Caloric restriction stimulates autophagy in rat cortical neurons through neuropeptide Y and ghrelin receptors activation

Aging

Volumn 8, Issue 7, 2016, Pages 1470-1484

  Ferreira Marques, Marisa ^a   Aveleira, Célia A ^a   Carmo Silva, Sara ^a,b   Botelho, Mariana ^a,b   de Almeida, Luís Pereira ^a,b   Cavadas, Cláudia ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Autophagy; Caloric restriction; Cortical neurons; Ghrelin; Neuropeptide Y (NPY)

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GHRELIN; GHRELIN RECEPTOR; NEUROPEPTIDE RECEPTOR; NEUROPEPTIDE Y; NPY1R PROTEIN, RAT;

ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; BRAIN CORTEX; CALORIC RESTRICTION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FEMALE; METABOLISM; NERVE CELL; PHYSIOLOGY; RAT; WISTAR RAT;

ANIMALS; AUTOPHAGY; CALORIC RESTRICTION; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; GHRELIN; NEURONS; NEUROPEPTIDE Y; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, GHRELIN; RECEPTORS, NEUROPEPTIDE;

EID: 85014143445     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100996     Document Type: Article

References (94)

1. Flatt T. A new definition of aging? Front Genet. 2012; 3:148.
2. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW and Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science. 2009; 325:201-04.
3. Colman RJ, Beasley TM, Kemnitz JW, Johnson SC, Weindruch R and Anderson RM. Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat Commun. 2014; 5:3557.
4. Fowler CG, Torre P, 3rd and Kemnitz JW. Effects of caloric restriction and aging on the auditory function of rhesus monkeys (Macaca mulatta): The University of Wisconsin Study. Hear Res. 2002; 169:24-35.
5. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W, et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature. 2012; 489:318-21.
6. Yamada Y, Colman RJ, Kemnitz JW, Baum ST, Anderson RM, Weindruch R and Schoeller DA. Long-term calorie restriction decreases metabolic cost of movement and prevents decrease of physical activity during aging in rhesus monkeys. Exp Gerontol. 2013; 48:1226-35.
7. Masoro EJ. Dietary restriction-induced life extension: a broadly based biological phenomenon. Biogerontology. 2006; 7:153-55.
8. Roberts SB and Schoeller DA. Human caloric restriction for retardation of aging: current approaches and preliminary data. J Nutr. 2007; 137:1076-77.
9. Bergamini E, Cavallini G, Donati A and Gori Z. The role of autophagy in aging: its essential part in the anti-aging mechanism of caloric restriction. Ann N Y Acad Sci. 2007; 1114:69-78.
10. Fontana L, Partridge L and Longo VD. Extending healthy life span-from yeast to humans. Science. 2010; 328:321-26.
11. Fontana L and Partridge L. Promoting health and longevity through diet: from model organisms to humans. Cell. 2015; 161:106-18.
12. Donati A. The involvement of macroautophagy in aging and anti-aging interventions. Mol Aspects Med. 2006; 27:455-70.
13. Bergamini E, Cavallini G, Donati A and Gori Z. The anti-ageing effects of caloric restriction may involve stimulation of macroautophagy and lysosomal degradation, and can be intensified pharmacologically. Biomed Pharmacother. 2003; 57:203-208.
14. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M and Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 2008; 4:24.
15. Blagosklonny MV. Linking calorie restriction to longevity through sirtuins and autophagy: any role for TOR. Cell Death Dis. 2010; 1:12.
16. Cuervo AM. Autophagy and aging: keeping that old broom working. Trends Genet. 2008; 24:604-12.
17. Lopez-Otin C, Blasco MA, Partridge L, Serrano M and Kroemer G. The hallmarks of aging. Cell. 2013; 153:1194-17.
