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

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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.

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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

References

  1. Barzilai N, Huffman DM, Muzumdar RH, Bartke A (2012) The critical role of metabolic pathways in aging. Diabetes 61(6):1315–1322

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153(6):1194–1217

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Hoggatt J, Scadden DT (2012) The stem cell niche: tissue physiology at a single cell level. J Clin Invest 122(9):3029–3034

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Li L, Xie T (2005) Stem cell niche: structure and function. Annual review of cell and developmental biology 21:605–631

    CAS  PubMed  Google Scholar 

  5. Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nature reviews Molecular cell biology 14(6):329–340

    CAS  PubMed  Google Scholar 

  6. Wagers AJ (2012) The stem cell niche in regenerative medicine. Cell stem cell 10(4):362–369

    CAS  PubMed  Google Scholar 

  7. Rezza A, Sennett R, Rendl M (2014) Adult stem cell niches: cellular and molecular components. Current topics in developmental biology 107:333–372

    CAS  PubMed  Google Scholar 

  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):201–204

    CAS  Google Scholar 

  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 8:14063

    CAS  PubMed  PubMed Central  Google Scholar 

  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):5779

    PubMed  PubMed Central  Google Scholar 

  11. Bales CW, Kraus WE (2013) Caloric restriction: implications for human cardiometabolic health. Journal of cardiopulmonary rehabilitation and prevention 33(4):201–208

    PubMed  PubMed Central  Google Scholar 

  12. Roth GS, Lane MA, Ingram DK (2005) Caloric restriction mimetics: the next phase. Ann N Y Acad Sci 1057:365–371

    CAS  PubMed  Google Scholar 

  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 1019:412–423

    CAS  PubMed  Google Scholar 

  14. Oh J, Lee YD, Wagers AJ (2014) Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nature medicine 20(8):870–880

    CAS  PubMed  PubMed Central  Google Scholar 

  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):287–296

    CAS  PubMed  Google Scholar 

  16. Liu L, Rando TA (2011) Manifestations and mechanisms of stem cell aging. The Journal of cell biology 193(2):257–266

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Burtner CR, Kennedy BK (2010) Progeria syndromes and ageing: what is the connection? Nature reviews Molecular cell biology 11(8):567–578

    CAS  PubMed  Google Scholar 

  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):1109–1112

    CAS  Google Scholar 

  20. Pervaiz S, Taneja R, Ghaffari S (2009) Oxidative stress regulation of stem and progenitor cells. Antioxidants & redox signaling 11(11):2777–2789

    CAS  Google Scholar 

  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):997–1002

    CAS  PubMed  Google Scholar 

  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):1197–1208

    CAS  PubMed  PubMed Central  Google Scholar 

  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):1865–1873

    CAS  Google Scholar 

  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):323–327

    CAS  PubMed  PubMed Central  Google Scholar 

  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):455–467

    CAS  PubMed  PubMed Central  Google Scholar 

  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 78:959–991

    CAS  PubMed  Google Scholar 

  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):319–327

    CAS  PubMed  Google Scholar 

  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):852–859

    CAS  Google Scholar 

  29. Watt FM, Huck WT (2013) Role of the extracellular matrix in regulating stem cell fate. Nature reviews Molecular cell biology 14(8):467–473

    CAS  PubMed  Google Scholar 

  30. Wang LD, Wagers AJ (2011) Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nature reviews Molecular cell biology 12(10):643–655

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Lane SW, Williams DA, Watt FM (2014) Modulating the stem cell niche for tissue regeneration. Nature biotechnology 32(8):795–803

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Wei Q, Frenette PS (2018) Niches for hematopoietic stem cells and their progeny. Immunity 48(4):632–648

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Crane GM, Jeffery E, Morrison SJ (2017) Adult haematopoietic stem cell niches. Nature reviews Immunology 17(9):573–590

