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Caloric restriction maintains stem cells through niche and regulates stem cell aging

  • Nagarajan Maharajan
  • Karthikeyan Vijayakumar
  • Chul Ho Jang
  • Goang-Won ChoEmail author
Review
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Abstract

The functional loss of adult stem cells is a major cause of aging and age-related diseases. Changes in the stem cell niche, increased energy metabolic rate, and accumulation of cell damage severely affect the function and regenerative capacity of stem cells. Reducing the cellular damage and maintaining a pristine stem cell niche by regulating the energy metabolic pathways could be ideal for the proper functioning of stem cells and tissue homeostasis. Numerous studies point out that caloric restriction (CR) has beneficiary effects on stem cell maintenance and tissue regeneration. Recent researches indicate the preventive nature of calorie restriction in stem cells by modulating the stem cell niche through the reduction of energy metabolism and eventually decrease stem cell damage. In this review, we have focused on the general stimuli of stem cell aging, particularly the energy metabolism as an intrinsic influence and stem cell niche as an extrinsic influence in different adult stem cells. Further, we discussed the mechanism behind CR in different adult stem cells and their niche. Finally, we conclude on how CR can enhance the stem cell function and tissue homeostasis through the stem cells niche.

Keywords

Stem cells Stem cell niche Caloric restriction Longevity Aging Energy metabolism 

Abbreviations

4E-BP1

Eukaryotic translation initiation factor 4E-binding protein 1

AKT

Protein kinase B

AML

Acute myeloid leukemia

AMPK

Adenosine monophosphate-activated protein kinase

Atg7

Autophagy-related gene 7

ATP

Adenosine triphosphate

BMP

Bone morphogenetic protein

Bst1

Bone marrow stromal cell antigen 1

Ca2+

Calcium

cADPR

Cyclic ADP ribose

CaMKK

Calcium/calmodulin-dependent protein kinase kinase 1

CaMKK-β

Calmodulin-dependent protein kinase kinase beta

CR

Caloric restriction

CRM

Caloric restriction mimetics

dPGC1/spargel

Drosophila PGC-1 homolog

ECM

Extracellular matrix

FOXO3A

Forkhead box protein O3

FOXO

Forkhead box O

GCN2

Nonderepressible 2

Glu

Glucose

GSCs

Germline stem cells

GSH

Glutathione

hBM-MSCs

Human bone marrow MSCs

HepG2

Hepatoma-derived cell line

HGPS

Hutchinson-Gilford progeria syndrome

HIF 1α

Hypoxic-inducible factor 1 α

HSCs

Hematopoietic stem cells

IGF-1

Insulin-like growth factor-1

IIS

Insulin and IGF-1 signaling

ISCs

Intestinal stem cells

MSCs

Mesenchymal stem cells

MtDNA

Mitochondrial DNA

mTOR

Mammalian target of rapamycin

mTORC1

Mammalian target of rapamycin complex 1

MuSCs

Muscle stem cells/satellite stem cells

NAC

N-acetylcysteine

Nampt

Nicotinamide phosphoribosyl transferase

NF-kB

Nuclear factor-kappa B

NMN

Nicotinamide mononucleotide

NSCs

Neural stem cells

OXPHOS

Oxidative phosphorylation

PDKs

Pyruvate dehydrogenase kinases

PGC1

Peroxisome proliferator-activated receptor gamma coactivator-1α

PI3K

Phosphoinositide 3-kinase

ROS

Reactive oxygen species

S6K1

Ribosomal protein S6 kinase beta-1

SIRT1

Sirtuin 1

SIRT3

Sirtuin 3

TA

Transit-amplifying cells

TSC1-TSC2

Tuberous sclerosis 1 and 2 complex

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Notes

Funding information

This work was supported by research fund from Chosun University (2019).

