Genetic deletion of Nrf2 promotes immortalization and decreases life span of murine embryonic fibroblasts

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 66 A, Issue 3, 2011, Pages 247-256

  Jódar, Laura ^a   Mercken, Evi M ^b   Ariza, Julia ^a   Younts, Caitlin ^b   González Reyes, José A ^a   Alcaín, Francisco J ^b,c   Burón, Isabel ^a   De Cabo, Rafael ^b   Villalba, José M ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

Cellular immortalization; Life span; MEFs; Nrf2; Replicative senescence

Indexed keywords

MURINAE;

TRANSCRIPTION FACTOR NRF2;

ANIMAL; ARTICLE; CELL AGING; COMPARATIVE STUDY; FIBROBLAST; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE;

ANIMALS; CELL AGING; FIBROBLASTS; GENE EXPRESSION REGULATION; MICE; NF-E2-RELATED FACTOR 2; SEQUENCE DELETION;

EID: 79955154110     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glq181     Document Type: Article

References (54)

1. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res. 1965;37:614-636.
2. Sherr CJ, DePinho RA. Cellular senescence: mitotic clock or culture shock? Cell. 2000;102:407-410.
3. Dirac AM, Bernards R. Reversal of senescence in mouse fibroblasts through lentiviral suppression of p53. J Biol Chem. 2003;278: 11731-11734. (Pubitemid 36800139)
4. Todaro GJ, Green H. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol. 1963;17:299-313.
5. Kiyono T. Molecular mechanisms of cellular senescence and immortalization of human cells. Expert Opin Ther Targets. 2007; 11:1623-1637. (Pubitemid 350300964)
6. Leal JF, Fominaya J, Cascón A, et al. Cellular senescence bypass screen identifies new putative tumor suppressor genes. Oncogene. 2008;27:1961-1970. (Pubitemid 351442744)
7. Campisi J. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol. 2001;11:S27-S31.
8. Michaloglou C, Vredeveld LC, Soengas MS, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436: 720-724. (Pubitemid 41117276)
9. Chen Z, Trotman LC, Shaffer D, et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature. 2005;436:725-730. (Pubitemid 41117277)
10. Vom Brocke J, Schmeiser HH, Reinbold M, Hollstein M. MEF immortalization to investigate the ins and outs of mutagenesis. Carcinogenesis. 2006;27:2141-2147. (Pubitemid 44649117)
11. Kilbey A, Blyth K, Wotton S, et al. Runx2 disruption promotes immortalization and confers resistance to oncogene-induced senescence in primary murine fibroblasts. Cancer Res. 2007;67:11263-11271. (Pubitemid 350248552)
12. Feng Z, Hu W, Teresky AK, Hernando E, Cordon-Cardo C, Levine AJ. Declining p53 function in the aging process: a possible mechanism for the increased tumor incidence in older populations. Proc Natl Acad Sci U S A. 2007;104:16633-16638. (Pubitemid 350211068)
13. Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci U SA. 1994;91:9926-9930. (Pubitemid 24311921)
14. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem. 1999;274:26071-26078.
15. Kwak MK, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW. Antioxidants enhance mammalian proteasome expression through the Keapl-Nrf2 signaling pathway. Mol Cell Biol. 2003;23:8786-8794. (Pubitemid 37433379)
16. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med. 2004;36:1199-1207. (Pubitemid 38526313)
17. Lee JM, Li J, Johnson DA, et al. Nrf2, a multi-organ protector? FASEB J. 2005;19:1061-1066. (Pubitemid 40946431)
18. Jain AK, Jaiswal AK. Phosphorylation of tyrosine 568 controls nuclear export of Nrf2. J Biol Chem. 2006;281:12132-12142. (Pubitemid 43855477)
19. Sykiotis GP, Bohmann D. Keapl/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell. 2008;14:76-85.
20. Sykiotis GP, Bohmann D. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci Signal. 2010;3:re3.
21. Kapeta S, Chondrogianni N, Gonos ES. Nuclear erythroid factor 2-mediated proteasome activation delays senescence in human fibroblasts. J Biol Chem. 2010;285:8171-8184.
22. Leiser SF, Miller RA. Nrf2 signaling, a mechanism for cellular stress resistance in long-lived mice. Mol Cell Biol. 2010;30:871-884.
23. Singh SP, Niemczyk M, Saini D, Sadovov V, Zimniak L, Zimniak P. Disruption of the mGsta4 gene increases life span of C57BL mice. J Gerontol A Biol Sci Med Sci. 2010;65:14-23.
24. Lind C, Cadenas E, Hochstein P, Ernster L. DT-diaphorase: purification, properties, and function. Methods Enzymol. 1990;186:287-301. (Pubitemid 20279970)
25. Navarro F, Villalba JM, Crane FL, MacKellar WC, Navas P. A phospholipid-dependent NADH-coenzyme Q reductase from liver plasma membrane. Biochem Biophys Res Commun. 1995;212: 138-143.
26. 5 reductase in HeLa cells. J Bioenerg Biomembr. 2003;35:169-179. (Pubitemid 36723661)
27. Dittmer A, Dittmer J. β-Actin is not a reliable loading control in Western blot analysis. Electrophoresis. 2006;27:2844-2845. (Pubitemid 44160833)