    CAS  PubMed  Google Scholar 

  34. Morrison SJ, Scadden DT (2014) The bone marrow niche for haematopoietic stem cells. Nature 505(7483):327–334

    CAS  PubMed  PubMed Central  Google Scholar 

  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):4815–4828

    CAS  PubMed  Google Scholar 

  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):470–478

    CAS  PubMed  Google Scholar 

  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):4633–4638

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nature reviews Molecular cell biology 15(1):19–33

    CAS  PubMed  Google Scholar 

  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):415–418

    CAS  PubMed  Google Scholar 

  40. Porter EM, Bevins CL, Ghosh D, Ganz T (2002) The multifaceted Paneth cell. Cellular and molecular life sciences : CMLS 59(1):156–170

    CAS  PubMed  Google Scholar 

  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):134–144

    CAS  PubMed  Google Scholar 

  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):637–640

    Google Scholar 

  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):458–469

    CAS  PubMed  Google Scholar 

  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):1651–1657

    CAS  PubMed  Google Scholar 

  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.e1517

    Google Scholar 

  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):959–963

    PubMed  Google Scholar 

  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):1684–1686

    CAS  Google Scholar 

  48. Goodman SL, Picard M (2012) Integrins as therapeutic targets. Trends in pharmacological sciences 33(7):405–412

    CAS  PubMed  Google Scholar 

  49. Zutter MM (2007) Integrin-mediated adhesion: tipping the balance between chemosensitivity and chemoresistance. Advances in experimental medicine and biology 608:87–100

    CAS  PubMed  Google Scholar 

  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):518–528

    CAS  PubMed  PubMed Central  Google Scholar 

  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):760–764

    CAS  PubMed  Google Scholar 

  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):397–409

    CAS  PubMed  Google Scholar 

  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):1575–1577

    CAS  Google Scholar 

  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):1505–1511

    CAS  Google Scholar 

  55. Chakkalakal JV, Jones KM, Basson MA, Brack AS (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490(7420):355–360

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Ito K, Suda T (2014) Metabolic requirements for the maintenance of self-renewing stem cells. Nature reviews Molecular cell biology 15(4):243–256

    CAS  PubMed  PubMed Central  Google Scholar 

  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):380–390

    CAS  PubMed  PubMed Central  Google Scholar 

  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):150–161

    CAS  PubMed  Google Scholar 

  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):5597–5608

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Li L, Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science (New York, NY) 327(5965):542–545

    CAS  Google Scholar 

  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):232–236

    CAS  PubMed  PubMed Central  Google Scholar 

  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):2392–2403

    CAS  PubMed  Google Scholar 

  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.e805

    Google Scholar 

  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):29–38

    PubMed  Google Scholar 

  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):108–116

    CAS  PubMed  Google Scholar 

  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):311–319

    CAS  PubMed  Google Scholar 

  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.e320

    Google Scholar 

  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):515–519

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Bar-Peled L, Sabatini DM (2014) Regulation of mTORC1 by amino acids. Trends in cell biology 24(7):400–406

    CAS  PubMed  PubMed Central  Google Scholar 

  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):1196–1208

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Orentreich N, Matias JR, DeFelice A, Zimmerman JA (1993) Low methionine ingestion by rats extends life span. The Journal of nutrition 123(2):269–274

    CAS  PubMed  Google Scholar 

  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):29–39

    CAS  Google Scholar 

  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):119–125

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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):103–114

    CAS  PubMed  Google Scholar 

  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):746–756

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Laplante M, Sabatini DM (2009) mTOR signaling at a glance. Journal of cell science 122(Pt 20):3589–3594

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  79. Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115(5):577–590

    CAS  PubMed  Google Scholar 

  80. Kadowaki T, Ueki K, Yamauchi T, Kubota N (2012) SnapShot: insulin signaling pathways. Cell 148(3):624, 624.e621

    Google Scholar 

  81. Soulard A, Hall MN (2007) SnapShot: mTOR signaling. Cell 129(2):434

    PubMed  Google Scholar 

  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):200–205

    CAS  PubMed  Google Scholar 

  83. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span--from yeast to humans. Science (New York, NY) 328(5976):321–326

