Resveratrol prevents oxidative stress-induced senescence and proliferative dysfunction by activating the AMPK-FOXO3 cascade in cultured primary human keratinocytes

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Ido, Yasuo ^a   Duranton, Albert ^b   Lan, Fan ^c   Weikel, Karen A ^a   Breton, Lionel ^b   Ruderman, Neil B ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b L ORÉAL RECHERCHE   (France)

^c CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; RESVERATROL; SIRTUIN; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; SIRT1 PROTEIN, HUMAN; STILBENE DERIVATIVE;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DRUG ACTIVITY; ENZYME ACTIVITY; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; OXIDATIVE STRESS; PHENOTYPE; SENESCENCE; ADULT; CELL AGING; CYTOLOGY; DRUG EFFECTS; ENZYME ACTIVATION; INFANT; METABOLISM; MIDDLE AGED; SIGNAL TRANSDUCTION;

ADULT; AMP-ACTIVATED PROTEIN KINASES; CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; ENZYME ACTIVATION; FORKHEAD BOX PROTEIN O3; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; HYDROGEN PEROXIDE; INFANT; KERATINOCYTES; MIDDLE AGED; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SIRTUIN 1; STILBENES;

EID: 84922384237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115341     Document Type: Article

References (77)

1. Wallace DC (2010) Bioenergetics and the epigenome: interface between the environment and genes in common diseases. Dev Disabil Res Rev 16: 114-119. doi: 10.1002/ddrr.113 PMID: 20818725
2. Garg D, Cohen SM (2014) miRNAs and aging: A genetic perspective. Ageing Res Rev.
3. Waaijer ME, Parish WE, Strongitharm BH, van Heemst D, Slagboom PE, et al. (2012) The number of p16INK4a positive cells in human skin reflects biological age. Aging Cell 11: 722-725. doi: 10.1111/j. 1474-9726.2012.00837.x PMID: 22612594
4. Dimri GP, Lee X, Basile G, Acosta M, Scott G, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92: 9363-9367. PMID: 7568133
5. Jeyapalan JC, Sedivy JM (2008) Cellular senescence and organismal aging. Mech Ageing Dev 129: 467-474. doi: 10.1016/j.mad.2008.04.001 PMID: 18502472
6. Cordisco S, Maurelli R, Bondanza S, Stefanini M, Zambruno G, et al. (2010) Bmi-1 reduction plays a key role in physiological and premature aging of primary human keratinocytes. J Invest Dermatol 130: 1048-1062. doi: 10.1038/jid.2009.355 PMID: 19907431
7. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, et al. (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5: 379-389. PMID: 16911562
8. Gunschmann C, Stachelscheid H, Akyuz MD, Schmitz A, Missero C, et al. (2013) Insulin/IGF-1 controls epidermal morphogenesis via regulation of FoxO-mediated p63 inhibition. Dev Cell 26: 176-187. doi: 10.1016/j.devcel.2013.05.017 PMID: 23906066
9. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460. PMID: 15734678
10. Ruderman NB, Carling D, Prentki M, Cacicedo JM (2013) AMPK, insulin resistance, and the metabolic syndrome. J Clin Invest 123: 2764-2772. doi: 10.1172/JCI67227 PMID: 23863634
11. Corbi G, Conti V, Russomanno G, Longobardi G, Furgi G, et al. (2013) Adrenergic signaling and oxidative stress: a role for sirtuins? Front Physiol 4: 324. doi: 10.3389/fphys.2013.00324 PMID: 24265619
12. Frojdo S, Durand C, Molin L, Carey AL, El-Osta A, et al. (2011) Phosphoinositide 3-kinase as a novel functional target for the regulation of the insulin signaling pathway by SIRT1. Mol Cell Endocrinol 335: 166-176. doi: 10.1016/j.mce.2011.01.008 PMID: 21241768
