Senescence of human skin-derived precursors regulated by Akt-FOXO3-p27KIP1/p15INK4b signaling

详细信息    查看全文

• 作者：Shuang Liu ; Xinyue Wang ; Qian Zhao ; Shu Liu&#8230
• 关键词：Cellular senescence ; Skin ; derived precursors ; Akt ; p15INK4b ; p27KIP1 ; Adult stem cells
• 刊名：Cellular and Molecular Life Sciences (CMLS)
• 出版年：2015
• 出版时间：August 2015
• 年：2015
• 卷：72
• 期：15
• 页码：2949-2960
• 全文大小：5,843 KB
• 参考文献：1.Liu S, Zhang H, Duan E (2013) Epidermal development in mammals: key regulators, signals from beneath, and stem cells. Int J Mol Sci 14:10869鈥?0895. doi:10.鈥?390/鈥媔jms140610869 PubMed Central PubMed View Article
  2.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鈥?23. doi:10.鈥?016/鈥媕.鈥媠tem.鈥?009.鈥?0.鈥?19 PubMed Central PubMed View Article
  3.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鈥?68. doi:10.鈥?089/鈥媠cd.鈥?009.鈥?058 PubMed View Article
  4.Lavoie JF, Biernaskie JA, Chen Y, Bagli D, Alman B, Kaplan DR, Miller FD (2009) Skin-derived precursors differentiate into skeletogenic cell types and contribute to bone repair. Stem Cells Dev 18:893鈥?06. doi:10.鈥?089/鈥媠cd.鈥?008.鈥?260 PubMed View Article
  5.Biernaskie J, Sparling JS, Liu J, Shannon CP, Plemel JR, Xie Y, Miller FD, Tetzlaff W (2007) Skin-derived precursors generate myelinating Schwann cells that promote remyelination and functional recovery after contusion spinal cord injury. J Neurosci 27:9545鈥?559. doi:10.鈥?523/鈥婮NEUROSCI.鈥?930-07.鈥?007 PubMed View Article
  6.Toma JG, McKenzie IA, Bagli D, Miller FD (2005) Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727鈥?37. doi:10.鈥?634/鈥媠temcells.鈥?004-0134 PubMed View Article
  7.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鈥?172. doi:10.鈥?002/鈥媠tem.鈥?7 PubMed View Article
  8.Liu S, Liu S, Wang X, Zhou J, Cao Y, Wang F, Duan E (2011) The PI3K-Akt pathway inhibits senescence and promotes self-renewal of human skin-derived precursors in vitro. Aging Cell 10:661鈥?74. doi:10.鈥?111/鈥媕.鈥?474-9726.鈥?011.鈥?0704.鈥媥 PubMed Central PubMed View Article
  9.Wang X, Liu S, Zhao Q et al (2014) Three-dimensional hydrogel scaffolds facilitate in vitro self-renewal of human skin-derived precursors. Acta Biomater 10:3177鈥?187. doi:10.鈥?016/鈥媕.鈥媋ctbio.鈥?014.鈥?3.鈥?18 PubMed View Article
  10.Campisi J (1997) The biology of replicative senescence. Eur J Cancer 33:703鈥?09. doi:10.鈥?016/鈥婼0959-8049(96)00058-5 PubMed View Article
  11.Campisi J (2013) Aging, cellular senescence, and cancer. Annu Rev Physiol 75:685鈥?05. doi:10.鈥?146/鈥媋nnurev-physiol-030212-183653 PubMed Central PubMed View Article
  12.Suzuki M, Boothman DA (2008) Stress-induced premature senescence (SIPS). J Radiat Res 49:105鈥?12. doi:10.鈥?269/鈥媕rr.鈥?7081 PubMed View Article
  13.Minamino T, Miyauchi H, Tateno K, Kunieda T, Komuro I (2004) Akt-induced cellular senescence: implication for human disease. Cell Cycle 3:449鈥?51. doi:10.鈥?161/鈥媍c.鈥?.鈥?.鈥?19 PubMed View Article
  14.Kuki S, Imanishi T, Kobayashi K, Matsuo Y, Obana M, Akasaka T (2006) Hyperglycemia accelerated endothelial progenitor cell senescence via the activation of p38 mitogen-activated protein kinase. Circ J 70:1076鈥?081. doi:10.鈥?253/鈥媍ircj.鈥?0.鈥?076 PubMed View Article
  15.Chien Y, Scuoppo C, Wang X et al (2011) Control of the senescence-associated secretory phenotype by NF-魏B promotes senescence and enhances chemosensitivity. Genes Dev 25:2125鈥?136. doi:10.鈥?101/鈥媑ad.鈥?7276711 PubMed Central PubMed View Article
  16.Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinform 7:191. doi:10.鈥?186/鈥?471-2105-7-191 View Article
  17.Ben-Porath I, Weinberg RA (2005) The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37:961鈥?76. doi:10.鈥?016/鈥媕.鈥媌iocel.鈥?004.鈥?0.鈥?13 PubMed View Article
  18.Hornberger TA, Chu WK, Mak YW, Hsiung JW, Huang SA, Chien S (2006) The role of phospholipase D and phosphatidic acid in the mechanical activation of mTOR signaling in skeletal muscle. Proc Natl Acad Sci USA 103:4741鈥?746. doi:10.鈥?073/鈥媝nas.鈥?600678103 PubMed Central PubMed View Article