18. Marino G and Lopez-Otin C. Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci. 2004; 61:1439-54.
19. Cataldo AM, Hamilton DJ and Nixon RA. Lysosomal abnormalities in degenerating neurons link neuronal compromise to senile plaque development in Alzheimer disease. Brain Res. 1994; 640:68-80.
20. Cataldo AM, Hamilton DJ, Barnett JL, Paskevich PA and Nixon RA. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci. 1996; 16:186-99.
21. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Bruck W, Jellinger K and Lassmann H. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am J Pathol. 1999; 155:1459-66.
22. Yang DS, Kumar A, Stavrides P, Peterson J, Peterhoff CM, Pawlik M, Levy E, Cataldo AM and Nixon RA. Neuronal apoptosis and autophagy cross talk in aging PS/APP mice, a model of Alzheimer's disease. Am J Pathol. 2008; 173:665-81.
23. Anglade P, Vyas S, Javoy-Agid F, Herrero MT, Michel PP, Marquez J, Mouatt-Prigent A, Ruberg M, Hirsch EC and Agid Y. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histopathol. 1997; 12:25-31.
24. Spencer B, Potkar R, Trejo M, Rockenstein E, Patrick C, Gindi R, Adame A, Wyss-Coray T and Masliah E. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases. J Neurosci. 2009; 29:13578-88.
25. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N and DiFiglia M. Huntingtin expression stimulates endosomallysosomal activity, endosome tubulation, and autophagy. J Neurosci. 2000; 20:7268-78.
26. Sapp E, Schwarz C, Chase K, Bhide PG, Young AB, Penney J, Vonsattel JP, Aronin N and DiFiglia M. Huntingtin localization in brains of normal and Huntington's disease patients. Ann Neurol. 1997; 42:604-12.
27. Liberski PP, Sikorska B, Bratosiewicz-Wasik J, Gajdusek DC and Brown P. Neuronal cell death in transmissible spongiform encephalopathies (prion diseases) revisited: from apoptosis to autophagy. Int J Biochem Cell Biol. 2004; 36:2473-90.
28. Nascimento-Ferreira I, Santos-Ferreira T, Sousa-Ferreira L, Auregan G, Onofre I, Alves S, Dufour N, Colomer Gould VF, Koeppen A, Deglon N and Pereira de Almeida L. Overexpression of the autophagic beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease. Brain. 2011; 134:1400-15.
29. Minor RK, Chang JW and de Cabo R. Hungry for life: How the arcuate nucleus and neuropeptide Y may play a critical role in mediating the benefits of calorie restriction. Mol Cell Endocrinol. 2009; 299:79-88.
30. Bi S, Robinson BM and Moran TH. Acute food deprivation and chronic food restriction differentially affect hypothalamic NPY mRNA expression. Am J Physiol Regul Integr Comp Physiol. 2003; 285:1030-36.
31. Brady LS, Smith MA, Gold PW and Herkenham M. Altered expression of hypothalamic neuropeptide mRNAs in foodrestricted and food-deprived rats. Neuroendocrinology. 1990; 52:441-47.
32. de Rijke CE, Hillebrand JJ, Verhagen LA, Roeling TA and Adan RA. Hypothalamic neuropeptide expression following chronic food restriction in sedentary and wheel-running rats. J Mol Endocrinol. 2005; 35:381-90.
33. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA and O'Donohue TL. The anatomy of neuropeptide-Ycontaining neurons in rat brain. Neuroscience. 1985; 15:1159-81.
34. Silva AP, Xapelli S, Grouzmann E and Cavadas C. The putative neuroprotective role of neuropeptide Y in the central nervous system. Curr Drug Targets CNS Neurol Disord. 2005; 4:331-47.
35. Wettstein JG, Earley B and Junien JL. Central nervous system pharmacology of neuropeptide Y. Pharmacol Ther. 1995; 65:397-414.
36. Malva JO, Xapelli S, Baptista S, Valero J, Agasse F, Ferreira R and Silva AP. Multifaces of neuropeptide Y in the brain-neuroprotection, neurogenesis and neuroinflammation. Neuropeptides. 2012; 46:299-308.