13. Salminen A, Hyttinen JM, Kaarniranta K (2011) AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan. J Mol Med (Berl) 89: 667-676. doi: 10.1007/s00109-011-0748-0 PMID: 21431325
14. Tullet JM, Araiz C, Sanders MJ, Au C, Benedetto A, et al. (2014) DAF-16/FoxO directly regulates an atypical AMP-activated protein kinase gamma isoform to mediate the effects of insulin/IGF-1 signaling on aging in Caenorhabditis elegans. PLoS Genet 10: e1004109. doi: 10.1371/journal.pgen.1004109 PMID: 24516399
15. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, et al. (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458: 1056-1060. doi: 10.1038/nature07813 PMID: 19262508
16. Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, et al. (2013) A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci 70: 2015-2029. doi: 10.1007/s00018-012-1244-6 PMID: 23283301
17. Chiacchiera F, Simone C (2010) The AMPK-FoxO3A axis as a target for cancer treatment. Cell Cycle 9: 1091-1096. PMID: 20190568
18. Flachsbart F, Caliebe A, Kleindorp R, Blanche H, von Eller-Eberstein H, et al. (2009) Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc Natl Acad Sci U S A 106: 2700-2705. doi: 10.1073/pnas.0809594106 PMID: 19196970
19. Webb AE, Brunet A (2013) FOXO flips the longevity SWItch. Nat Cell Biol 15: 444-446. doi: 10.1038/ncb2749 PMID: 23636422
20. Soerensen M, Dato S, Christensen K, McGue M, Stevnsner T, et al. (2010) Replication of an association of variation in the FOXO3A gene with human longevity using both case-control and longitudinal data. Aging Cell 9: 1010-1017. doi: 10.1111/j.1474-9726.2010.00627.x PMID: 20849522
21. Iglesias-Bartolome R, Patel V, Cotrim A, Leelahavanichkul K, Molinolo AA, et al. (2012) mTOR inhibition prevents epithelial stem cell senescence and protects from radiation-induced mucositis. Cell Stem Cell 11: 401-414. doi: 10.1016/j.stem.2012.06.007 PMID: 22958932
22. Ido Y, Duranton A, Lan F, Cacicedo JM, Chen TC, et al. (2012) Acute activation of AMP-activated protein kinase prevents H2O2-induced premature senescence in primary human keratinocytes. PLoS One 7: e35092. doi: 10.1371/journal.pone.0035092 PMID: 22514710
23. Velarde MC, Flynn JM, Day NU, Melov S, Campisi J (2012) Mitochondrial oxidative stress caused by Sod2 deficiency promotes cellular senescence and aging phenotypes in the skin. Aging (Albany NY) 4: 3-12.
24. Melov S, Ravenscroft J, Malik S, Gill MS, Walker DW, et al. (2000) Extension of life-span with superoxide dismutase/catalase mimetics. Science 289: 1567-1569. PMID: 10968795
25. Suchankova G, Nelson LE, Gerhart-Hines Z, Kelly M, Gauthier MS, et al. (2009) Concurrent regulation of AMP-activated protein kinase and SIRT1 in mammalian cells. Biochem Biophys Res Commun 378: 836-841. doi: 10.1016/j.bbrc.2008.11.130 PMID: 19071085
26. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, et al. (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191-196. PMID: 12939617
27. Cacicedo JM, Yagihashi N, Keaney JF Jr., Ruderman NB, Ido Y (2004) AMPK inhibits fatty acid-induced increases in NF-kappaB transactivation in cultured human umbilical vein endothelial cells. Biochem Biophys Res Commun 324: 1204-1209. PMID: 15504342
