Induction of morphological changes in BEAS-2B human bronchial epithelial cells following chronic sub-cytotoxic and mildly cytotoxic hexavalent chromium exposures

Molecular Carcinogenesis

Volumn 49, Issue 6, 2010, Pages 582-591

  Costa, André N ^a   Moreno, Virtudes ^a   Prieto, María J ^a   Urbano, Ana M ^b,c,d   Alpoim, M Carmen ^b,d,e  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

BEAS 2B cells; Cellular models; Chronic exposures; Hexavalent chromium; Transformation

Indexed keywords

CHROMIUM;

APOPTOSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL CULTURE; CELL GROWTH; CELL INTERACTION; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; EPITHELIUM CELL; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; PHENOTYPE; PRIORITY JOURNAL;

CARCINOGENS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHROMIUM; EPITHELIAL CELLS; HUMANS; RESPIRATORY MUCOSA; TIME FACTORS;

EID: 77953902669     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20624     Document Type: Article

References (87)

1. International Agency for Research on Cancer. Chromium, nickel and welding. In: IARC monographs on the evaluation of carcinogenic risks to humans, Vol. 49. Lyon: IARC Scientific Publications; 1990.
2. World Health Organization. Chromium. In: Environmental health criteria, Vol. 61. Geneva: WHO; 1988.
3. USEPA. Integrated risk information system (IRIS). Cincinnati, OH: US Environmental Protection Agency; Environmental Criteria and Assessment Office; 1992.
4. O'Brien TJ, Ceryak S, Patierno SR. Complexities of chromium carcinogenesis: Role of cellular response, repair and recovery mechanisms. Mutat Res/Fundam Mol Mech Mutagen 2003; 533:3-36.
5. Barceloux DG. Chromium. J Toxicol Clin Toxicol 1999;37: 173-194.
6. De Flora S, Bagnasco M, Serra D, Zanacchi P. Genotoxicity of chromium compounds. A review. Mutat Res 1990;238:99-172.
7. Urbano AM, Rodrigues CFD, Alpoim MC. Hexavalent chromium exposure, genomic instability and lung cancer. Gene Ther Mol Biol 2008;12:219-238.
8. Stearns DM, Wetterhahn KE. Reaction of Cr(VI) with ascorbate produces chromium(V), chromium(IV), and carbon-based radicals. Chem Res Toxicol 1994;7:219-230.
9. Connett PH, Wetterhahn KE. Metabolism of the carcinogen chromate by cellular constituents. Struct Bond 1983;54:93-124.
10. Suzuki Y, Fukuda K. Reduction of hexavalent chromium by ascorbic acid and glutathione with special reference to the rat lung. Arch Toxicol 1990;64:169-176. (Pubitemid 20151258)
11. Quievryn G, Goulart M, Messer J, Zhitkovich A. Reduction of Cr(VI) by cysteine: Significance in human lymphocytes and formation of DNA damage in reactions with variable reduction rates. Mol Cell Biochem 2001;222:107-118. (Pubitemid 32910326)
12. Standeven AM, Wetterhahn KE. Ascorbate is the principal reductant of chromium(VI) in rat lung ultrafiltrates and cytosols and mediates chromium-DNA binding in vitro. Carcinogenesis 1992;13:1319-1324.
13. Bose RN, Moghadda S, Gelerinter E. Long-lived chromium(IV) and chromium(V) metabolites in the chromium(VI)-glutathione reaction: NMR, ESR, HPLC, and kinetic characterization. Inorg Chem 1992;31:1987-1994.
14. Sugden KD, Stearns DM. The role of chromium(V) in the mechanism of chromate-induced oxidative DNA damage and cancer. J Environ Pathol Toxicol Oncol 2000;19:215-230.
15. Tsapakos MJ, Wetterhanh KE. The interaction of chromium with nucleic acids. Chem Biol Interact 1983;46:265-277.
16. Xu J, Bubley GJ, Detrick B, Blankenship LJ, Patierno SR. Chromium(VI) treatment of normal lung human cells results in guanine-specific DNA polymerase DNA arrest, DNA-DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis 1996;17:1511-1517.