37. Decressac M and Barker RA. Neuropeptide Y and its role in CNS disease and repair. Exp Neurol. 2012; 238:265-272.
38. Duarte-Neves J, Goncalves N, Cunha-Santos J, Simoes AT, den Dunnen WF, Hirai H, Kugler S, Cavadas C and Pereira de Almeida L. Neuropeptide Y mitigates neuropathology and motor deficits in mouse models of Machado-Joseph disease. Hum Mol Genet. 2015; 24:5451-63.
39. Aveleira CA, Botelho M, Carmo-Silva S, Pascoal JF, Ferreira-Marques M, Nobrega C, Cortes L, Valero J, Sousa-Ferreira L, Alvaro AR, Santana M, Kugler S, Pereira de Almeida L, et al. Neuropeptide Y stimulates autophagy in hypothalamic neurons. Proc Natl Acad Sci U S A. 2015; 112:1642-51.
40. Aveleira CA, Botelho M and Cavadas C. NPY/neuropeptide Y enhances autophagy in the hypothalamus: a mechanism to delay aging? Autophagy. 2015; 11:1431-33.
41. Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky SA, Anderson JG, Jung S, Birnbaum S, Yanagisawa M, Elmquist JK, Nestler EJ and Zigman JM. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci. 2008; 11:752-53.
42. Ariyasu H, Takaya K, Tagami T, Ogawa Y, Hosoda K, Akamizu T, Suda M, Koh T, Natsui K, Toyooka S, Shirakami G, Usui T, Shimatsu A, et al. Stomach is a major source of circulating ghrelin, and feeding state determines plasma ghrelin-like immunoreactivity levels in humans. J Clin Endocrinol Metab. 2001; 86:4753-58.
43. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H and Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999; 402:656-60.
44. Hou Z, Miao Y, Gao L, Pan H and Zhu S. Ghrelin-containing neuron in cerebral cortex and hypothalamus linked with the DVC of brainstem in rat. Regul Pept. 2006; 134:126-31.
45. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, et al. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron. 2003; 37:649-61.
46. Ferrini F, Salio C, Lossi L and Merighi A. Ghrelin in central neurons. Curr Neuropharmacol. 2009; 7:37-49.
47. Sato T, Nakamura Y, Shiimura Y, Ohgusu H, Kangawa K and Kojima M. Structure, regulation and function of ghrelin. J Biochem. 2012; 151:119-28.
48. Stengel A and Tache Y. Ghrelin-a pleiotropic hormone secreted from endocrine x/a-like cells of the stomach. Front Neurosci. 2012; 6:24.
49. Bayliss JA and Andrews ZB. Ghrelin is neuroprotective in Parkinson's disease: molecular mechanisms of metabolic neuroprotection. Ther Adv Endocrinol Metab. 2013; 4:25-36.
50. Miao Y, Xia Q, Hou Z, Zheng Y, Pan H and Zhu S. Ghrelin protects cortical neuron against focal ischemia/reperfusion in rats. Biochem Biophys Res Commun. 2007; 359:795-800.
51. Moon M, Choi JG, Nam DW, Hong HS, Choi YJ, Oh MS and Mook-Jung I. Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-beta1-42 oligomer-injected mice. J Alzheimers Dis. 2011; 23:147-59.
52. Spencer SJ, Miller AA and Andrews ZB. The role of ghrelin in neuroprotection after ischemic brain injury. Brain Sci. 2013; 3:344-59.
53. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016; 12:1-222.
54. Menzies FM, Moreau K, Puri C, Renna M and Rubinsztein DC. Measurement of autophagic activity in mammalian cells. Curr Protoc Cell Biol. 2012; Chapter 15:Unit 15. 16.
55. Mizushima N, Yoshimori T and Levine B. Methods in mammalian autophagy research. Cell. 2010; 140:313-26.
56. Gray TS and Morley JE. Neuropeptide Y: anatomical distribution and possible function in mammalian nervous system. Life Sci. 1986; 38:389-401.
57. Wren AM, Small CJ, Fribbens CV, Neary NM, Ward HL, Seal LJ, Ghatei MA and Bloom SR. The hypothalamic mechanisms of the hypophysiotropic action of ghrelin. Neuroendocrinology. 2002; 76:316-24.
