The PI3K-Akt pathway inhibits senescence and promotes self-renewal of human skin-derived precursors in vitro

Aging Cell

Volumn 10, Issue 4, 2011, Pages 661-674

  Liu, Shuang ^a,b   Liu, Shu ^a,b   Wang, Xinyue ^a,b   Zhou, Jiaxi ^c   Cao, Yujing ^a   Wang, Fei ^d   Duan, Enkui ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Adult stem cells; Cellular senescence; PI3K Akt; PTEN; Self renewal; Skin derived precursors

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MICROENVIRONMENT; MOUSE; NONHUMAN; PRECURSOR; PREPUCE; PRIORITY JOURNAL; REGENERATIVE MEDICINE; SENESCENCE; SKIN; STEM CELL;

CELL AGING; CELL DIFFERENTIATION; CELLS, CULTURED; FORKHEAD TRANSCRIPTION FACTORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MULTIPOTENT STEM CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SKIN;

EID: 79960322433     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2011.00704.x     Document Type: Article

References (37)

1. Beausejour CM, Krtolica A, Galimi F, Narita M, Lowe SW, Yaswen P, Campisi J (2003) Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J. 22, 4212-4222.
2. Ben-Porath I, Weinberg RA (2005) The signals and pathways activating cellular senescence. Int. J. Biochem. Cell Biol. 37, 961-976.
3. Biernaskie J, Paris M, Morozova O, Fagan BM, Marra M, Pevny L, Miller FD (2009) SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 5, 610-623.
4. Campisi J, d'Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8, 729-740.
5. Collado M, Medema RH, Garcia-Cao I, Dubuisson ML, Barradas M, Glassford J, Rivas C, Burgering BM, Serrano M, Lam EW (2000) Inhibition of the phosphoinositide 3-kinase pathway induces a senescence-like arrest mediated by p27Kip1. J. Biol. Chem. 275, 21960-21968.
6. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, Li W, Weng Z, Chen J, Ni S, Chen K, Li Y, Liu X, Xu J, Zhang S, Li F, He W, Labuda K, Song Y, Peterbauer A, Wolbank S, Redl H, Zhong M, Cai D, Zeng L, Pei D (2010) Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6, 71-79.
7. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabe-Heider F, Biernaskie J, Junek A, Kobayashi NR, Toma JG, Kaplan DR, Labosky PA, Rafuse V, Hui CC, Miller FD (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat. Cell Biol. 6, 1082-1093.
8. Gago N, Perez-Lopez V, Sanz-Jaka JP, Cormenzana P, Eizaguirre I, Bernad A, Izeta A (2009) Age-dependent depletion of human skin-derived progenitor cells. Stem Cells 27, 1164-1172.
9. Garkavtsev I, Hull C, Riabowol K (1998) Molecular aspects of the relationship between cancer and aging: tumor suppressor activity during cellular senescence. Exp. Gerontol. 33, 81-94.
10. Gregorian C, Nakashima J, Le Belle J, Ohab J, Kim R, Liu A, Smith KB, Groszer M, Garcia AD, Sofroniew MV, Carmichael ST, Kornblum HI, Liu X, Wu H (2009) Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. J. Neurosci. 29, 1874-1886.
11. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, Liu X, Wu H (2001) Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186-2189.
12. Groszer M, Erickson R, Scripture-Adams DD, Dougherty JD, Le Belle J, Zack JA, Geschwind DH, Liu X, Kornblum HI, Wu H (2006) PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc. Natl. Acad. Sci. U S A 103, 111-116.
13. Guo W, Miao C, Liu S, Qiu Z, Li J, Duan E (2009) Efficient differentiation of insulin-producing cells from skin-derived stem cells. Cell Prolif. 42, 49-62.
14. Han EK, Ng SC, Arber N, Begemann M, Weinstein IB (1999) Roles of cyclin D1 and related genes in growth inhibition, senescence and apoptosis. Apoptosis 4, 213-219.
15. Herbig U, Jobling WA, Chen BP, Chen DJ, Sedivy JM (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14, 501-513.
16. Hunt DP, Morris PN, Sterling J, Anderson JA, Joannides A, Jahoda C, Compston A, Chandran S (2008) A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26, 163-172.
