Hexavalent chromium induces energy metabolism disturbance and p53-dependent cell cycle arrest via reactive oxygen species in L-02 hepatocytes

Molecular and Cellular Biochemistry

Volumn 371, Issue 1-2, 2012, Pages 65-76

  Xiao, Fang ^a   Feng, Xiaotao ^b   Zeng, Ming ^a   Guan, Lan ^a   Hu, Qingqing ^c   Zhong, Caigao ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b GUANGXI UNIVERSITY OF CHINESE MEDICINE   (China)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Cell cycle arrest; Cr(VI); L 02 hepatocytes; p53; ROS

Indexed keywords

ACETYLCYSTEINE; BENZIMIDAZOLE DERIVATIVE; CHECKPOINT KINASE 1; CHROMIUM; CYCLIN DEPENDENT KINASE 2; PIFITHRIN ALPHA; PROTEIN P53; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; ENERGY METABOLISM; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LIVER CELL; PROTEIN EXPRESSION; RESPIRATION CONTROL; S PHASE CELL CYCLE CHECKPOINT; WESTERN BLOTTING;

ACETYLCYSTEINE; BENZOTHIAZOLES; CARCINOGENS, ENVIRONMENTAL; CELL CYCLE CHECKPOINTS; CHROMIUM; CYCLIN-DEPENDENT KINASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; ENVIRONMENTAL POLLUTANTS; HEPATOCYTES; HUMANS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLUENE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84868521916     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-012-1423-7     Document Type: Article

References (58)