58. Young JE, Martinez RA and La Spada AR. Nutrient deprivation induces neuronal autophagy and implicates reduced insulin signaling in neuroprotective autophagy activation. J Biol Chem. 2009; 284:2363-73.
59. Alirezaei M, Kemball CC, Flynn CT, Wood MR, Whitton JL and Kiosses WB. Short-term fasting induces profound neuronal autophagy. Autophagy. 2010; 6:702-10.
60. Botelho M and Cavadas C. Neuropeptide Y: An Anti-Aging Player? Trends Neurosci. 2015; 38:701-11.
61. Chiba T, Tamashiro Y, Park D, Kusudo T, Fujie R, Komatsu T, Kim SE, Park S, Hayashi H, Mori R, Yamashita H, Chung HY and Shimokawa I. A key role for neuropeptide Y in lifespan extension and cancer suppression via dietary restriction. Sci Rep. 2014; 4:4517.
62. Minor RK, Lopez M, Younts CM, Jones B, Pearson KJ, Anson RM, Dieguez C and de Cabo R. The arcuate nucleus and neuropeptide Y contribute to the antitumorigenic effect of calorie restriction. Aging Cell. 2011; 10:483-92.
63. Baranowska B, Bik W, Baranowska-Bik A, Wolinska-Witort E, Szybinska A, Martynska L and Chmielowska M. Neuroendocrine control of metabolic homeostasis in Polish centenarians. J Physiol Pharmacol. 2006; 57 Suppl 6:55-61.
64. Inoue H, Sakamoto Y, Kangawa N, Kimura C, Ogata T, Fujieda K, Qian ZR, Sano T and Itakura M. Analysis of expression and structure of the rat GH-secretagogue/ghrelin receptor (Ghsr) gene: roles of epigenetic modifications in transcriptional regulation. Mol Cell Endocrinol. 2011; 345:1-15.
65. Nass R, Farhy LS, Liu J, Pezzoli SS, Johnson ML, Gaylinn BD and Thorner MO. Age-dependent decline in acyl-ghrelin concentrations and reduced association of acyl-ghrelin and growth hormone in healthy older adults. J Clin Endocrinol Metab. 2014; 99:602-08.
66. Guan XM, Yu H, Palyha OC, McKee KK, Feighner SD, Sirinathsinghji DJ, Smith RG, Van der Ploeg LH and Howard AD. Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res. 1997; 48:23-29.
67. Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, Rosenblum CI, Hamelin M, Hreniuk DL, Palyha OC, Anderson J, Paress PS, Diaz C, Chou M, et al. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science. 1996; 273:974-77.
68. Zigman JM, Jones JE, Lee CE, Saper CB and Elmquist JK. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol. 2006; 494:528-48.
69. Spencer SJ, Miller AA and Andrews ZB. The Role of Ghrelin in Neuroprotection after Ischemic Brain Injury. Brain Sci. 2013; 3:344-59.
70. Lin L, Saha PK, Ma X, Henshaw IO, Shao L, Chang BH, Buras ED, Tong Q, Chan L, McGuinness OP and Sun Y. Ablation of ghrelin receptor reduces adiposity and improves insulin sensitivity during aging by regulating fat metabolism in white and brown adipose tissues. Aging Cell. 2011; 10:996-1010.
71. Finger BC, Dinan TG and Cryan JF. Behavioral satiety sequence in a genetic mouse model of obesity: effects of ghrelin receptor ligands. Behav Pharmacol. 2011; 22:624-32.
72. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K and Matsukura S. A role for ghrelin in the central regulation of feeding. Nature. 2001; 409:194-98.
73. Tschop M, Smiley DL and Heiman ML. Ghrelin induces adiposity in rodents. Nature. 2000; 407:908-13.
74. Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG, Dhillo WS, Ghatei MA and Bloom SR. Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab. 2001; 86:5992.
75. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA and Bloom SR. Ghrelin causes hyperphagia and obesity in rats. Diabetes. 2001; 50:2540-47.
76. Wren AM, Small CJ, Ward HL, Murphy KG, Dakin CL, Taheri S, Kennedy AR, Roberts GH, Morgan DG, Ghatei MA and Bloom SR. The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology. 2000; 141:4325-28.