17. Inoue-Narita T, Hamada K, Sasaki T, Hatakeyama S, Fujita S, Kawahara K, Sasaki M, Kishimoto H, Eguchi S, Kojima I, Beermann F, Kimura T, Osawa M, Itami S, Mak TW, Nakano T, Manabe M, Suzuki A (2008) Pten deficiency in melanocytes results in resistance to hair graying and susceptibility to carcinogen-induced melanomagenesis. Cancer Res. 68, 5760-5768.
18. Janzen V, Forkert R, Fleming HE, Saito Y, Waring MT, Dombkowski DM, Cheng T, DePinho RA, Sharpless NE, Scadden DT (2006) Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 443, 421-426.
19. Jinno H, Morozova O, Jones KL, Biernaskie JA, Paris M, Hosokawa R, Rudnicki MA, Chai Y, Rossi F, Marra MA, Miller FD (2010) Convergent genesis of an adult neural crest-like dermal stem cell from distinct developmental origins. Stem Cells 28, 2027-2040.
20. Joannides A, Gaughwin P, Schwiening C, Majed H, Sterling J, Compston A, Chandran S (2004) Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet 364, 172-178.
21. Karlseder J, Smogorzewska A, de Lange T (2002) Senescence induced by altered telomere state, not telomere loss. Science 295, 2446-2449.
22. Le LQ, Shipman T, Burns DK, Parada LF (2009) Cell of origin and microenvironment contribution for NF1-associated dermal neurofibromas. Cell Stem Cell 4, 453-463.
23. Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, Duan EK, Hsueh AJ (2010) Activation of dormant ovarian follicles to generate mature eggs. Proc. Natl. Acad. Sci. U S A 101, 10280-10284.
24. Murayama K, Kimura T, Tarutani M, Tomooka M, Hayashi R, Okabe M, Nishida K, Itami S, Katayama I, Nakano T (2007) Akt activation induces epidermal hyperplasia and proliferation of epidermal progenitors. Oncogene 26, 4882-4888.
25. Nogueira V, Park Y, Chen CC, Xu PZ, Chen ML, Tonic I, Unterman T, Hay N (2008) Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 14, 458-470.
26. Paling NR, Wheadon H, Bone HK, Welham MJ (2004) Regulation of embryonic stem cell self-renewal by phosphoinositide 3-kinase-dependent signaling. J. Biol. Chem. 279, 48063-48070.
27. Qiu Z, Miao C, Li J, Lei X, Liu S, Guo W, Cao Y, Duan EK (2010) Skeletal myogenic potential of mouse skin-derived precursors. Stem Cells Dev. 19, 259-268.
28. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, Jansen-Dürr P, Wlaschek M (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5, 379-389.
29. Rosivatz E, Matthews JG, McDonald NQ, Mulet X, Ho KK, Lossi N, Schmid AC, Mirabelli M, Pomeranz KM, Erneux C, Lam EW, Vilar R, Woscholski R (2006) A small molecule inhibitor for phosphatase and tensin homologue deleted on chromosome 10 (PTEN). ACS Chem. Biol. 1, 780-790.
30. Sahin E, DePinho RA (2010) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464, 520-528.
31. Sinor AD, Lillien L (2004) Akt-1 expression level regulates CNS precursors. J. Neurosci. 24, 8531-8541.
32. Su X, Paris M, Gi YJ, Tsai KY, Cho MS, Lin YL, Biernaskie JA, Sinha S, Prives C, Pevny LH, Miller FD, Flores ER (2009) TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 5, 64-75.
33. Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 3, 778-784.
34. Toma JG, McKenzie IA, Bagli D, Miller FD (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23, 727-737.
35. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, Igelmann H, Lu X, Soron G, Cooper B, Brayton C, Hee Park S, Thompson T, Karsenty G, Bradley A, Donehower LA (2002) p53 mutant mice that display early ageing-associated phenotypes. Nature 415, 45-53.
36. Watanabe S, Umehara H, Murayama K, Okabe M, Kimura T, Nakano T (2006) Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene 25, 2697-2707.
37. Zhu Y, Parada LF (2002) The molecular and genetic basis of neurological tumours. Nat. Rev. Cancer 2, 616-626.