Karlsson N, Berg ND, Bjork-Eriksson T, Blom-gren K, Isgaard J (2010) The growth hormone secretagogue hexarelin increases cell proliferation in neurogenic regions of the mouse hippocampus. Growth Horm IGF Res 20, 49-54.
22. Andrews ZB (2011) The extra-hypothalamic actions of ghre-lin on neuronal function. Trends Neurosci 34, 31-40.
23. 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. Endocr J 60, 781-789.
24. Chung H, Li E, Kim Y, Kim S, Park S (2013) Multiple signaling pathways mediate ghrelin-induced proliferation of hippocampal neural stem cells. J Endocrinol 218, 49-59.
25. Li E, Kim Y, Kim S, Park S Ghrelin-induced hippocam-pal neurogenesis and enhancement of cognitive function are mediated independently of GH/IGF-1 axis: Lessons from the spontaneous dwarf rats. Endocr J 60, 1065-1075.
26. Beck B, Pourie G (2013) Ghrelin, neuropeptide Y, and other feeding-regulatory peptides active in the hippocampus: Role in learning and memory. Nutr Rev 71, 541-561.
27. Zhao Z, Liu H, Xiao K, Yu M, Zhu Q, Zhao R, Li GD, Zhou Y (2014) Ghrelin administration enhances neurogen-esis but impairs spatial learning and memory in adult mice. Neuroscience 257, 175-185.
28. 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 oxygen-glucose deprivation. Endocrinology 148, 148-159.
29. Moon M, Kim HG, Hwang L, Seo JH, Kim S, Hwang S, Lee D, Chung H, Oh MS, Lee KT, Park S (2009) 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. Neurotox Res 15, 332-347.
30. Xu J, Wang S, Lin Y, Cao L, Wang R, Chi Z (2009) Ghre-lin protects against cell death of hippocampal neurons in pilocarpine-induced seizures inrats. Neurosci Lett453, 58-61.
31. Hwang S, Moon M, Kim S, Hwang L, Ahn KJ, Park S (2009) Neuroprotective effect of ghrelin is associated with decreased expressionofprostate apoptosis response-4. Endocr J 56, 609-617.
32. Paxinos G, Franklin KBJ (2001) The mouse brain in stereo-taxic coordinates, Academic Press, San Diego.
33. Moon M, Huh Y, Park C (2006) L-nitroimidazole ornithine limits exercise-induced increases in cell proliferation in the hippocampus of adult mice. Neuroreport 17, 1121-1125.
34. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21, 1-14.
35. Rao MS, Shetty AK (2004) Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19, 234-246.
36. Rodriguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM, Oddo S, Verkhratsky A (2008) Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS One 3, e2935.
37. von Bohlen Und Halbach O (2007) Immunohistological markers for staging neurogenesis in adult hippocampus. Cell Tissue Res 329, 409-420.
38. Li B, Yamamori H, Tatebayashi Y, Shafit-Zagardo B, Tan-imukai H, Chen S, Iqbal K, Grundke-Iqbal I (2008) Failure of neuronal maturation in Alzheimer disease dentate gyrus. J Neuropathol Exp Neurol 67, 78-84.
39. Choi SH, Li Y (2011) Elevated levels of BMP6 impair neu-rogenesis in Alzheimer's disease. J Neurosci 31, 371-372.
40. Curtis MA, Kam M, Faull RL (2011) Neurogenesisinhumans. Eur J Neurosci 33, 1170-1174.
41. Mu Y, Gage FH (2011) Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol Neurodegener 6, 85.
42. Lopez-Toledano MA, Ali Faghihi M, Patel NS, Wahlestedt C (2010) Adult neurogenesis: A potential tool for early diagnosis in Alzheimer's disease? J Alzheimers Dis 20, 395-408.
43. Verret L, Jankowsky JL, Xu GM, Borchelt DR, Rampon C (2007) Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hip-pocampal neurogenesis. J Neurosci 27, 6771-6780.