  19.Choi YJ, Park YJ, Park JY et al (2012) Inhibitory effect of mTOR activator MHY1485 on autophagy: suppression of lysosomal fusion. PLoS ONE 7:e43418. doi:10.鈥?371/鈥媕ournal.鈥媝one.鈥?043418 PubMed Central PubMed View Article
  20.Zhang R, Chen W, Adams PD (2007) Molecular dissection of formation of senescence-associated heterochromatin foci. Mol Cell Biol 27:2343鈥?358. doi:10.鈥?128/鈥婱CB.鈥?2019-06 PubMed Central PubMed View Article
  21.Kosar M, Bartkova J, Hubackova S, Hodny Z, Lukas J, Bartek J (2011) Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type- and insult-dependent manner and follow expression of p16ink4a. Cell Cycle 10:457鈥?68. doi:10.鈥?161/鈥媍c.鈥?0.鈥?.鈥?4707 PubMed View Article
  22.Coppe J-P, Desprez P-Y, Krtolica A, Campisi J (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5:99鈥?18. doi:10.鈥?146/鈥媋nnurev-pathol-121808-102144 PubMed Central PubMed View Article
  23.Gil J, Peters G (2006) Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol 7:667鈥?77. doi:10.鈥?038/鈥婲rm1987 PubMed View Article
  24.McConnell BB, Starborg M, Brookes S, Peters G (1998) Inhibitors of cyclin-dependent kinases induce features of replicative senescence in early passage human diploid fibroblasts. Curr Biol 8:351鈥?54. doi:10.鈥?016/鈥婼0960-9822(98)70137-X PubMed View Article
  25.Fuxe J, Akusj盲rvi G, Goike HM, Roos G, Collins VP, Pettersson RF (2000) Adenovirus-mediated overexpression of p15INK4B inhibits human glioma cell growth, induces replicative senescence, and inhibits telomerase activity similarly to p16INK4A. Cell Growth Differ 11:373鈥?84PubMed
  26.Malumbres M, P茅rez De Castro I, Hern谩ndez MI, Jim茅nez M, Corral T, Pellicer A (2000) Cellular response to oncogenic Ras involves induction of the Cdk4 and Cdk6 inhibitor p15 INK4b. Mol Cell Biol 20:2915鈥?925. doi:10.鈥?128/鈥媘cb.鈥?0.鈥?.鈥?915-2925.鈥?000 PubMed Central PubMed View Article
  27.Majumder PK, Grisanzio C, O鈥機onnell F et al (2008) A prostatic intraepithelial neoplasia-dependent p27Kip1 checkpoint induces senescence and inhibits cell proliferation and cancer progression. Cancer Cell 14:146鈥?55. doi:10.鈥?016/鈥媕.鈥媍cr.鈥?008.鈥?6.鈥?02 PubMed Central PubMed View Article
  28.Young AP, Schlisio S, Minamishima YA, Zhang Q, Li L, Grisanzio C, Signoretti S, Kaelin WG (2008) VHL loss actuates a HIF-independent senescence programme mediated by Rb and p400. Nat Cell Biol 10:361鈥?69. doi:10.鈥?038/鈥媙cb1699 PubMed View Article
  29.Alexander K, Hinds PW (2001) Requirement for p27KIP1 in retinoblastoma protein-mediated senescence. Mol Cell Biol 21:3616鈥?631. doi:10.鈥?128/鈥媘cb.鈥?1.鈥?1.鈥?616-3631.鈥?001 PubMed Central PubMed View Article
  30.Collado M, Medema RH, Garcia-Cao I et al (2000) Inhibition of the phosphoinositide 3-kinase pathway induces a senescence-like arrest mediated by p27Kip1. J Biol Chem 275:21960鈥?1968. doi:10.鈥?074/鈥媕bc.鈥婱000759200 PubMed View Article
  31.Medema RH, Kops GJ, Bos JL, Burgering BM (2000) AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404:782鈥?87. doi:10.鈥?038/鈥?5008115 PubMed View Article
  32.Katayama K, Nakamura A, Sugimoto Y, Tsuruo T, Fujita N (2007) FOXO transcription factor-dependent p15INK4b and p19INK4d expression. Oncogene 27:1677鈥?686. doi:10.鈥?038/鈥媠j.鈥媜nc.鈥?210813 PubMed View Article
  33.Courtois-Cox S, Genther Williams SM, Reczek EE, Johnson BW, McGillicuddy LT, Johannessen CM, Hollstein PE, MacCollin M, Cichowski K (2006) A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 10:459鈥?72. doi:10.鈥?016/鈥媕.鈥媍cr.鈥?006.鈥?0.鈥?03 PubMed Central PubMed View Article
  34.Nogueira V, Park Y, Chen C-C, Xu P-Z, Chen M-L, 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鈥?70. doi:10.鈥?016/鈥媕.鈥媍cr.鈥?008.鈥?1.鈥?03 PubMed Central PubMed View Article
  35.Kyoung Kim H, Kyoung Kim Y, Song I-H, Baek S-H, Lee S-R, Hye Kim J, Kim J-R (2005) Down-regulation of a forkhead transcription factor, FOXO3a, accelerates cellular senescence in human dermal fibroblasts. J Gerontol A Biol Sci Med Sci 60:4鈥?. doi:10.鈥?093/鈥媑erona/鈥?0.鈥?.鈥? PubMed View Article
  