17. Pritchard DE, Ceryak S, Ha L, et al. Mechanism of apoptosis and determination of cellular fate in chromium(VI)-exposed populations of telomerase-immortalized human fibroblasts. Cell Growth Differ 2001;12:487-496. (Pubitemid 33029874)
18. Blankenship LJ, Manning FCR, Orenstein JM, Patierno SR. Apoptosis is the mode of cell-death caused by carcinogenic chromium. Toxicol Appl Pharmacol 1994;126:75-83.
19. Patierno SR, Banh D, Landolph JR. Transformation of C3H/10T1/2 mouse embryo cells to focus formation and anchorage independence by insoluble lead but not soluble calcium chromate: Relationship to mutagenesis and internalization of lead chromate particle. Cancer Res 1988;48: 5280-5288.
20. Patierno SR, Landolph JR. Soluble vs. insoluble hexavalent chromate: Relationship of mutation to in vitro transformation and particle uptake. Biol Trace Elem Res 1989;21:469-474.
21. Bidermann KA, Landolph JR. Induction of anchorage independence in human diploid foreskin fibroblasts by carcinogenic metal salts. Cancer Res 1987;47:3815-3823.
22. Biedermann KA, Landolph JR. Role of valence state and solubility of chromium compounds on induction of cytotoxicity, mutagenesis, and anchorage independence in diploid human fibroblasts. Cancer Res 1990;50:7835-7842.
23. Kondo K, Hino N, Sasa M, et al. Mutations of the p53 gene in human lung cancer from chromate exposed workers. Biochem Biophys Res Commun 1997;239:95-100. (Pubitemid 27480322)
24. Kondo K, Takahashi Y, Hirose Y, et al. The reduced expression and aberrant methylation of p16(INK4a) in chromate workers with lung cancer. Lung Cancer 2006;53: 295-302. (Pubitemid 44192596)
25. Hirose T, Kondo K, Takahashi Y, et al. Frequent microsatellite instability in lung cancer from chromate-exposed workers. Mol Carcinog 2002;33:172-180.
26. Takahashi Y, Kondo K, Hirose T, et al. Microsatellite instability and protein expression of the DNA mismatch repair gene, hMLH1, of lung cancer in chromate-exposed workers. Mol Carcinog 2005;42:150-158. (Pubitemid 40271144)
27. Snow ET, Shu LS. Chromium(III) bound to DNA templates promotes increased polymerase processivity and decreased fidelity during replication in vitro. Biochemistry 1991;30: 11238-11245.
28. Snow ET, Shu LS. Effects of chromium(III) on DNA replication in vitro. Biol Trace Elem Res 1989;21:61-71. (Pubitemid 19256342)
29. Singh J, Snow ET. Chromium(III) decreases the fidelity of human polymerase b. Biochemistry 1998;37:9371-9378. (Pubitemid 28307691)
30. Snow ET. A possible role for chromium(III) in genotoxicity. Environ Health Perspect 1991;92:75-81.
31. 6-methylguanine. J Biol Chem 1996;271:28391- 28398.
32. Sirover MA, Loeb LA. Infidelity of DNA synthesis in vitro: Screening for potential mutagens or carcinogens. Science 1976;194:1434-1436.
33. Tkeshelashvili LK, Shearman CW, Zakour RA, Koplitz RM, Loeb LA. Effects of arsenic, selenium, and chromium on the fidelity of DNA synthesis. Cancer Res 1980;40:2455-2460. (Pubitemid 10082267)
34. Maeng SH, Chung HW, Yu IJ, et al. Changes of 8-OH-dG levels in DNA and its base excision repair activity in rat lungs after inhalation and exposure to hexavalent chromium. Mutat Res/Genet Toxicol Environ Mutagen 2003;539:109-116.
35. Hodges NJ, Chipman JK. Down-regulation of the DNA-repair endonuclease 8-oxo-guanine DNA glycosylase 1 (hOGG1) by sodium dichromate in cultured human A549 lung carcinoma cells. Carcinogenesis 2002;23:55-60.
36. Reynolds M, Zhitkovich A. Cellular vitamin C increases chromate toxicity via a death program requiring mismatch repair but not p53. Carcinogenesis 2007;28:1613-1620. (Pubitemid 47241813)
37. Peterson-Roth E, Reynolds M, Quievryn G, Zhitkovich A. Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Mol Cell Biol 2005;25:3596-3607. (Pubitemid 40559566)
