Differential Regulation of Hippocampal IGF-1-Associated Signaling Proteins by Dietary Restriction in Aging Mouse

Cellular and Molecular Neurobiology

Volumn 37, Issue 6, 2017, Pages 985-993

  Hadem, Ibanylla Kynjai Hynniewta ^a   Sharma, Ramesh ^a  

^a NORTH EASTERN HILL UNIVERSITY   (India)

Author keywords

Aging; DR; Hippocampus; IGF 1; Mouse

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR FOXO;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; DIET RESTRICTION; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LIVER; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; YOUNG ADULT; AGING; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; CALORIC RESTRICTION; DENSITOMETRY; GENETICS; METABOLISM;

AGING; ANIMALS; BODY WEIGHT; CALORIC RESTRICTION; DENSITOMETRY; FEMALE; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; LIVER; MICE, INBRED BALB C; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84990909250     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-016-0431-7     Document Type: Article

References (53)

1. Adams MM, Shi L, Linville MC, Forbes ME, Long AB, Bennett C, Newton IG, Carter CS, Sonntag WE, Riddle DR, Brunso-Bechtold JK (2008) Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Exp Neurol 211:141–149
2. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F (1995) Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14:717–730
3. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464:529–535
4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
5. Breese CR, Ingram RL, Sonntag WE (1991) Influence of age and long-term dietary restriction on plasma insulin-like growth factor-I (IGF-1), IGF-1 gene expression, and IGF-1 binding-proteins. J Gerontol 46:180–187
6. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11:297–305
7. Burger JM, Buechel SD, Kawecki TJ (2010) Dietary restriction affects lifespan but not cognitive aging in Drosophila melanogaster. Aging Cell 9:327–335
8. Carro E, Nunez A, Busiguina S, Torres-Aleman I (2000) Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 20:2926–2933
9. Carro E, Trejo JL, Nunez A, Torres-Aleman I (2003) Brain repair and neuroprotection by serum insulin-like growth factor I. Mol Neurobiol 27:153–162
10. Chia DJ (2014) Minireview: mechanisms of growth hormone-mediated gene regulation. Mol Endocrinol 28:1012–1025
11. Chiba T, Yamaza H, Shimokawa I (2007) Role of insulin and growth hormone/insulin-like growth factor-I signaling in lifespan extension: rodent longevity models for studying aging and calorie restriction. Curr Genomics 8:423–428
12. Clemmons DR (2007) Modifying IGF-1 activity: an approach to treat endocrine disorders, atherosclerosis, and cancer. Nat Rev Drug Discover 6:821–833
13. Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D, Estepa G, Adame A, Pham HM, Holzenberger M, Kelly JW, Masliah E, Dillin A (2009) Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139:1157–1169
14. Colman RJ, Beasley TM, Kemnitz JW, Johnson SC, Weindruch R, Anderson RM (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204
15. Dkhar P, Sharma R (2014) Late-onset dietary restriction modulates protein carbonylation and catalase in cerebral hemispheres of aged mice. Cell Mol Neurobiol 34:307–313
16. Eckel-Mahan KL, Phan T, Han S, Chan Wang HGCK, Scheiner ZS, Storm DR (2008) Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nat Neurosci 11:1074–1082
17. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span- from yeast to humans. Science 328:321–326
18. Geinisman Y, Detoledo-Morrell L, Morrell F, Heller RE (1995) Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog Neurobiol 45:223–252
19. Gkikas I, Petratou D, Tavernarakis N (2014) Longevity pathways and memory aging. Front Genet 5:1–10
20. Gómez-Crisóstomo NP, Rodríguez Martínez E, Rivas-Arancibia S (2014) Oxidative stress activates the transcription factors FoxO 1a and FoxO 3a in the hippocampus of rats exposed to low doses of ozone. Oxid Med Cell Longev 805764:1–8
21. Gontier G, George C, Chaker Z, Holzenberger M, Aïd S (2015) Blocking IGF signaling in adult neurons alleviates Alzheimer’s disease pathology through amyloid-β clearance. J Neurosci 35:11500–11513
22. Hadem IKH, Sharma R (2016) Age- and tissue-dependent modulation of IGF-1/PI3K/Akt protein expression by dietary restriction in mice. Horm Metab Res 48:201–206
23. Jackson TC, Rani A, Kumar A, Foster TC (2009) Regional hippocampal differences in AKT survival signaling across the lifespan: implications for CA1 vulnerability with aging. Cell Death Differ 16:439–448
