Cellular Redox Imbalance and Changes of Protein S-glutathionylation Patterns Are Associated with Senescence Induced by Oncogenic H-Ras

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Armeni, Tatiana ^a   Ercolani, Luisa ^a   Urbanelli, Lorena ^b   Magini, Alessandro ^b   Magherini, Francesca ^c   Pugnaloni, Armanda ^a   Piva, Francesco ^a   Modesti, Alessandra ^c   Emiliani, Carla ^b   Principato, Giovanni ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; ENZYME; GLUTATHIONE; PROTEIN S; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL AGING; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; GLUTATHIONYLATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; METABOLIC PARAMETERS; NUCLEOTIDE SEQUENCE; ONCOGENE H RAS; OXIDATION REDUCTION STATE; PRECANCER; PROTEIN MODIFICATION; TOTAL ANTIOXIDANT CAPACITY;

ANTIOXIDANTS; APOPTOSIS; AUTOPHAGY; CELL AGING; CELL CYCLE; CELL DEATH; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENES, RAS; HUMANS; IMMUNOBLOTTING; MASS SPECTROMETRY; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES;

EID: 84871447941     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052151     Document Type: Article

References (60)

1. Ferbeyre G, De Stanchina E, Lin AW, Querido E, McCurrach ME, et al. (2002) Oncogenic ras and p53 cooperate to induce cellular senescence. Mol Cell Biol 22: 3497-3508.
2. Land H, Parada LF, Weinberg RA, (1983) Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304: 596-602.
3. Luo J, Solimini NL, Elledge SJ, (2009) Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136: 823-837.
4. Elgendy M, Sheridan C, Brumatti G, Martin SJ, (2011) Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol Cell 42: 23-35.
5. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
6. Nicke B, Bastien J, Khanna SJ, Warne PH, Cowling V, et al. (2005) Involvement of MINK, a Ste20 family kinase, in Ras oncogene-induced growth arrest in human ovarian surface epithelial cells. Mol Cell 20: 673-685.
7. Sarkisian CJ, Keister BA, Stairs DB, Boxer RB, Moody SE, et al. (2007) Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis. Nat Cell Biol 9: 493-505.
8. Collado M, Serrano M, (2005) The senescent side of tumor suppression. Cell Cycle 4: 1722-1724.
9. Bartek J, Lukas J, (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19: 238-245.
10. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
11. Bartkova J, Hamerlik P, Stockhausen MT, Ehrmann J, Hlobilkova A, et al. (2010) Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 29: 5095-5102.
12. Lee JJ, Lee JH, Ko YG, Hong SI, Lee JS, (2010) Prevention of premature senescence requires JNK regulation of Bcl-2 and reactive oxygen species. Oncogene 29: 561-575.
13. Ralph SJ, Rodriguez-Enriquez S, Neuzil J, Saavedra E, Moreno-Sanchez R, (2010) The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation - why mitochondria are targets for cancer therapy. Mol Aspects Med 31: 145-170.
14. Duan J, Zhang Z, Tong T, (2005) Irreversible cellular senescence induced by prolonged exposure to H2O2 involves DNA-damage-and-repair genes and telomere shortening. Int J Biochem Cell Biol 37: 1407-1420.
15. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M, (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160: 1-40.
16. Giles GI, (2006) The redox regulation of thiol dependent signaling pathways in cancer. Curr Pharm Des 12: 4427-4443.
17. Burhans WC, Heintz NH, (2009) The cell cycle is a redox cycle: linking phase-specific targets to cell fate. Free Radic Biol Med 47: 1282-1293.
18. Thamsen M, Jakob U, (2011) The redoxome. Proteomic analysis of cellular redox networks. Curr Opin Chem Biol 15: 113-119.
19. Biswas S, Chida AS, Rahman I, (2006) Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol 71: 551-564.
20. Xiong Y, Uys JD, Tew KD, Townsend DM, (2011) S-glutathionylation: from molecular mechanisms to health outcomes. Antioxid Redox Signal 15: 233-270.
21. Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, et al. (2008) Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10: 445-473.
22. Ghezzi P, Di Simplicio P, (2007) Glutathionylation pathways in drug response. Curr Opin Pharmacol 7: 398-403.
23. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, Shelton MD, (2008) Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941-1988.
24. Gilge JL, Fisher M, Chai YC, (2008) The effect of oxidant and the non-oxidant alteration of cellular thiol concentration on the formation of protein mixed-disulfides in HEK 293 cells. Plos One 3: 1-7.
25. Tew KD, Townsend DM, (2011) Redox platforms in cancer drug discovery and development. Curr Opin Chem Biol 15: 156-161.
26. Adachi T, Pimentel DR, Heibeck T, Hou X, Lee Y J, et al. (2004) S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem 279: 29857-29862.
27. Mohd AY, Trinette C, G Jayarama B, Kalkunte S, (2010) Cys-141glutathionylation of human p53: Studies using specific polyclonal antibodies in cancer samples and cell lines. Free Radic Biol Med 49: 908-917.
28. Borras C, Esteve JM, Vina JR, Sastre J, Vina J, et al. (2004) Glutathione regulates telomerase activity in 3T3 fibroblasts. J Biol Chem 279: 34332-34335.
29. Markovic J, Garcia-Gimenez JL, Gimeno A, Vina J, Pallardo FV, (2010) Role of glutathione in cell nucleus. Free Radic Res 44: 721-733.