28. Lan F, Cacicedo JM, Ruderman N, Ido Y (2008) SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem 283: 27628-27635. doi: 10.1074/jbc.M805711200 PMID: 18687677
29. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-342. PMID: 17086191
30. Nelson LE, Valentine RJ, Cacicedo JM, Gauthier MS, Ido Y, et al. (2012) A novel inverse relationship between metformin-triggered AMPK-SIRT1 signaling and p53 protein abundance in high glucoseexposed HepG2 cells. Am J Physiol Cell Physiol 303: C4-C13. doi: 10.1152/ajpcell.00296.2011 PMID: 22378745
31. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, et al. (2012) SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab 15: 675-690. doi: 10.1016/j.cmet.2012.04.003 PMID: 22560220
32. Ruderman NB, Xu XJ, Nelson L, Cacicedo JM, Saha AK, et al. (2010) AMPK and SIRT1: a longstanding partnership? Am J Physiol Endocrinol Metab 298: E751-760. doi: 10.1152/ajpendo.00745. 2009 PMID: 20103737
33. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr., et al. (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296: 530-534. PMID: 11964479
34. Bulow MH, Bulow TR, Hoch M, Pankratz MJ, Junger MA (2014) Src tyrosine kinase signaling antagonizes nuclear localization of FOXO and inhibits its transcription factor activity. Sci Rep 4: 4048. doi: 10.1038/srep04048 PMID: 24513978
35. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015. PMID: 14976264
36. Beerman I, Bock C, Garrison BS, Smith ZD, Gu H, et al. (2013) Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell Stem Cell 12: 413-425. doi: 10.1016/j.stem.2013.01.017 PMID: 23415915
37. Jiang H, Shang X, Wu H, Huang G, Wang Y, et al. (2010) Combination treatment with resveratrol and sulforaphane induces apoptosis in human U251 glioma cells. Neurochem Res 35: 152-161. doi: 10.1007/s11064-009-0040-7 PMID: 19685289
38. Castino R, Pucer A, Veneroni R, Morani F, Peracchio C, et al. (2011) Resveratrol reduces the invasive growth and promotes the acquisition of a long-lasting differentiated phenotype in human glioblastoma cells. J Agric Food Chem 59: 4264-4272. doi: 10.1021/jf104917q PMID: 21395220
39. Dai Z, Li Y, Quarles LD, Song T, Pan W, et al. (2007) Resveratrol enhances proliferation and osteoblastic differentiation in human mesenchymal stem cells via ER-dependent ERK1/2 activation. Phytomedicine 14: 806-814. PMID: 17689939
40. Peltz L, Gomez J, Marquez M, Alencastro F, Atashpanjeh N, et al. (2012) Resveratrol exerts dosage and duration dependent effect on human mesenchymal stem cell development. PLoS One 7: e37162. doi: 10.1371/journal.pone.0037162 PMID: 22615926
41. Song LH, Pan W, Yu YH, Quarles LD, Zhou HH, et al. (2006) Resveratrol prevents CsA inhibition of proliferation and osteoblastic differentiation of mouse bone marrow-derived mesenchymal stem cells through an ER/NO/cGMP pathway. Toxicol In Vitro 20: 915-922. PMID: 16524694
42. Yu CC, Woods AL, Levison DA (1992) The assessment of cellular proliferation by immunohistochemistry: a review of currently available methods and their applications. Histochem J 24: 121-131. PMID: 1349881
43. Hibino T, Matsuda Y, Takahashi T, Goetinck PF (1999) Suppression of keratinocyte proliferation by plasminogen activator inhibitor-2. J Invest Dermatol 112: 85-90. PMID: 9886269
44. Shen S, Alt A, Wertheimer E, Gartsbein M, Kuroki T, et al. (2001) PKCdelta activation: a divergence point in the signaling of insulin and IGF-1-induced proliferation of skin keratinocytes. Diabetes 50: 255-264. PMID: 11272134
