Pleiotropic age-dependent effects of mitochondrial dysfunction on epidermal stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10407-10412

  Velarde, Michael C ^a   Demaria, Marco ^a   Melov, Simon ^a   Campisi, Judith ^a,b  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Cellular senescence; Oxidative stress; Skin aging; Stem cell proliferation; Superoxide dismutase 2

Indexed keywords

CD36 ANTIGEN; CRE RECOMBINASE; CYTOCHROME C OXIDASE; CYTOKERATIN 10; CYTOKERATIN 14; CYTOKERATIN 6; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR A; SUCCINATE DEHYDROGENASE (UBIQUINONE); COLLAGEN; PRIMER DNA; SUPEROXIDE DISMUTASE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL AGING; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL FUNCTION; CELL REGENERATION; CELL RENEWAL; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME DEFICIENCY; EPIDERMAL STEM CELL; EPITHELIZATION; FLOW CYTOMETRY; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; LOXP SITE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; SKELETAL MUSCLE; TUNEL ASSAY; WOUND CLOSURE; ALLELE; ANIMAL; CELL PROLIFERATION; CHEMISTRY; CUTANEOUS PARAMETERS; CYTOLOGY; EPIDERMIS; GENE DELETION; GENE EXPRESSION PROFILING; GENOTYPE; HOMEOSTASIS; HUMAN; METABOLISM; PATHOLOGY; STEM CELL; TIME FACTOR; TRANSGENIC MOUSE; WOUND HEALING;

MUS;

ALLELES; ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN; DNA PRIMERS; EPIDERMIS; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC PLEIOTROPY; GENOTYPE; HOMEOSTASIS; HUMANS; KERATINOCYTES; MICE; MICE, TRANSGENIC; MITOCHONDRIA; OXIDATIVE STRESS; PHENOTYPE; SKIN AGING; STEM CELLS; SUPEROXIDE DISMUTASE; TIME FACTORS; WOUND HEALING;

EID: 84940190647     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505675112     Document Type: Article

References (53)