30. Vayalil PK, Iles KE, Choi J, Yi AK, Postlethwait EM, et al. (2007) Glutathione suppresses TGF-beta-induced PAI-1 expression by inhibiting p38 and JNK MAPK and the binding of AP-1, SP-1, and Smad to the PAI-1 promoter. Am J Physiol Lung Cell Mol Physiol 293: L1281-1292.
31. Balendiran GK, Dabur R, Fraser D, (2004) The role of glutathione in cancer. Cell Biochem Funct 22: 343-352.
32. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, et al. (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390: 191-214.
33. Estrela JM, Ortega A, Obrador E, (2006) Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci 43: 143-181.
34. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.34.
35. Shlush LI, Itzkovitz S, Cohen A, Rutenberg A, Berkovitz R, et al. (2011) Quantitative digital in situ senescence-associated beta-galactosidase assay. BMC Cell Biol 12: 16.
36. Regoli F, Winston GW, (1999) Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol Appl Pharmacol 156: 96-105.
37. Brigelius R, Muckel C, Akerboom TP, Sies H, (1983) Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem Pharmacol 32: 2529-2534.
38. Carlberg I, Mannervik B, (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250: 5475-5480.
39. Habig WH, Pabst MJ, Fleischner G, Gatmaitan Z, Arias IM, et al. (1974) The identity of glutathione S-transferase B with ligandin, a major binding protein of liver. Proc Natl Acad Sci USA 71: 3879-3882.
40. Bergmeyer HU (1974) Methods in Enzyme Analysis, 466-467, Verlagchemie GmbH, Weinheim.
41. Hellman U, Wernstedt C, Gonez J, Heldin CH, (1995) Improvement of an "in gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal Biochem 224: 451-455.
42. Itahana K, Campisi J, Dimri GP, (2007) Methods to detect biomarkers of cellular senescence: the senescence-associated beta-galactosidase assay. Methods Mol Biol 371: 21-31.
43. Liu R, Li B, Qiu M, (2001) Elevated superoxide production by active H-ras enhances human lung WI-38VA-13 cell proliferation, migration and resistance to TNF-alpha. Oncogene 20(12): 1486-1496.
44. Lee AC, Fenster BE, Ito H, Takeda K, Bae NS, et al. (1999) Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J Biol Chem 274(12): 7936-7940.
45. Serù R, Mondola P, Damiano S, Svegliati S, Agnese S, et al. (2004) HaRas activates the NADPH oxidase complex in human neuroblastoma cells via extracellular signal regulated kinase 1/2 pathway. J Neurochem 91(3): 613-622.
46. Hole PS, Pearn L, Tonks AJ, James PE, Burnett AK, et al. (2010) Ras-induced reactive oxygen species promote growth factor-independent proliferation in human CD34+ hematopoietic progenitor cells. Blood. 115(6): 1238-1246.
47. Banerjee P, Basu A, Datta D, Gasser M, Waaga-Gasser AM, et al. (2011) The heme oxygenase-1protein is overexpressed in human renal cancer cells following activation of the Ras-Raf-ERK pathway and mediates anti-apoptotic signal. J Biol Chem Sep 23 286(38): 33580-33590.
48. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
49. Giustarini D, Rossi R, Milzani A, Colombo R, Dalle-Donne I, (2004) S-glutathionylation: from redox regulation of protein functions to human diseases. J Cell Mol Med 8: 201-212.
50. Martinez-Ruiz A, Lamas S, (2007) Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences. Cardiovasc Res 75: 220-228.
51. Magherini F, Carpentieri A, Amoresano A, Gamberi T, De Filippo C, et al. (2009) Different carbon sources affect lifespan and protein redox state during Saccharomyces cerevisiae chronological ageing. Cell Mol Life Sci 66(5): 933-47.
52. Mohr S, Hallak H, de Boitte A, Lapetina EG, Brüne B, (1999) Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem. 274: 9427-9430.
53. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, et al. (2002) Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci USA. 99(6): 3505-3510.
54. Garcia J, Han D, Sancheti H, Yap LP, Kaplowitz N, et al. (2010) Regulation of mitochondrial glutathione redox status and protein glutathionylation by respiratory substrates. J Biol Chem. 285(51): 39646-39654.
55. Townsend DM, Findlay VJ, Fazilev F, Ogle M, Fraser J, et al. (2005) A glutathione S-transferase pi-activated prodrug causes kinase activation concurrent with S-glutathionylation of proteins. Mol Pharmacol. 69(2): 501-508.
56. Kagawa Y, Hamamoto T, Endo H, Ichida M, Shibui H, et al. (1997) Genes of human ATP synthase: their roles in physiology and aging. Biosci Rep. 17(2): 115-146.
57. Ivaska J, Pallari HM, Nevo J, Eriksson JE, (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res. 313: 2050-2062.
58. Perluigi M, Di Domenico F, Giorgi A, Schininà ME, Coccia R, et al. (2010) Redox proteomics in aging rat brain: involvement of mitochondrial reduced glutathione status and mitochondrial protein oxidation in the aging process J Neurosci Res. 88(16): 3498-3507.
59. Tu SH, Chang CC, Chen CS, Tam KW, Wang YJ, et al. (2010) Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells Breast Cancer Res Treat. 121(3): 539-53.
60. Andrei D, Maciag AE, Chakrapani H, Citro ML, Keefer LK, et al. (2008) Aryl bis(diazeniumdiolates): potent inducers of S-glutathionylation of cellular proteins and their in vitro antiproliferative activities. J Med Chem 51: 7944-7952.