MnSOD upregulation induces autophagic programmed cell death in senescent keratinocytes

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-18

  Deruy, Emeric ^a,b,c   Gosselin, Karo ^a,b,c   Vercamer, Chantal ^a,b,c   Martien, Sébastien ^a,b,c   Bouali, Fatima ^a,b,c   Slomianny, Christian ^a,d   Bertout, Julie ^a,b,c   Bernard, David ^e   Pourtier, Albin ^a,b,c   Abbadie, Corinne ^a,b,c  

^a UNIV LILLE   (France)

^b INSTITUT DE BIOLOGIE DE LILLE   (France)

^c INSTITUT PASTEUR DE LILLE   (France)

^d Université des Sciences et Technologies de Lille   (France)

^e CENTRE LÉON BÉRARD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; CATALASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; SMALL INTERFERING RNA; SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DAMAGE; CELL NUCLEUS; CELL VACUOLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; MITOCHONDRION; OXIDATIVE STRESS; SENESCENCE; UPREGULATION; CELL AGING; CELL CULTURE; CELL DEATH; CYTOLOGY; ENZYMOLOGY; FEMALE; GENETICS; METABOLISM;

AUTOPHAGY; CELL AGING; CELL DEATH; CELL NUCLEUS; CELLS, CULTURED; FEMALE; HUMANS; HYDROGEN PEROXIDE; KERATINOCYTES; MITOCHONDRIA; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 77958587997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012712     Document Type: Article

References (58)

1. Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37: 614-636.
2. Cristofalo VJ, Lorenzini A, Allen RG, Torres C, Tresini M (2004) Replicative senescence: a critical review. Mech Ageing Dev 125: 827-48.
3. Zwerschke W, Mazurek S, Stockl P, Hutter E, Eigenbrodt E, et al. (2003) Metabolic analysis of senescent human fibroblasts reveals a role for AMP in cellular senescence. Biochem J 376: 403-11.
4. Gosselin K, Deruy E, Martien S, Vercamer C, Bouali F, et al. (2009) Senescent keratinocytes die by autophagic programmed cell death. Am J Pathol 174: 423-35.
5. Young AR, Narita M, Ferreira M, Kirschner K, Sadaie M, et al. (2009) Autophagy mediates the mitotic senescence transition. Genes Dev 23: 798-803.
6. Sasaki M, Miyakoshi M, Sato Y, Nakanuma Y (2010) Autophagy mediates the process of cellular senescence characterizing bile duct damages in primary biliary cirrhosis. Lab Invest.
7. Gozuacik D, Kimchi A (2007) Autophagy and cell death. Curr Top Dev Biol 78: 217-45.
8. Xie Z, Klionsky DJ (2007) Autophagosome formation: core machinery and adaptations. Nat Cell Biol 9: 1102-9.
9. Mizushima N (2007) Autophagy: process and function. Genes Dev 21: 2861-73.
10. Bernard D, Gosselin K, Monte D, Vercamer C, Bouali F, et al. (2004) Involvement of Rel/NF-kappaB transcription factors in keratinocyte senescence. Cancer Res 64: 472-81.
11. Boyce ST, Ham RG (1983) Calcium-regulated differentiation of normal human epidermal keratinocytes in chemically defined clonal culture and serum-free serial culture. J Invest Dermatol 81: 33s-40s.
12. Martinon O, Poulet JP, Chancerelle Y, Viret-Soropogui R, Mathieu J, et al. (1994) Immunization of mice with proteins reacted with malonic dialdehyde (MDA): comparison between autologous and heterologous modified proteins. Biochem Mol Biol Int 34: 135-45.
13. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208-12.
14. 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 USA 92: 9363-9367.
15. Bernard D, Quatannens B, Begue A, Vandenbunder B, Abbadie A (2001) Antiproliferative and anti-apoptotic effects of cRel may occur within the same cells via the up-regulation of MnSOD. Cancer Research 61: 2656-2664.
16. Chartier C, Degryse E, Gantzer M, Dieterle A, Pavirani A, et al. (1996) Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J Virol 70: 4805-10.
17. Schiedner G, Hertel S, Kochanek S (2000) Efficient transformation of primary human amniocytes by E1 functions of Ad5: generation of new cell lines for adenoviral vector production. Hum Gene Ther 11: 2105-16.
18. Kimura S, Noda T, Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452-60.
19. Sekiguchi M, Tsuzuki T (2002) Oxidative nucleotide damage: consequences and prevention. Oncogene 21: 8895-904.
20. Seglen PO, Gordon PB (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79: 1889-92.
21. Bowman EJ, Siebers A, Altendorf K (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85: 7972-6.
22. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, et al. (1998) Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42.
23. Hanada T, Noda NN, Satomi Y, Ichimura Y, Fujioka Y, et al. (2007) The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J Biol Chem 282: 37298-302.
24. Abuchowski A, McCoy JR, Palczuk NC, van Es T, Davis FF (1977) Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase. J Biol Chem 252: 3582-6.
25. Beckman JS, Minor RL, Jr., White CW, Repine JE, Rosen GM, et al. (1988) Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J Biol Chem 263: 6884-92.
26. Clarke PGH (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181: 195-213.
27. Tsujimoto Y, Shimizu S (2005) Another way to die: autophagic programmed cell death. Cell Death Differ 12 Suppl 2: 1528-34.
28. Kourtis N, Tavernarakis N (2009) Autophagy and cell death in model organisms. Cell Death Differ 16: 21-30.
29. Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23: 2891-906.
30. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, et al. (2004) Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-8.
31. Yu L, Wan F, Dutta S, Welsh S, Liu Z, et al. (2006) Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci U S A 103: 4952-7.
32. Kiffin R, Bandyopadhyay U, Cuervo AM (2006) Oxidative stress and autophagy. Antioxid Redox Signal 8: 152-62.
33. Scherz-Shouval R, Elazar Z (2007) ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 17: 422-7.
34. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, et al. (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Embo J 26: 1749-60.
35. Lee HC, Yin PH, Lu CY, Chi CW, Wei YH (2000) Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 348 Pt 2: 425-32.
36. Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, et al. (2007) Specific Aquaporins Facilitate the Diffusion of Hydrogen Peroxide across Membranes. J Biol Chem 282: 1183-92.
37. Kirkland RA, Adibhatla RM, Hatcher JF, Franklin JL (2002) Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 115: 587-602.
38. Kim EH, Choi KS (2008) A critical role of superoxide anion in selenite-induced mitophagic cell death. Autophagy 4: 76-8.
39. Dagda RK, Cherra SJ, 3rd, Kulich SM, Tandon A, Park D, et al. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284: 13843-55.
40. Huang Q, Shen HM (2009) To die or to live: the dual role of poly(ADP-ribose) polymerase-1 in autophagy and necrosis under oxidative stress and DNA damage. Autophagy 5: 273-6.
41. Daido S, Yamamoto A, Fujiwara K, Sawaya R, Kondo S, et al. (2005) Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 65: 4368-75.
42. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, et al. (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 21: 1621-35.
43. Roberts P, Moshitch-Moshkovitz S, Kvam E, O'Toole E, Winey M, et al. (2003) Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol Biol Cell 14: 129-41.
44. Krick R, Muehe Y, Prick T, Bremer S, Schlotterhose P, et al. (2008) Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell 19: 4492-505.
45. Kovacs AL, Rez G, Palfia Z, Kovacs J (2000) Autophagy in the epithelial cells of murine seminal vesicle in vitro. Formation of large sheets of nascent isolation membranes, sequestration of the nucleus and inhibition by wortmannin and 3- ethyladenine. Cell Tissue Res 302: 253-61.
46. Park YE, Hayashi YK, Bonne G, Arimura T, Noguchi S, et al. (2009) Autophagic degradation of nuclear components in mammalian cells. Autophagy 5: 795-804.
47. Wagner M, Hampel B, Bernhard D, Hala M, Zwerschke W, et al. (2001) Replicative senescence of human endothelial cells in vitro involves G1 arrest, polyploidization and senescence-associated apoptosis. Exp Gerontol 36: 1327-47.
48. Unterluggauer H, Hampel B, Zwerschke W, Jansen-Durr P (2003) Senescenceassociated cell death of human endothelial cells: the role of oxidative stress. Exp Gerontol 38: 1149-60.
49. Hampel B, Malisan F, Niederegger H, Testi R, Jansen-Durr P (2004) Differential regulation of apoptotic cell death in senescent human cells. Exp Gerontol 39: 1713-21.
50. Lee BY, Han JA, Im JS, Morrone A, Johung K, et al. (2006) Senescenceassociated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 5: 187-95.
51. Ding G, Franki N, Kapasi AA, Reddy K, Gibbons N, et al. (2001) Tubular cell senescence and expression of TGF-beta1 and p21(WAF1/CIP1) in tubulointerstitial fibrosis of aging rats. Exp Mol Pathol 70: 43-53.
52. Martin JA, Buckwalter JA (2003) The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J Bone Joint Surg Am 85-A Suppl 2: 106-10.
53. Keyes WM, Wu Y, Vogel H, Guo X, Lowe SW, et al. (2005) p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes Dev 19: 1986-99.
54. Yin D (1996) Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic Biol Med 21: 871-88.
55. Yue Z, Jin S, Yang C, Levine AJ, Heintz N (2003) Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 100: 15077-82.
56. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, et al. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-20.
57. Sansal I, Sellers WR (2004) The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol 22: 2954-63.
58. Arico S, Petiot A, Bauvy C, Dubbelhuis PF, Meijer AJ, et al. (2001) The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem 276: 35243-6.