45. Hou X, Xu S, Maitland-Toolan KA, Sato K, Jiang B, et al. (2008) SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J Biol Chem 283: 20015-20026. doi: 10.1074/jbc.M802187200 PMID: 18482975
46. Warren R, Gartstein V, Kligman AM, Montagna W, Allendorf RA, et al. (1991) Age, sunlight, and facial skin: a histologic and quantitative study. J Am Acad Dermatol 25: 751-760. PMID: 1802896
47. Christensen K, Thinggaard M, McGue M, Rexbye H, Hjelmborg JV, et al. (2009) Perceived age as clinically useful biomarker of ageing: cohort study. BMJ 339: b5262. PMID: 20008378
48. Gunn DA, de Craen AJ, Dick JL, Tomlin CC, van Heemst D, et al. (2013) Facial appearance reflects human familial longevity and cardiovascular disease risk in healthy individuals. J Gerontol A Biol Sci Med Sci 68: 145-152. doi: 10.1093/gerona/gls154 PMID: 22879455
49. Vierkotter A, Krutmann J (2012) Environmental influences on skin aging and ethnic-specific manifestations. Dermatoendocrinol 4: 227-231. doi: 10.4161/derm.19858 PMID: 23467702
50. Gunn DA, Rexbye H, Griffiths CE, Murray PG, Fereday A, et al. (2009) Why some women look young for their age. PLoS One 4: e8021. doi: 10.1371/journal.pone.0008021 PMID: 19956599
51. Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8: 113-127. doi: 10.1111/j.1474-9726. 2009.00459.x PMID: 19239417
52. Um JH, Park SJ, Kang H, Yang S, Foretz M, et al. (2010) AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59: 554-563. doi: 10.2337/db09-0482 PMID: 19934007
53. Tanno M, Sakamoto J, Miura T, Shimamoto K, Horio Y (2007) Nucleocytoplasmic shuttling of the NAD +-dependent histone deacetylase SIRT1. J Biol Chem 282: 6823-6832. PMID: 17197703
54. Pirinen E, Lo Sasso G, Auwerx J (2012) Mitochondrial sirtuins and metabolic homeostasis. Best Pract Res Clin Endocrinol Metab 26: 759-770. doi: 10.1016/j.beem.2012.05.001 PMID: 23168278
55. Senoo M (2013) Epidermal Stem Cells in Homeostasis and Wound Repair of the Skin. Adv Wound Care (New Rochelle) 2: 273-282. PMID: 24527349
56. Paris M, Rouleau M, Puceat M, Aberdam D (2012) Regulation of skin aging and heart development by TAp63. Cell Death Differ 19: 186-193. doi: 10.1038/cdd.2011.181 PMID: 22158419
57. Zobiri O, Deshayes N, Rathman-Josserand M (2012) Evolution of the clonogenic potential of human epidermal stem/progenitor cells with age. Stem Cells Cloning 5: 1-4. doi: 10.2147/SCCAA.S28355 PMID: 24198533
58. Seoane J, Le HV, Shen L, Anderson SA, Massague J (2004) Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117: 211-223. PMID: 15084259
59. Gomis RR, Alarcon C, He W, Wang Q, Seoane J, et al. (2006) A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci U S A 103: 12747-12752. PMID: 16908841
60. Hori YS, Kuno A, Hosoda R, Horio Y (2013) Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS One 8: e73875. doi: 10.1371/journal.pone.0073875 PMID: 24040102
61. Mandinova A, Lefort K, Tommasi di Vignano A, Stonely W, Ostano P, et al. (2008) The FoxO3a gene is a key negative target of canonical Notch signalling in the keratinocyte UVB response. EMBO J 27: 1243-1254. doi: 10.1038/emboj.2008.45 PMID: 18388864
62. Warr MR, Binnewies M, Flach J, Reynaud D, Garg T, et al. (2013) FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 494: 323-327. doi: 10.1038/nature11895 PMID: 23389440