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. 1.
    Barzilai N, Huffman DM, Muzumdar RH, Bartke A (2012) The critical role of metabolic pathways in aging. Diabetes 61(6):1315–1322PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153(6):1194–1217PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Hoggatt J, Scadden DT (2012) The stem cell niche: tissue physiology at a single cell level. J Clin Invest 122(9):3029–3034PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Li L, Xie T (2005) Stem cell niche: structure and function. Annual review of cell and developmental biology 21:605–631PubMedCrossRefGoogle Scholar
  5. 5.
    Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nature reviews Molecular cell biology 14(6):329–340PubMedCrossRefGoogle Scholar
  6. 6.
    Wagers AJ (2012) The stem cell niche in regenerative medicine. Cell stem cell 10(4):362–369PubMedCrossRefGoogle Scholar
  7. 7.
    Rezza A, Sennett R, Rendl M (2014) Adult stem cell niches: cellular and molecular components. Current topics in developmental biology 107:333–372PubMedCrossRefGoogle Scholar
  8. 8.
    Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science (New York, NY) 325(5937):201–204CrossRefGoogle Scholar
  9. 9.
    Mattison JA, Colman RJ, Beasley TM, Allison DB, Kemnitz JW, Roth GS, Ingram DK, Weindruch R, de Cabo R, Anderson RM (2017) Caloric restriction improves health and survival of rhesus monkeys. Nature communications 8:14063PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Liang Y, Liu C, Lu M, Dong Q, Wang Z, Wang Z, Xiong W, Zhang N, Zhou J, Liu Q, Wang X, Wang Z (2018) Calorie restriction is the most reasonable anti-ageing intervention: a meta-analysis of survival curves. Scientific reports 8(1):5779PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Bales CW, Kraus WE (2013) Caloric restriction: implications for human cardiometabolic health. Journal of cardiopulmonary rehabilitation and prevention 33(4):201–208PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Roth GS, Lane MA, Ingram DK (2005) Caloric restriction mimetics: the next phase. Ann N Y Acad Sci 1057:365–371PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Ingram DK, Anson RM, de Cabo R, Mamczarz J, Zhu M, Mattison J, Lane MA, Roth GS (2004) Development of calorie restriction mimetics as a prolongevity strategy. Ann N Y Acad Sci 1019:412–423PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Oh J, Lee YD, Wagers AJ (2014) Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nature medicine 20(8):870–880PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Sousa-Victor P, Garcia-Prat L, Serrano AL, Perdiguero E, Munoz-Canoves P (2015) Muscle stem cell aging: regulation and rejuvenation. Trends in endocrinology and metabolism: TEM 26(6):287–296PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Liu L, Rando TA (2011) Manifestations and mechanisms of stem cell aging. The Journal of cell biology 193(2):257–266PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Rube CE, Fricke A, Widmann TA, Furst T, Madry H, Pfreundschuh M, Rube C (2011) Accumulation of DNA damage in hematopoietic stem and progenitor cells during human aging. PloS one 6(3):e17487.  https://doi.org/10.1371/journal.pone.0017487 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Burtner CR, Kennedy BK (2010) Progeria syndromes and ageing: what is the connection? Nature reviews Molecular cell biology 11(8):567–578PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Green DR, Galluzzi L, Kroemer G (2011) Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science (New York, NY) 333(6046):1109–1112CrossRefGoogle Scholar
  20. 20.
    Pervaiz S, Taneja R, Ghaffari S (2009) Oxidative stress regulation of stem and progenitor cells. Antioxidants & redox signaling 11(11):2777–2789CrossRefGoogle Scholar
  21. 21.
    Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I, Nomiyama K, Hosokawa K, Sakurada K, Nakagata N, Ikeda Y, Mak TW, Suda T (2004) Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431(7011):997–1002PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Almeida M, O'Brien CA (2013) Basic biology of skeletal aging: role of stress response pathways. The journals of gerontology Series A, Biological sciences and medical sciences 68(10):1197–1208PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Drowley L, Okada M, Beckman S, Vella J, Keller B, Tobita K, Huard J (2010) Cellular antioxidant levels influence muscle stem cell therapy. Molecular therapy : the journal of the American Society of Gene Therapy 18(10):1865–1873CrossRefGoogle Scholar