1. Barnhart J (1997) Occurrences, uses, and properties of chromium. Regul Toxicol Pharmacol 26(1):S3-S7
2. Stern RM (1982) Chromium compounds: production and occupational exposure. NTIS, Springfield
3. Kerger B, Paustenbach D, Corbett G, Finley B (1996) Absorption and elimination of trivalent and hexavalent chromium in humans following ingestion of a bolus dose in drinking water. Toxicol Appl Pharmacol 141(1):145-158
4. Gunaratnam M, Grant MH (2008) Cr(VI) inhibits DNA, RNA and protein syntheses in hepatocytes: involvement of glutathione reductase, reduced glutathione and DT-diaphorase. Toxicol In Vitro 22(4):879-886. doi: 10.1016/j.tiv.2008.01.005
5. Rafael AI, Almeida A, Santos P, Parreira I, Madeira VM, Alves R, Cabrita AM, Alpoim MC (2007) A role for transforming growth factor-beta apoptotic signaling pathway in liver injury induced by ingestion of water contaminated with high levels of Cr(VI). Toxicol Appl Pharmacol 224(2):163-173. doi: 10.1016/j.taap.2007.07.004
6. Wang XF, Xing ML, Shen Y, Zhu X, Xu LH (2006) Oral administration of Cr(VI) induced oxidative stress, DNA damage and apoptotic cell death in mice. Toxicology 228(1):16-23
7. Brown GC (1992) Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem J 284(Pt 1):1
8. Vedel F, Lalanne É, Sabar M, Chetrit P, De Paepe R (1999) The mitochondrial respiratory chain and ATP synthase complexes: composition, structure and mutational studies. Plant Physiol Biochem 37(9):629-643
9. Jensen P (1966) Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-transport particles I. pH dependency and hydrogen peroxide formation. Biochimica et Biophysica Acta (BBA)-Enzymology and Biological Oxidation 122(2):157-166
10. Turrens JF, Alexandre A, Lehninger AL (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys 237(2):408-414
11. Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191(2):421
12. Son YO, Hitron JA, Wang X, Chang Q, Pan J, Zhang Z, Liu J, Wang S, Lee JC, Shi X (2010) Cr(VI) induces mitochondrial-mediated and caspase-dependent apoptosis through reactive oxygen species-mediated p53 activation in JB6 Cl41 cells. Toxicol Appl Pharmacol 245(2):226-235
13. Bagchi D, Vuchetich P, Bagchi M, Hassoun E, Tran M, Tang L, Stohs S (1997) Induction of oxidative stress by chronic administration of sodium dichromate [chromium VI] and cadmium chloride [cadmium II] to rats. Free Radic Biol Med 22(3):471-478
14. Murray A, Hunt t (1993) The cell cycle: an introduction. Oxford University Press, New York
15. Elledge SJ (1996) Cell cycle checkpoints: preventing an identity crisis. Science 274(5293):1664
16. Kops GJ, Weaver BA, Cleveland DW (2005) On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5(10):773-785. doi: 10.1038/nrc1714
17. Wang S, Leonard SS, Ye J, Ding M, Shi X (2000) The role of hydroxyl radical as a messenger in Cr(VI)-induced p53 activation. Am J Physiol Cell Physiol 279(3):C868-C875
18. Zhang Z, Leonard SS, Wang S, Vallyathan V, Castranova V, Shi X (2001) CR (VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol Cell Biochem 222(1):77-83
19. Singh J, Carlisle DL, Pritchard DE, Patierno S (1998) Chromium-induced genotoxicity and apoptosis: relationship to chromium carcinogenesis (review). Oncol Rep 5(6):1307
20. Bagchi D, Bagchi M, Stohs SJ (2001) Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Mol Cell Biochem 222(1):149-158
21. Ryberg D, Alexander J (1984) Inhibitory action of hexavalent chromium (Cr(VI)) on the mitochondrial respiration and a possible coupling to the reduction of Cr(VI). Biochem Pharmacol 33(15):2461-2466
22. Shi X, Dalal N (1990) Evidence for a Fenton-type mechanism for the generation of. OH radicals in the reduction of Cr(VI) in cellular media. Arch Biochem Biophys 281(1):90-95
23. Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 19(3):201-213
24. Ye J, Wang S, Leonard SS, Sun Y, Butterworth L, Antonini J, Ding M, Rojanasakul Y, Vallyathan V, Castranova V, Shi X (1999) Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J Biol Chem 274(49):34974-34980
25. Finkel T, Hwang PM (2009) The Krebs cycle meets the cell cycle: mitochondria and the G1-S transition. Proc Natl Acad Sci USA 106(29):11825-11826. doi: 10.1073/pnas.0906430106
26. Cinatl J Jr, Cinatl J, Driever PH, Kotchetkov R, Pouckova P, Kornhuber B, Schwabe D (1997) Sodium valproate inhibits in vivo growth of human neuroblastoma cells. Anticancer Drugs 8(10):958-963
27. Brustovetsky N, Brustovetsky T, Jemmerson R, Dubinsky JM (2002) Calcium-induced Cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J Neurochem 80(2):207-218
28. 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. doi: S0003269776699996 [pii]
29. Spach PI, Cunningham CC (1987) Control of state 3 respiration in liver mitochondria from rats subjected to chronic ethanol consumption. Biochim Biophys Acta 894(3):460-467
30. Emaus RK, Grunwald R, Lemasters JJ (1986) Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties. Biochim Biophys Acta 850(3):436-448