• 作者单位：Shuang Liu (1)
  Xinyue Wang (1)
  Qian Zhao (2)
  Shu Liu (1)
  Huishan Zhang (1)
  Junchao Shi (1) (3)
  Na Li (1) (3)
  Xiaohua Lei (1)
  Huashan Zhao (1) (3)
  Zhili Deng (1) (3)
  Yujing Cao (1)
  Lina Ning (1)
  Guoliang Xia (2)
  Enkui Duan (1)
  
  1. State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing, 100101, China
  2. State Key Laboratory of Agrobiotechnology, College of Biological Sciences, China Agricultural University, No. 2 Yuanmingyuan Xilu, Haidian District, Beijing, 100193, China
  3. University of Chinese Academy of Sciences, Beijing, 100049, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Cell Biology
  Biomedicine
  Life Sciences
  Biochemistry
  
• 出版者：Birkh盲user Basel
• ISSN：1420-9071

文摘

Multipotent skin-derived precursors (SKPs) are dermal stem cells with the capacity to reconstitute the dermis and other tissues, such as muscles and the nervous system. Thus, the easily available human SKPs (hSKPs) hold great promises in regenerative medicine. However, long-term expansion is difficult for hSKPs in vitro. We previously demonstrated that hSKPs senesced quickly under routine culture conditions. To identify the underlying mechanisms so as to find an effective way to expand hSKPs, time-dependent microarray analysis of gene expression in hSKPs during in vitro culture was performed. We found that the senescence of hSKPs had a unique gene expression pattern that differs from reported typical senescence. Subsequent investigation ruled out the role of DNA damage and classical p53 and p16INK4a signaling in hSKP senescence. Examination of cyclin-dependent kinase inhibitors revealed the involvement of p15INK4b and p27KIP1. Further exploration about upstream signals indicated the contribution of Akt hypo-activity and FOXO3 to hSKP senescence. Forced activation of Akt and knockdown of FOXO3, p15INK4b and p27KIP1 effectively inhibited hSKP senescence and promoted hSKP proliferation. The unique senescent phenotype of human dermal stem cells and the role of Akt-FOXO3-p27KIP1/p15INK4b signaling in regulating hSKP senescence provide novel insights into the senescence and self-renewal regulation of adult stem cells. The present study also points out a way to propagate hSKPs in vitro so as to fulfill their promises in regenerative medicine.