  24. 24.
    Warr MR, Binnewies M, Flach J, Reynaud D, Garg T, Malhotra R, Debnath J, Passegue E (2013) FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 494(7437):323–327PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Mortensen M, Soilleux EJ, Djordjevic G, Tripp R, Lutteropp M, Sadighi-Akha E, Stranks AJ, Glanville J, Knight S, Jacobsen SE, Kranc KR, Simon AK (2011) The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. The Journal of experimental medicine 208(3):455–467PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Powers ET, Morimoto RI, Dillin A, Kelly JW, Balch WE (2009) Biological and chemical approaches to diseases of proteostasis deficiency. Annual review of biochemistry 78:959–991PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Brown K, Xie S, Qiu X, Mohrin M, Shin J, Liu Y, Zhang D, Scadden DT, Chen D (2013) SIRT3 reverses aging-associated degeneration. Cell reports 3(2):319–327PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Rojas-Rios P, Gonzalez-Reyes A (2014) Concise review: the plasticity of stem cell niches: a general property behind tissue homeostasis and repair. Stem cells (Dayton, Ohio) 32(4):852–859CrossRefGoogle Scholar
  29. 29.
    Watt FM, Huck WT (2013) Role of the extracellular matrix in regulating stem cell fate. Nature reviews Molecular cell biology 14(8):467–473PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Wang LD, Wagers AJ (2011) Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nature reviews Molecular cell biology 12(10):643–655PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Lane SW, Williams DA, Watt FM (2014) Modulating the stem cell niche for tissue regeneration. Nature biotechnology 32(8):795–803PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Wei Q, Frenette PS (2018) Niches for hematopoietic stem cells and their progeny. Immunity 48(4):632–648PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Crane GM, Jeffery E, Morrison SJ (2017) Adult haematopoietic stem cell niches. Nature reviews Immunology 17(9):573–590PubMedCrossRefGoogle Scholar
  34. 34.
    Morrison SJ, Scadden DT (2014) The bone marrow niche for haematopoietic stem cells. Nature 505(7483):327–334PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Winkler IG, Sims NA, Pettit AR, Barbier V, Nowlan B, Helwani F, Poulton IJ, van Rooijen N, Alexander KA, Raggatt LJ, Levesque JP (2010) Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116(23):4815–4828PubMedCrossRefGoogle Scholar
  36. 36.
    Boyle M, Wong C, Rocha M, Jones DL (2007) Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell stem cell 1(4):470–478PubMedCrossRefGoogle Scholar
  37. 37.
    Kai T, Spradling A (2003) An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proceedings of the National Academy of Sciences of the United States of America 100(8):4633–4638PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nature reviews Molecular cell biology 15(1):19–33PubMedCrossRefGoogle Scholar
  39. 39.
    Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469(7330):415–418PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Porter EM, Bevins CL, Ghosh D, Ganz T (2002) The multifaceted Paneth cell. Cellular and molecular life sciences : CMLS 59(1):156–170PubMedCrossRefGoogle Scholar
  41. 41.
    Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143(1):134–144CrossRefGoogle Scholar
  42. 42.
    Sabelstrom H, Stenudd M, Reu P, Dias DO, Elfineh M, Zdunek S, Damberg P, Goritz C, Frisen J (2013) Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science (New York, NY) 342(6158):637–640CrossRefGoogle Scholar
  43. 43.
    Pan L, Chen S, Weng C, Call G, Zhu D, Tang H, Zhang N, Xie T (2007) Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell stem cell 1(4):458–469PubMedCrossRefGoogle Scholar
  44. 44.
    Winkler IG, Barbier V, Nowlan B, Jacobsen RN, Forristal CE, Patton JT, Magnani JL, Levesque JP (2012) Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nature medicine 18(11):1651–1657PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Farin HF, Van Es JH, Clevers H (2012) Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143(6):1518-1529.e1517CrossRefGoogle Scholar
  46. 46.
    van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H (2005) Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435(7044):959–963PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, Offerhaus GJ, Clevers H (2004) De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science (New York, NY) 303(5664):1684–1686CrossRefGoogle Scholar