31. Ekinci R, Kadakal C (2005) Determination of seven water-soluble vitamins in Tarhana, a traditional Turkish cereal food, by high-performance liquid chromatography. ACTA chromatographica 15:289
32. Berry MN, Gregory RB, Grivell AR, Henly DC, Nobes CD, Phillips JW, Wallace PG (1988) Intracellular mitochondrial membrane potential as an indicator of hepatocyte energy metabolism: further evidence for thermodynamic control of metabolism. Biochimica et Biophysica Acta (BBA)-Bioenergetics 936(3):294-306
33. Kaur G, Stetler-Stevenson M, Sebers S, Worland P, Sedlacek H, Myers C, Czech J, Naik R, Sausville E (1992) Growth inhibition with reversible cell cycle arrest of carcinoma cells by flavone L86-8275. J Natl Cancer Inst 84(22):1736-1740
34. Chinni SR, Li Y, Upadhyay S, Koppolu PK, Sarkar FH (2001) Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene 20(23):2927
35. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria. J Biol Chem 278(38):36027-36031
36. Liu Y, Fiskum G, Schubert D (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J Neurochem 80(5):780-787
37. Wilbur SB, Corporation SR, Substances USAfT, Registry D (2000) Toxicological profile for chromium. US Dept. of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry
38. Kamo N, Muratsugu M, Hongoh R, Kobatake Y (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J Membr Biol 49(2):105-121
39. Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. In: National Acad Sciences
40. Fernandes M, Santos M, Alpoim M, Madeira V, Vicente J (2002) Chromium (VI) interaction with plant and animal mitochondrial bioenergetics: a comparative study. J Biochem Mol Toxicol 16(2):53-63
41. Yen TC, Chen YS, King KL, Yeh SH, Wei YH (1989) Liver mitochondrial respiratory functions decline with age. Biochem Biophys Res Commun 165(3):994-1003
42. Chomova M, Racay P (2010) Mitochondrial complex I in the network of known and unknown facts. Gen Physiol Biophys 29:3-11
43. Sholl-Franco A, Fragel-Madeira L, Macama Ada C, Linden R, Ventura AL (2010) ATP controls cell cycle and induces proliferation in the mouse developing retina. Int J Dev Neurosci 28(1):63-73. doi: 10.1016/j.ijdevneu.2009.09.004
44. Xu J, Bubley GJ, Detrick B, Blankenship LJ, Patierno SR (1996) CARCINOGENESIS: chromium (VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA-DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis 17(7):1511-1517
45. Lee EA, Keutmann MK, Dowling ML, Harris E, Chan G, Kao GD (2004) Inactivation of the mitotic checkpoint as a determinant of the efficacy of microtubule-targeted drugs in killing human cancer cells. Mol Cancer Ther 3(6):661
46. Guadagno TM, Newport JW (1996) Cdk2 kinase is required for entry into mitosis as a positive regulator of Cdc2-cyclin B kinase activity. Cell 84(1):73-82
47. Wade Harper J, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75(4):805-816
48. Wang XW, Zhan Q, Coursen JD, Khan MA, Kontny HU, Yu L, Hollander MC, Ohonnor PM, Fornace AJ, Harris CC (1999) GADD45 induction of a G2/M cell cycle checkpoint. Proc Natl Acad Sci 96(7):3706
49. Jin S, Tong T, Fan W, Fan F, Antinore MJ, Zhu X, Mazzacurati L, Li X, Petrik KL, Rajasekaran B (2002) GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene 21(57):8696
50. Oikawa T, Okuda M, Ma Z, Goorha R, Tsujimoto H, Inokuma H, Fukasawa K (2005) Transcriptional control of BubR1 by p53 and suppression of centrosome amplification by BubR1. Mol Cell Biol 25(10):4046
51. Ceryak S, Zingariello C, O'Brien T, Patierno SR (2004) Induction of pro-apoptotic and cell cycle-inhibiting genes in chromium (VI)-treated human lung fibroblasts: lack of effect of ERK. Mol Cell Biochem 255(1):139-149
52. Tully DB, Collins BJ, Overstreet JD, Smith CS, Dinse GE, Mumtaz MM, Chapin RE (2000) Effects of arsenic, cadmium, chromium, and lead on gene expression regulated by a battery of 13 different promoters in recombinant HepG2 cells. Toxicol Appl Pharmacol 168(2):79-90
53. García-Ruiz C, Colell A, Marí M, Morales A, Fernández-Checa JC (1997) Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. J Biol Chem 272(17):11369
54. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277(47):44784-44790
55. Walters J, Pop C, Scott FL, Drag M, Swartz P, Mattos C, Salvesen GS, Clark AC (2009) A constitutively active and uninhibitable caspase-3 zymogen efficiently induces apoptosis. Biochem J 424(3):335-345. doi: 10.1042/BJ20090825
56. Abu-Qare AW, Abou-Donia MB (2001) Biomarkers of apoptosis: release of cytochrome c, activation of caspase-3, induction of 8-hydroxy-2′- deoxyguanosine, increased 3-nitrotyrosine, and alteration of p53 gene. J Toxicol Environ Health Part B 4(3):313
57. Paitel E, Fahraeus R, Checler F (2003) Cellular prion protein sensitizes neurons to apoptotic stimuli through Mdm2-regulated and p53-dependent caspase 3-like activation. J Biol Chem 278(12):10061
58. Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM (2006) Cellular senescence in aging primates. Science 311(5765):1257