24. Kappeler L, De Magalhaes Filho C, Dupont J, Leneuve P, Cervera P, Périn L, Loudes C, Blaise A, Klein R, Epelbaum J, Le Bouc Y, Holzenberger M (2008) Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol 6:e254
25. Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512
26. Khanna A, Muthusamy S, Liang R, Sarojini H, Wang E (2011) Gain of survival signaling by down-regulation of three Key miRNAs in brain of calorie-restricted mice. Aging 3:223–236
27. Kinney BA, Coschigano KT, Kopchick JJ, Steger RW, Bartke A (2001) Evidence that age-induced decline in memory retention is delayed in growth hormone resistant GH-R-KO (Laron) mice. Physiol Behav 72:653–660
28. Lai M, Hibbard CJ, Gluckman PD, Seckl JR (2000) Reduced expression of insulin-like growth factor 1 messenger RNA in the hippocampus of aged rats. Neurosci Lett 288:66–70
29. Lee CK, Weindruch R, Prolla TA (2000) Gene-expression profile of the ageing brain in mice. Nature Genet 25:294–297
30. Lee J, Duan W, Mattson MP (2002) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem 82:1367–1375
31. Liang R, Khanna A, Muthusamy S, Li N, Sarojini H, Kopchick JJ, Masternak MM, Bartke A, Wang E (2011) Post-transcriptional regulation of IGF1R byKey microRNAs in long-lived mutant mice. Aging Cell 10:1080–1088
32. -DDCt method. Methods 25:402–408
33. Longo VD, Mattson MP (2014) Fasting: molecular mechanisms and clinical applications. Cell Metab 19:181–192
34. Majaw T, Sharma R (2015) Arginase I expression is upregulated by dietary restriction in the liver of mice as a function of age. Mol Cell Biochem 407:1–7
35. Martin B, Mattson MP, Maudsley S (2006) Caloric restriction and intermittent fasting: two potential diets for successful brain aging. Ageing Res Rev 5:332–353
36. Mercken EM, Carboneau BA, Krzysik-Walker SM, de Cabo R (2012) Of mice and men: the benefits of caloric restriction, exercise, and mimetics. Ageing Res Rev 11:390–398
37. Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, Chae SS, Zheng H, Ying H, Mahoney J, Hiller D, Jiang S, Protopopov A, Wong WH, Chin L, Ligon KL, DePinho RA (2009) FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5:540–553
38. Park SK, Kim K, Page GP, Allison DB, Weindruch R, Prolla TA (2009) Gene expression profiling of aging in multiple mouse strains: identification of aging biomarkers and impact of dietary antioxidants. Aging Cell 8:484–495
39. Qiu G, Liu S, So KF (2010) Dietary restriction and brain health. Neurosci Bull 26:55–65
40. Rafalski VA, Brunet A (2011) Energy metabolism in adult neural stem cell fate. Prog Neurobiol 9:182–203
41. Reinhardt RR, Bondy CA (1994) Insulin-like growth factors cross the blood–brain barrier. Endocrinology 135:1753–1761
42. Renault VM, Rafalski VA, Morgan AA, Salih DA, Brett JO, Webb AE, Villeda SA, Thekkat PU, Guillerey C, Denko NC, Palmer TD, Butte AJ, Brunet A (2009) FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5:527–539
43. Shahmoradia A, Radyushkina K, Rossnera MJ (2015) Enhanced memory consolidation in mice lacking the circadian modulators Sharp1 and -2 caused by elevated Igf2 signaling in the cortex. Proc Natl Acad Sci USA 112:E3582–E3589
44. Sonntag WE, Lynch C, Thornton P, Khan A, Bennett S, Ingram R (2000) The effects of growth hormone and IGF-1 deficiency on cerebrovascular and brain ageing. J Anat 197:575–585
45. Speakman JR, Mitchell SE (2011) Caloric restriction. Mol Aspects Med 32:159–221
46. Suh HS, Zhao ML, Derico L, Choi N, Lee SC (2013) Insulin-like growth factor 1 and 2 (IGF1, IGF2) expression in human microglia: differential regulation by inflammatory mediators. J Neuroinflammation 10:37
47. Sun LY, Bartke A (2007) Adult neurogenesis in the hippocampus of long-lived mice during aging. J Gerontol A Biol Sci Med Sci 62:117–125
48. Taguchi A, Wartschow LM, White MF (2007) Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317:369–372
49. Toker A (2000) ProteinKinases as mediators of phosphoinositide 3-kinase signaling. Mol Pharmacol 57:652–658
50. Uranga RM, Katz S, Salvador GA (2013) Enhanced phosphatidylinositol 3-kinase (PI3K)/Akt signaling has pleiotropic targets in hippocampal neurons exposed to iron-induced oxidative stress. J Biol Chem 288:19773–19784
51. Vanhaesebroeck B, Alessi DR (2000) The PI3K-PDK1 connection. More than just a road to PKB. Biochem J 346:561–576
52. Witte AV, Fobker M, Gellner R, Knecht S, Flöel A (2009) Caloric restriction improves memory in elderly humans. Proc Natl Acad Sci USA 106:1255–1260
53. Zheng WH, Kar S, Quirion R (2002) Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/AktKinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol Pharmacol 62:225–233