  48. 48.
    Goodman SL, Picard M (2012) Integrins as therapeutic targets. Trends in pharmacological sciences 33(7):405–412PubMedCrossRefGoogle Scholar
  49. 49.
    Zutter MM (2007) Integrin-mediated adhesion: tipping the balance between chemosensitivity and chemoresistance. Advances in experimental medicine and biology 608:87–100PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Stearns-Reider KM, D'Amore A, Beezhold K, Rothrauff B, Cavalli L, Wagner WR, Vorp DA, Tsamis A, Shinde S, Zhang C, Barchowsky A, Rando TA, Tuan RS, Ambrosio F (2017) Aging of the skeletal muscle extracellular matrix drives a stem cell fibrogenic conversion. Aging cell 16(3):518–528PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433(7027):760–764PubMedCrossRefGoogle Scholar
  52. 52.
    Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Developmental cell 3(3):397–409PubMedCrossRefGoogle Scholar
  53. 53.
    Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science (New York, NY) 302(5650):1575–1577CrossRefGoogle Scholar
  54. 54.
    Ryu BY, Orwig KE, Oatley JM, Avarbock MR, Brinster RL (2006) Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal. Stem cells (Dayton, Ohio) 24(6):1505–1511CrossRefGoogle Scholar
  55. 55.
    Chakkalakal JV, Jones KM, Basson MA, Brack AS (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490(7420):355–360PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Ito K, Suda T (2014) Metabolic requirements for the maintenance of self-renewing stem cells. Nature reviews Molecular cell biology 15(4):243–256PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zhang CC, Sadek HA (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell stem cell 7(3):380–390PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell stem cell 7(2):150–161PubMedCrossRefGoogle Scholar
  59. 59.
    Rafalski VA, Mancini E, Brunet A (2012) Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. Journal of cell science 125(Pt 23):5597–5608PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Li L, Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science (New York, NY) 327(5965):542–545CrossRefGoogle Scholar
  61. 61.
    Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479(7372):232–236PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Barcena C, Quiros PM, Durand S, Mayoral P, Rodriguez F, Caravia XM, Marino G, Garabaya C, Fernandez-Garcia MT, Kroemer G, Freije JMP, Lopez-Otin C (2018) Methionine restriction extends lifespan in progeroid mice and alters lipid and bile acid metabolism. Cell reports 24(9):2392–2403PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Haller S, Kapuria S, Riley RR, O'Leary MN, Schreiber KH, Andersen JK, Melov S, Que J, Rando TA, Rock J, Kennedy BK, Rodgers JT, Jasper H (2017) mTORC1 Activation during repeated regeneration impairs somatic stem cell maintenance. Cell stem cell 21(6):806-818.e805CrossRefGoogle Scholar
  64. 64.
    Choi KM, Hong SJ, van Deursen JM, Kim S, Kim KH, Lee CK (2017) Caloric restriction and rapamycin differentially alter energy metabolism in yeast. The journals of gerontology Series A, Biological sciences and medical sciences 73(1):29–38PubMedCrossRefGoogle Scholar
  65. 65.
    Fok WC, Zhang Y, Salmon AB, Bhattacharya A, Gunda R, Jones D, Ward W, Fisher K, Richardson A, Perez VI (2013) Short-term treatment with rapamycin and dietary restriction have overlapping and distinctive effects in young mice. The journals of gerontology Series A, Biological sciences and medical sciences 68(2):108–116PubMedCrossRefGoogle Scholar
  66. 66.
    Fok WC, Bokov A, Gelfond J, Yu Z, Zhang Y, Doderer M, Chen Y, Javors M, Wood WH 3rd, Zhang Y, Becker KG, Richardson A, Perez VI (2014) Combined treatment of rapamycin and dietary restriction has a larger effect on the transcriptome and metabolome of liver. Aging cell 13(2):311–319PubMedCrossRefGoogle Scholar
  67. 67.
    Delarue M, Brittingham GP, Pfeffer S, Surovtsev IV, Pinglay S, Kennedy KJ, Schaffer M, Gutierrez JI, Sang D, Poterewicz G, Chung JK, Plitzko JM, Groves JT, Jacobs-Wagner C, Engel BD, Holt LJ (2018) mTORC1 controls phase separation and the biophysical properties of the cytoplasm by tuning crowding. Cell 174(2):338-349.e320CrossRefGoogle Scholar
  68. 68.
    Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ (2012) Short-term calorie restriction enhances skeletal muscle stem cell function. Cell stem cell 10(5):515–519PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Bar-Peled L, Sabatini DM (2014) Regulation of mTORC1 by amino acids. Trends in cell biology 24(7):400–406PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Bar-Peled L, Schweitzer LD, Zoncu R, Sabatini DM (2012) Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 150(6):1196–1208PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Orentreich N, Matias JR, DeFelice A, Zimmerman JA (1993) Low methionine ingestion by rats extends life span. The Journal of nutrition 123(2):269–274PubMedGoogle Scholar
  72. 72.
    Troen AM, French EE, Roberts JF, Selhub J, Ordovas JM, Parnell LD, Lai CQ (2007) Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet. Age (Dordrecht, Netherlands) 29(1):29–39CrossRefGoogle Scholar
  73. 73.
    Miller RA, Buehner G, Chang Y, Harper JM, Sigler R, Smith-Wheelock M (2005) Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging cell 4(3):119–125PubMedCrossRefGoogle Scholar
  74. 74.
    Mirisola MG, Taormina G, Fabrizio P, Wei M, Hu J, Longo VD (2014) Serine- and threonine/valine-dependent activation of PDK and Tor orthologs converge on Sch9 to promote aging. PLoS genetics 10(2):e1004113.  https://doi.org/10.1371/journal.pgen.1004113 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Guo F, Cavener DR (2007) The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell metabolism 5(2):103–114PubMedCrossRefGoogle Scholar
  76. 76.
    Xiao F, Huang Z, Li H, Yu J, Wang C, Chen S, Meng Q, Cheng Y, Gao X, Li J, Liu Y, Guo F (2011) Leucine deprivation increases hepatic insulin sensitivity via GCN2/mTOR/S6K1 and AMPK pathways. Diabetes 60(3):746–756PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Laplante M, Sabatini DM (2009) mTOR signaling at a glance. Journal of cell science 122(Pt 20):3589–3594PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Meng D, Frank AR, Jewell JL (2018) mTOR signaling in stem and progenitor cells. Development (Cambridge, England) 145(1).  https://doi.org/10.1242/dev.152595 PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115(5):577–590CrossRefGoogle Scholar
  80. 80.
    Kadowaki T, Ueki K, Yamauchi T, Kubota N (2012) SnapShot: insulin signaling pathways. Cell 148(3):624, 624.e621CrossRefGoogle Scholar
  81. 81.
    Soulard A, Hall MN (2007) SnapShot: mTOR signaling. Cell 129(2):434PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431(7005):200–205PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Fontana L, Partridge L, Longo VD (2010) Extending healthy life span--from yeast to humans. Science (New York, NY) 328(5976):321–326CrossRefGoogle Scholar
  84. 84.
    Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512CrossRefGoogle Scholar
  85. 85.
    Guarente L, Picard F (2005) Calorie restriction--the SIR2 connection. Cell 120(4):473–482PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Webb AE, Kundaje A, Brunet A (2016) Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging cell 15(4):673–685PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Murtaza G, Khan AK, Rashid R, Muneer S, Hasan SMF, Chen J (2017) FOXO transcriptional factors and long-term living. Oxidative medicine and cellular longevity 2017:3494289PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Eijkelenboom A, Burgering BM (2013) FOXOs: signalling integrators for homeostasis maintenance. Nature reviews Molecular cell biology 14(2):83–97PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Kim DH, Park MH, Lee EK, Choi YJ, Chung KW, Moon KM, Kim MJ, An HJ, Park JW, Kim ND, Yu BP, Chung HY (2015) The roles of FoxOs in modulation of aging by calorie restriction. Biogerontology 16(1):1–14PubMedCrossRefGoogle Scholar
  90. 90.
    Kim S, Koh H (2017) Role of FOXO transcription factors in crosstalk between mitochondria and the nucleus. Journal of bioenergetics and biomembranes 49(4):335–341PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Kume S, Uzu T, Horiike K, Chin-Kanasaki M, Isshiki K, Araki S, Sugimoto T, Haneda M, Kashiwagi A, Koya D (2010) Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest 120(4):1043–1055PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Jeong SG, Cho GW (2015) Trichostatin A modulates intracellular reactive oxygen species through SOD2 and FOXO1 in human bone marrow-mesenchymal stem cells. Cell Biochem Funct 33(1):37–43PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    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(5):540–553PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447(7145):725–729PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, Hur JH, Ansari WS, Lo T