28. Debidda M, Williams DA, Zheng Y Rac1 GTPase regulates cell genomic stability and senescence. J Biol Chem. 2006;281:38519-38528. (Pubitemid 46041976)
29. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S. Identification of Nrf2-regulated genes induced by the che-mopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 2002;62:5196-5203. (Pubitemid 35033454)
30. Navas P, Villalba JM, de Cabo R. The importance of plasma membrane coenzyme Q in aging and stress responses. Mitochondrion. 2007;7S:S34-S40. (Pubitemid 46722290)
31. Hyun D-H, Emerson SS, Jo D-G, Mattson MP, de Cabo R. Calorie restriction up-regulates the plasma membrane redox system in brain cells and suppresses oxidative stress during aging. Proc Natl Acad Sci U S A. 2006;103:19908-19912. (Pubitemid 46037529)
32. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nature Cell Biol. 2003;5:741-747. (Pubitemid 36986782)
33. Collavitti R, Finkel T. Reactive oxygen species as mediators of cellular senescence. IUBMB Life. 2005;57:277-281. (Pubitemid 40904255)
34. Di Micco R, Cicalese A, Fumagalli M, et al. DNA damage response activation in mouse embryonic fibroblasts undergoing replicative senescence and following spontaneous immortalization. Cell Cycle. 2008;7:3601-3606.
35. Oberdoerffer P, Michan S, McVay M, et al. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell. 2008;135:907-918.
36. Allen RG, Tresini M. Oxidative stress and gene regulation. Free Radic Biol Med. 2000;28:463-499. (Pubitemid 30110662)
37. Reddy NM, Kleeberger SR, Yamamoto M, et al. Genetic dissection of the Nrf2-dependent redox signaling-regulated transcriptional programs of cell proliferation and cytoprotection. Physiol Genomics. 2007;32:74-81.
38. Reddy NM, Kleeberger SR, Bream JH, et al. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signalling. Oncogene. 2008;27:5821-5832.
39. Reddy NM, Kleeberger SR, Cho HY, et al. Deficiency in Nrf2-GSH signaling impairs type II cell growth and enhances sensitivity to oxidants. Am J Respir Cell Mol Biol. 2007;37:3-8. (Pubitemid 46999531)
40. Pani G, Colavitti R, Bedogni B, Anzevino R, Borrello S, Galeotti T. A redox signaling mechanism for density-dependent inhibition of cell growth. J Biol Chem. 2000;275:38891-38899. (Pubitemid 32010745)
41. 1 to S transition in the mouse embryo fibroblast cell cycle. Cancer Res. 2003;63:2109-2117. (Pubitemid 36538614)
42. Levonen AL, Inkala M, Heikura T, et al. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vase Biol. 2007;27:741-747. (Pubitemid 46606701)
43. Frohlich DA, McCabe MT, Arnold RS, Day ML. The role of Nrf2 in increased reactive oxygen species and DNA damage in prostate tumorigenesis. Oncogene. 2008;27:4353-4362. (Pubitemid 352010007)
44. Jeong WS, Jun M, Kong AN. Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal. 2006;8:99-106. (Pubitemid 43324535)
45. Giudice A, Montella M. Activation of the Nrf2-ARE signaling pathway: a promising strategy in cancer prevention. Bioessays. 2006;28: 169-181.
46. Iida K, Itoh K, Maher JM, et al. Nrf2 and p53 cooperatively protect against BBN-induced urinary bladder carcinogenesis. Carcinogenesis. 2007;28:2398-2403. (Pubitemid 350111600)
47. Pearson KJ, Lewis KN, Price NL, et al. Nrf2 mediates cancer protection but not prolongevity induced by caloric restriction. Proc Natl AcadSci U S A. 2008;105:2325-2330. (Pubitemid 351520512)
48. Schäfer M, Dütsch Sauf dem Keller U, et al. Nrf2 establishes a glutathione-mediated gradient of UVB cytoprotection in the epidermis. Genes Dev. 2010;24:1045-1058.
49. Kweon MH, Adhami VN, Lee JS, Mukhtar H. Constitutive overexpres-sion of Nrf2-dependent heme oxygenase-1 in A549 cells contributes to resistance to apoptosis induced by epigallocatechin 3-gallate. J Biol Chem. 2006;281:33761-33772. (Pubitemid 46036754)
50. Padmanabhan B, Tong KI, Ohta T, et al. Structural basis for defects of Keapl activity provoked by its point mutations in lung cancer. Mol Cell. 2006;21:689-700. (Pubitemid 43290735)
51. Hayes JD, McMahon M. The double-edged sword of Nrf2: subversion of redox homeostasis during the evolution of cancer. Mol Cell. 2006;21:732-734. (Pubitemid 43376123)
52. Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, Park YM. Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygen-ation: implication to tumor biology. Cancer Res. 2007;67:546-554. (Pubitemid 46192191)
53. Trachootham D, Zhou Y, Zhang H, et al. Selective killing of onco-genically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell. 2006;10:241-252. (Pubitemid 44311067)
54. Dolado I, Swat A, Ajenjo N, de Vita G, Cuadrado A, Nebreda AR. p38α MAP kinase as a sensor of reactive oxygen species in tumorige-neris. Cancer Cell. 2007;11:191-205. (Pubitemid 46209847)