77. Ariyasu H, Iwakura H, Yamada G, Nakao K, Kangawa K and Akamizu T. Efficacy of ghrelin as a therapeutic approach for agerelated physiological changes. Endocrinology. 2008; 149:3722-28.
78. Fujitsuka N, Asakawa A, Morinaga A, Amitani MS, Amitani H, Katsuura G, Sawada Y, Sudo Y, Uezono Y, Mochiki E, Sakata I, Sakai T, Hanazaki K, et al. Increased ghrelin signaling prolongs survival in mouse models of human aging through activation of sirtuin1. Mol Psychiatry. 2016. Epub ahead of print.
79. Al Massadi O, Lopez M, Ferno J, Dieguez C and Nogueiras R. What is the real relevance of endogenous ghrelin? Peptides. 2015; 70:1-6.
80. Wierup N, Yang S, McEvilly RJ, Mulder H and Sundler F. Ghrelin is expressed in a novel endocrine cell type in developing rat islets and inhibits insulin secretion from INS-1 (832/13) cells. J Histochem Cytochem. 2004; 52:301-10.
81. Fernandez-Fernandez R, Tena-Sempere M, Aguilar E and Pinilla L. Ghrelin effects on gonadotropin secretion in male and female rats. Neurosci Lett. 2004; 362:103-07.
82. Akamizu T and Kangawa K. The physiological significance and potential clinical applications of ghrelin. Eur J Intern Med. 2012; 23:197-202.
83. Strasser F. Clinical application of ghrelin. Curr Pharm Des. 2012; 18:4800-12.
84. Chen HY, Trumbauer ME, Chen AS, Weingarth DT, Adams JR, Frazier EG, Shen Z, Marsh DJ, Feighner SD, Guan XM, Ye Z, Nargund RP, Smith RG, et al. Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology. 2004; 145:2607-12.
85. Fujimiya M, Asakawa A, Ataka K, Chen CY, Kato I and Inui A. Ghrelin, des-acyl ghrelin, and obestatin: regulatory roles on the gastrointestinal motility. Int J Pept. 2010; 2010.
86. Gualillo O, Lago F, Gomez-Reino J, Casanueva FF and Dieguez C. Ghrelin, a widespread hormone: insights into molecular and cellular regulation of its expression and mechanism of action. FEBS Lett. 2003; 552:105-109.
87. Horvath TL, Diano S, Sotonyi P, Heiman M and Tschop M. Minireview: ghrelin and the regulation of energy balance-a hypothalamic perspective. Endocrinology. 2001; 142:4163-4169.
88. Chiodera P, Volpi R, Pilla S, Cataldo S and Coiro V. Decline in circulating neuropeptide Y levels in normal elderly human subjects. Eur J Endocrinol. 2000; 143:715-16.
89. Rigamonti AE, Pincelli AI, Corra B, Viarengo R, Bonomo SM, Galimberti D, Scacchi M, Scarpini E, Cavagnini F and Muller EE. Plasma ghrelin concentrations in elderly subjects: comparison with anorexic and obese patients. J Endocrinol. 2002; 175:1-5.
90. Sturm K, MacIntosh CG, Parker BA, Wishart J, Horowitz M and Chapman IM. Appetite, food intake, and plasma concentrations of cholecystokinin, ghrelin, and other gastrointestinal hormones in undernourished older women and well-nourished young and older women. J Clin Endocrinol Metab. 2003; 88:3747-55.
91. Decressac M, Pain S, Chabeauti PY, Frangeul L, Thiriet N, Herzog H, Vergote J, Chalon S, Jaber M and Gaillard A. Neuroprotection by neuropeptide Y in cell and animal models of Parkinson's disease. Neurobiol Aging. 2012; 33:2125-37.
92. Decressac M, Wright B, Tyers P, Gaillard A and Barker RA. Neuropeptide Y modifies the disease course in the R6/2 transgenic model of Huntington's disease. Exp Neurol. 2010; 226:24-32.
93. Rose JB, Crews L, Rockenstein E, Adame A, Mante M, Hersh LB, Gage FH, Spencer B, Potkar R, Marr RA and Masliah E. Neuropeptide Y fragments derived from neprilysin processing are neuroprotective in a transgenic model of Alzheimer's disease. J Neurosci. 2009; 29:1115-25.
94. Stoyanova, II. Ghrelin: A link between ageing, metabolism and neurodegenerative disorders. Neurobiol Dis. 2014; 72:72-83.