Jr, Jones DL, Walker DW (2011) Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell metabolism 14(5):623–634PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Chen C, Liu Y, Liu Y, Zheng P (2009) mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Science signaling 2(98):ra75PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, Larsen CP, Ahmed R (2009) mTOR regulates memory CD8 T-cell differentiation. Nature 460(7251):108–112PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Jasper H, Jones DL (2010) Metabolic regulation of stem cell behavior and implications for aging. Cell metabolism 12(6):561–565PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Igarashi M, Guarente L (2016) mTORC1 and SIRT1 cooperate to foster expansion of gut adult stem cells during calorie restriction. Cell 166(2):436–450PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Kim W, Jang YG, Yang J, Chung J (2017) Spatial activation of TORC1 is regulated by hedgehog and E2F1 signaling in the drosophila eye. Developmental cell 42(4):363-375.e364CrossRefGoogle Scholar
  101. 101.
    Fontana L, Partridge L (2015) Promoting health and longevity through diet: from model organisms to humans. Cell 161(1):106–118PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. The Biochemical journal 404(1):1–13PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Chen J, Astle CM, Harrison DE (2003) Hematopoietic senescence is postponed and hematopoietic stem cell function is enhanced by dietary restriction. Experimental hematology 31(11):1097–1103PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Yilmaz OH, Katajisto P, Lamming DW, Gultekin Y, Bauer-Rowe KE, Sengupta S, Birsoy K, Dursun A, Yilmaz VO, Selig M, Nielsen GP, Mino-Kenudson M, Zukerberg LR, Bhan AK, Deshpande V, Sabatini DM (2012) mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486(7404):490–495PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Wen L, Chen Z, Zhang F, Cui X, Sun W, Geary GG, Wang Y, Johnson DA, Zhu Y, Chien S, Shyy JY (2013) Ca2+/calmodulin-dependent protein kinase kinase beta phosphorylation of Sirtuin 1 in endothelium is atheroprotective. Proceedings of the National Academy of Sciences of the United States of America 110(26):E2420–E2427PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M, Yamaguchi M, Namiki S, Nakayama R, Tabata M, Ogata H, Kubota N, Takamoto I, Hayashi YK, Yamauchi N, Waki H, Fukayama M, Nishino I, Tokuyama K, Ueki K, Oike Y, Ishii S, Hirose K, Shimizu T, Touhara K, Kadowaki T (2010) Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 464(7293):1313–1319PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Ahn MJ, Cho GW (2017) Metformin promotes neuronal differentiation and neurite outgrowth through AMPK activation in human bone marrow-mesenchymal stem cells. Biotechnol Appl Biochem 64(6):836–842PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Neumann B, Baror R, Zhao C, Segel M, Dietmann S, Rawji KS, Foerster S, McClain CR, Chalut K, van Wijngaarden P, Franklin RJM (2019) Metformin restores CNS remyelination capacity by rejuvenating aged stem cells. Cell Stem Cell 25(4):473-485.e478CrossRefGoogle Scholar
  109. 109.
    Hong S, Zhao B, Lombard DB, Fingar DC, Inoki K (2014) Cross-talk between sirtuin and mammalian target of rapamycin complex 1 (mTORC1) signaling in the regulation of S6 kinase 1 (S6K1) phosphorylation. The Journal of biological chemistry 289(19):13132–13141PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Safaeinejad Z, Nabiuni M, Peymani M, Ghaedi K, Nasr-Esfahani MH, Baharvand H (2017) Resveratrol promotes human embryonic stem cells self-renewal by targeting SIRT1-ERK signaling pathway. European journal of cell biology 96(7):665–672PubMedCrossRefGoogle Scholar
  111. 111.
    Joe IS, Jeong SG, Cho GW (2015) Resveratrol-induced SIRT1 activation promotes neuronal differentiation of human bone marrow mesenchymal stem cells. Neurosci Lett 584:97–102PubMedCrossRefGoogle Scholar
  112. 112.
    Jang J, Huh YJ, Cho HJ, Lee B, Park J, Hwang DY, Kim DW (2017) SIRT1 enhances the survival of human embryonic stem cells by promoting DNA repair. Stem cell reports 9(2):629–641PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biology, College of Natural SciencesChosun UniversityDong-guKorea
  2. 2.Department of Life Science, BK21-Plus Research Team for Bioactive Control TechnologyChosun UniversityGwangjuKorea
  3. 3.Department of OtolaryngologyChonnam National University Medical SchoolGwangjuKorea

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