44. Haughey NJ, Nath A, Chan SL, Borchard AC, Rao MS, Mattson MP (2002) Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell home-ostasis, in models of Alzheimer's disease. J Neurochem 83, 1509-1524.
45. Biscaro B, Lindvall O, Hock C, Ekdahl CT, Nitsch RM (2009) Abeta immunotherapy protects morphology and survival of adult-born neurons in doubly transgenic APP/PS1 mice. J Neurosci 29, 14108-14119.
46. Ohno M (2009) Failures to reconsolidate memory in a mouse modelof Alzheimer's disease. Neurobiol Learn Mem 92, 455-459.
47. Jagasia R, Song H, Gage FH, Lie DC (2006) New regulators in adult neurogenesis and their potential role for repair. Trends Mol Med 12, 400-405.
48. Theil MM, Miyake S, Mizuno M, Tomi C, Croxford JL, Hosoda H, Theil J, von Horsten S, Yokote H, Chiba A, Lin Y, Oki S, Akamizu T, Kangawa K, Yamamura T (2009) Suppression of experimental autoimmune encephalomyelitis by ghrelin. J Immunol 183, 2859-2866.
49. Lee JY, Chung H, Yoo YS, Oh YJ, Oh TH, Park S, Yune TY (2010) Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 151, 3815-3826.
50. Gahete MD, Cordoba-Chacon J, Kineman RD, Luque RM, Castano JP (2011) Role of ghrelin system in neuroprotection and cognitive functions: Implications in Alzheimer's disease. Peptides 32, 2225-2228.
51. Dos Santos VV, Rodrigues AL, De Lima TC, de Barioglio SR, Raisman-Vozari R, Prediger RD (2013) Ghrelin as a neuro-protective and palliative agent in Alzheimer's and Parkinson's disease. Curr Pharm Des 19, 6773-6790.
52. Gahete MD, Rubio A, Cordoba-Chacon J, Gracia-Navarro F, Kineman RD, Avila J, Luque RM, Castano JP (2010) Expression of the ghrelin and neurotensin systems is altered in the temporal lobe of Alzheimer's disease patients. J Alzheimers Dis 22, 819-828.
53. Theodoropoulou A, Metallinos IC, Psyrogiannis A, Vage-nakis GA, Kyriazopoulou V (2012) Ghrelin and leptin secretion in patients with moderate Alzheimer's disease. J Nutr Health Aging 16, 472-477.
54. Shibata N, Ohnuma T, Kuerban B, Komatsu M, Arai H (2011) Genetic association between ghrelin polymorphisms and Alzheimer's disease in a Japanese population. Dement Geriatr Cogn Disord 32, 178-181.
55. Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, Hor-vath B, Gaskin FS, Nonaka N, Jaeger LB, Banks WA, Morley JE, Pinto S, Sherwin RS, Xu L, Yamada KA, Sleeman MW, Tschop MH, Horvath TL (2006) Ghrelin controls hippocam-pal spine synapse density and memory performance. Nat Neurosci 9, 381-388.
56. Dhurandhar EJ, Allison DB, van Groen T, Kadish I Hunger in the absence of caloric restriction improves cognition and attenuates Alzheimer's disease pathology in a mouse model. PLoS One 8, e60437.
57. Martins I, Gomes S, Costa RO, Otvos L, Oliveira CR, Resende R, Pereira CM (2013) Leptin and ghrelin prevent hippocampal dysfunction induced by Abeta oligomers. Neuroscience 241, 41-51.
58. Bulgarelli I, Tamiazzo L, Bresciani E, Rapetti D, Caporali S, Lattuada D, Locatelli V, Torsello A (2009) Desacyl-ghrelin and synthetic GH-secretagogues modulate the production of inflammatory cytokines in mouse microglia cells stimulated by beta-amyloid fibrils. J Neurosci Res 87, 2718-2727.
59. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407, 908-913.