1. Hsu YC, Li L, Fuchs E (2014) Emerging interactions between skin stem cells and their niches. Nat Med 20(8):847-856.
2. Plikus MV, et al. (2012) Epithelial stem cells and implications for wound repair. Semin Cell Dev Biol 23(9):946-953.
3. Candi E, Schmidt R, Melino G (2005) The cornified envelope: A model of cell death in the skin. Nat Rev Mol Cell Biol 6(4):328-340.
4. Jones DL, Rando TA (2011) Emerging models and paradigms for stem cell ageing. Nat Cell Biol 13(5):506-512.
5. Friedman JS, et al. (2001) Absence of mitochondrial superoxide dismutase results in a murine hemolytic anemia responsive to therapy with a catalytic antioxidant. J Exp Med 193(8):925-934.
6. Ito K, et al. (2006) Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 12(4):446-451.
7. Gilchrest BA (2013) Photoaging. J Invest Dermatol 133(E1):E2-E6.
8. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4): 483-495.
9. Birch-Machin MA, Russell EV, Latimer JA (2013) Mitochondrial DNA damage as a biomarker for ultraviolet radiation exposure and oxidative stress. Br J Dermatol 169 (Suppl 2):9-14.
10. Flynn JM, et al. (2011) Impaired spare respiratory capacity in cortical synaptosomes from Sod2 null mice. Free Radic Biol Med 50(7):866-873.
11. Hinerfeld D, et al. (2004) Endogenous mitochondrial oxidative stress: Neurodegeneration, proteomic analysis, specific respiratory chain defects, and efficacious antioxidant therapy in superoxide dismutase 2 null mice. J Neurochem 88(3):657-667.
12. Li Y, et al. (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11(4):376-381.
13. Melov S, et al. (1999) Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci USA 96(3):846-851.
14. Melov S, et al. (2001) Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J Neurosci 21(21):8348-8353.
15. Melov S, et al. (1998) A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18(2):159-163.
16. Morten KJ, Ackrell BA, Melov S (2006) Mitochondrial reactive oxygen species in mice lacking superoxide dismutase 2: Attenuation via antioxidant treatment. J Biol Chem 281(6):3354-3359.
17. Samper E, Nicholls DG, Melov S (2003) Mitochondrial oxidative stress causes chromosomal instability of mouse embryonic fibroblasts. Aging Cell 2(5):277-285.
18. Campisi J (2013) Aging, cellular senescence, and cancer. Annu Rev Physiol 75:685-705.
19. 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(1):3-12.
20. Dai DF, et al. (2010) Age-dependent cardiomyopathy in mitochondrial mutator mice is attenuated by overexpression of catalase targeted to mitochondria. Aging Cell 9(4): 536-544.
21. Schriner SE, et al. (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308(5730):1909-1911.
22. Pan L, et al. (2007) Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 1(4):458-469.
23. Hill S, Van Remmen H (2014) Mitochondrial stress signaling in longevity: A new role for mitochondrial function in aging. Redox Biol 2:936-944.
24. Coulombe PA, Kopan R, Fuchs E (1989) Expression of keratin K14 in the epidermis and hair follicle: Insights into complex programs of differentiation. J Cell Biol 109(5): 2295-2312.
25. Vasioukhin V, Degenstein L, Wise B, Fuchs E (1999) The magical touch: Genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci USA 96(15):8551-8556.
26. Jensen UB, et al. (2008) A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus. J Cell Sci 121(Pt 5):609-617.
27. Jensen KB, Watt FM (2006) Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci USA 103(32):11958-11963.
28. Snippert HJ, et al. (2010) Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327(5971):1385-1389.
29. Navarro JM, Casatorres J, Jorcano JL (1995) Elements controlling the expression and induction of the skin hyperproliferation-associated keratin K6. J Biol Chem 270(36): 21362-21367.
30. Haertel E, Werner S, Schäfer M (2014) Transcriptional regulation of wound inflammation. Semin Immunol 26(4):321-328.
31. Thuringer JM, Katzberg AA (1959) The effect of age on mitosis in the human epidermis. J Invest Dermatol 33:35-39.
32. Adler AS, et al. (2007) Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev 21(24):3244-3257.
33. Mascré G, et al. (2012) Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 489(7415):257-262.
34. Jensen KB, Driskell RR, Watt FM (2010) Assaying proliferation and differentiation capacity of stem cells using disaggregated adult mouse epidermis. Nat Protoc 5(5): 898-911.
35. Ziegler DV, Wiley CD, Velarde MC (2015) Mitochondrial effectors of cellular senescence: Beyond the free radical theory of aging. Aging Cell 14(1):1-7.
36. Demaria M, et al. (2014) An essential role for senescent cells in optimal wound healing through secretion of PDGF-AA. Dev Cell 31(6):722-733.
37. Dimri GP, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92(20):9363-9367.
38. Doles J, Storer M, Cozzuto L, Roma G, Keyes WM (2012) Age-associated inflammation inhibits epidermal stem cell function. Genes Dev 26(19):2144-2153.
39. Owusu-Ansah E, Banerjee U (2009) Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461(7263):537-541.
40. Hamanaka RB, et al. (2013) Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci Signal 6(261):ra8.
41. Tamiji S, et al. (2005) Induction of apoptosis-like mitochondrial impairment triggers antioxidant and Bcl-2-dependent keratinocyte differentiation. J Invest Dermatol 125(4):647-658.
42. Lago CU, et al. (2012) Mitochondrial respiratory uncoupling promotes keratinocyte differentiation and blocks skin carcinogenesis. Oncogene 31(44):4725-4731.
43. Stern MM, Bickenbach JR (2007) Epidermal stem cells are resistant to cellular aging. Aging Cell 6(4):439-452.
44. Giangreco A, Qin M, Pintar JE, Watt FM (2008) Epidermal stem cells are retained in vivo throughout skin aging. Aging Cell 7(2):250-259.
45. Jensen UB, Lowell S, Watt FM (1999) The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: A new view based on wholemount labelling and lineage analysis. Development 126(11):2409-2418.
46. Castilho RM, Squarize CH, Chodosh LA, Williams BO, Gutkind JS (2009) mTOR mediates Wnt-induced epidermal stem cell exhaustion and aging. Cell Stem Cell 5(3): 279-289.
47. Signer RA, Morrison SJ (2013) Mechanisms that regulate stem cell aging and life span. Cell Stem Cell 12(2):152-165.
48. Baker DJ, et al. (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479(7372):232-236.
49. Jun JI, Lau LF (2010) The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol 12(7):676-685.
50. Krizhanovsky V, et al. (2008) Senescence of activated stellate cells limits liver fibrosis. Cell 134(4):657-667.
51. Muñoz-Espín D, et al. (2013) Programmed cell senescence during mammalian embryonic development. Cell 155(5):1104-1118.
52. Storer M, et al. (2013) Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 155(5):1119-1130.
53. Braun KM, et al. (2003) Manipulation of stem cell proliferation and lineage commitment: Visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130(21):5241-5255.