    CAS  Google Scholar 

  84. Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512

    CAS  PubMed  Google Scholar 

  85. Guarente L, Picard F (2005) Calorie restriction--the SIR2 connection. Cell 120(4):473–482

    CAS  PubMed  Google Scholar 

  86. Webb AE, Kundaje A, Brunet A (2016) Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging cell 15(4):673–685

    CAS  PubMed  PubMed Central  Google Scholar 

  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 2017:3494289

    PubMed  PubMed Central  Google Scholar 

  88. Eijkelenboom A, Burgering BM (2013) FOXOs: signalling integrators for homeostasis maintenance. Nature reviews Molecular cell biology 14(2):83–97

    CAS  PubMed  Google Scholar 

  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):1–14

    PubMed  Google Scholar 

  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):335–341

    CAS  PubMed  Google Scholar 

  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):1043–1055

    CAS  PubMed  PubMed Central  Google Scholar 

  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):37–43

    CAS  PubMed  Google Scholar 

  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):540–553

    CAS  PubMed  PubMed Central  Google Scholar 

  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):725–729

    CAS  PubMed  Google Scholar 

  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):623–634

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Chen C, Liu Y, Liu Y, Zheng P (2009) mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Science signaling 2(98):ra75

    PubMed  PubMed Central  Google Scholar 

  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):108–112

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Jasper H, Jones DL (2010) Metabolic regulation of stem cell behavior and implications for aging. Cell metabolism 12(6):561–565

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Igarashi M, Guarente L (2016) mTORC1 and SIRT1 cooperate to foster expansion of gut adult stem cells during calorie restriction. Cell 166(2):436–450

    CAS  PubMed  Google Scholar 

  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.e364

    Google Scholar 

  101. Fontana L, Partridge L (2015) Promoting health and longevity through diet: from model organisms to humans. Cell 161(1):106–118

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. The Biochemical journal 404(1):1–13

    CAS  PubMed  Google Scholar 

  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):1097–1103

    CAS  PubMed  Google Scholar 

  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):490–495

    CAS  PubMed  PubMed Central  Google Scholar 

  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–E2427

    CAS  PubMed  PubMed Central  Google Scholar 

  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):1313–1319

    CAS  PubMed  Google Scholar 

  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):836–842

    CAS  PubMed  Google Scholar 

  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.e478

    Google Scholar 

  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):13132–13141

    CAS  PubMed  PubMed Central  Google Scholar 

  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):665–672

    CAS  PubMed  Google Scholar 

  111. Joe IS, Jeong SG, Cho GW (2015) Resveratrol-induced SIRT1 activation promotes neuronal differentiation of human bone marrow mesenchymal stem cells. Neurosci Lett 584:97–102

    CAS  PubMed  Google Scholar 

  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):629–641

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

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

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Authors and Affiliations

  1. Department of Biology, College of Natural Sciences, Chosun University, 309 Pilmun-daero, Dong-gu, GwangJu, 501-759, Korea

    Nagarajan Maharajan, Karthikeyan Vijayakumar & Goang-Won Cho

  2. Department of Life Science, BK21-Plus Research Team for Bioactive Control Technology, Chosun University, Gwangju, 61452, Korea

    Nagarajan Maharajan, Karthikeyan Vijayakumar & Goang-Won Cho

  3. Department of Otolaryngology, Chonnam National University Medical School, Gwangju, 61469, Korea

    Chul Ho Jang

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  1. Nagarajan Maharajan
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  2. Karthikeyan Vijayakumar
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  3. Chul Ho Jang
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  4. Goang-Won Cho
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Correspondence to Goang-Won Cho.

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Maharajan, N., Vijayakumar, K., Jang, C.H. et al. Caloric restriction maintains stem cells through niche and regulates stem cell aging. J Mol Med 98, 25–37 (2020). https://doi.org/10.1007/s00109-019-01846-1

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  • DOI: https://doi.org/10.1007/s00109-019-01846-1

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