63. Winter MC, Bickenbach JR (2009) Aging epidermis is maintained by changes in transit-amplifying cell kinetics, not stem cell kinetics. J Invest Dermatol 129: 2541-2543. doi: 10.1038/jid.2009.236 PMID: 19826444
64. Franco SS, De Falco L, Ghaffari S, Brugnara C, Sinclair DA, et al. (2014) Resveratrol accelerates erythroid maturation by activation of FoxO3 and ameliorates anemia in beta-thalassemic mice. Haematologica 99: 267-275. doi: 10.3324/haematol.2013.090076 PMID: 23975182
65. Reznikova TV, Phillips MA, Patterson TJ, Rice RH (2010) Opposing actions of insulin and arsenite converge on PKCdelta to alter keratinocyte proliferative potential and differentiation. Mol Carcinog 49: 398-409. doi: 10.1002/mc.20612 PMID: 20082316
66. Puig O, Tjian R (2005) Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev 19: 2435-2446. PMID: 16230533
67. Stachelscheid H, Ibrahim H, Koch L, Schmitz A, Tscharntke M, et al. (2008) Epidermal insulin/IGF-1 signalling control interfollicular morphogenesis and proliferative potential through Rac activation. EMBO J 27: 2091-2101. doi: 10.1038/emboj.2008.141 PMID: 18650937
68. Coffer PJ, van Puijenbroek A, Burgering BM, Klop-de Jonge M, Koenderman L, et al. (1997) Insulin activates Stat3 independently of p21ras-ERK and PI-3K signal transduction. Oncogene 15: 2529-2539. PMID: 9399641
69. Boric M, Skopljanac I, Ferhatovic L, Jelicic Kadic A, Banozic A, et al. (2013) Reduced epidermal thickness, nerve degeneration and increased pain-related behavior in rats with diabetes type 1 and 2. J Chem Neuroanat 53: 33-40. doi: 10.1016/j.jchemneu.2013.10.001 PMID: 24126225
70. Jelicic Kadic A, Boric M, Vidak M, Ferhatovic L, Puljak L (2014) Changes in epidermal thickness and cutaneous innervation during maturation in long-term diabetes. J Tissue Viability 23: 7-12. doi: 10.1016/j. jtv.2013.11.002 PMID: 24361118
71. Giacomoni PU, Rein G (2004) A mechanistic model for the aging of human skin. Micron 35: 179-184. PMID: 15036272
72. Gilhar A, Ullmann Y, Karry R, Shalaginov R, Assy B, et al. (2004) Aging of human epidermis: reversal of aging changes correlates with reversal of keratinocyte fas expression and apoptosis. J Gerontol A Biol Sci Med Sci 59: 411-415. PMID: 15123749
73. Sen CK, Gordillo GM, Roy S, Kirsner R, Lambert L, et al. (2009) Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen 17: 763-771. doi: 10.1111/j.1524-475X.2009.00543.x PMID: 19903300
74. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, et al. (2008) FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A 105: 13987-13992. doi: 10.1073/pnas.0801030105 PMID: 18765803
75. Saha AK, Xu XJ, Balon TW, Brandon A, Kraegen EW, et al. (2011) Insulin resistance due to nutrient excess: is it a consequence of AMPK downregulation? Cell Cycle 10: 3447-3451. doi: 10.4161/cc.10.20. 17886 PMID: 22067655
76. Xu XJ, Gauthier MS, Hess DT, Apovian CM, Cacicedo JM, et al. (2012) Insulin sensitive and resistant obesity in humans: AMPK activity, oxidative stress, and depot-specific changes in gene expression in adipose tissue. J Lipid Res 53: 792-801. doi: 10.1194/jlr.P022905 PMID: 22323564
77. Kola B, Christ-Crain M, Lolli F, Arnaldi G, Giacchetti G, et al. (2008) Changes in adenosine 5'-monophosphate-activated protein kinase as a mechanism of visceral obesity in Cushing's syndrome. J Clin Endocrinol Metab 93: 4969-4973. doi: 10.1210/jc.2008-1297 PMID: 18782871