38. Reynolds M, Stoddard L, Bespalov I, Zhitkovich A. Ascorbate acts as a highly potent inducer of chromate mutagenesis and clastogenesis: Linkage to DNA breaks in G2 phase by mismatch repair. Nucleic Acids Res 2007;35:465-476. (Pubitemid 46232064)
39. Wise JP, Sr., Wise SS, Little JE. The cytotoxicity and genotoxicity of particulate and soluble hexavalent chromium in human lung cells. Mutat Res/Genet Toxicol Environ Mutagen 2002;517:221-229.
40. Wise SS, Elmore LW, Holt SE, et al. Telomerase-mediated lifespan extension of human bronchial cells does not affect hexavalent chromium-induced cytotoxicity and genotoxicity. Mol Cell Biochem 2004;255:103-111.
41. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semi-automated colorimetric assay: Assessment of chemosensitivity testing. Cancer Res 1987;47:936-942. (Pubitemid 17027905)
42. Allen RT, Hunter WJ III, Agrawal DK. Morphological and biochemical characterization and analysis of apoptosis. J Pharmacol Toxicol Methods 1997;37:215-228.
43. Singh J, Pritchard DE, Carlisle DL, et al. Internalization of carcinogenic lead chromate particles by cultured normal human lung epithelial cells. Formation of intracellular lead-inclusion bodies and induction of apoptosis. Toxicol Appl Pharmacol 1999;161:240-248.
44. Lechner JF, LaVeck MA. A serum-free method for culturing normal human bronchial epithelial cells at clonal density. J Tissue Cult Method 1985;9:43-48.
45. Reddel RR, Ke Y, Gerwin BI, et al. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res 1988;48:1904-1909.
46. Dubrovskaya VA, Wetterhahn KE. Effects of Cr(VI) on the expression of the oxidative stress genes in human lung cells. Carcinogenesis 1998;19:1401-1407. (Pubitemid 28409838)
47. Sun SY, Yue P, Chen XY, Hong WK, Lotan R. The synthetic retinoid CF437 selectively induced apoptosis in human lung cancer cells while sparing normal human lung epithelial cells. Cancer Res 2002;62:2430-2436. (Pubitemid 34411728)
48. Ishikawa Y, Nakagawa K, Satoh Y, et al. Characteristics of chromate workers' cancers, chromium lung deposition and precancerous bronchial lesions: An autopsy study. Br J Cancer 1994;70:160-166. (Pubitemid 24203646)
49. Fornace AJ, Jr., Seres DS, Lechner JF, Harris CC. DNA-protein cross-linking by chromium salts. Chem Biol Interact 1981; 36:345-354.
50. Russo P, Catassi A, Cesario A, et al. Molecular mechanisms of hexavalent chromium-induced apoptosis in human bronchoalveolar cells. Am J Respir Cell Mol Biol 2005;33:589-600. (Pubitemid 41753135)
51. Wise SS, Holmes AL, Wise JP, Sr. Particulate and hexavalent chromium are cytotoxic and genotoxic to human lung cells. Mutat Res/Genet Toxicol Environ Mutagen 2006;610:2-7. (Pubitemid 44486900)
52. Xie H, Holmes AL, Wise SS, Huang SP, Peng C, Wise JP, Sr. Neoplastic transformation of human bronchial cells by lead chromate particles. Am J Respir Cell Mol Biol 2007;37:544-552.
53. Caglieri A, Goldoni M, De Palma G, et al. Exposure to low levels of hexavalent chromium: Target doses and comparative effects on two human pulmonary cell lines. Acta Biomed 2008;79:104-115.
54. Borthiry GR, Antholine WE, Myers JM, Myers CR. Reductive activation of hexavalent chromium by human lung epithelial cells: Generation of Cr(V) and Cr(V)-thiol species. J Inorg Biochem 2008;102:1449-1462.
55. Myers JM, Antholine WE, Myers CR. Hexavalent chromium causes the oxidation of thioredoxin in human bronchial epithelial cells. Toxicology 2008;246:222-233.
56. Schmid M, Zimmermann S, Krug HF, Sures B. Influence of platinum, palladium and rhodium as compared with cadmium, nickel and chromium on cell viability and oxidative stress in human bronchial epithelial cells. Environ Int 2007; 33:385-390.
57. O'Hara KA, Vaghjiani RJ, Nemec AA, Klei LR, Barchowsky A. Cr(VI)-stimulated STAT3 tyrosine phosphorylation and nuclear translocation in human airway epithelial cells requires Lck. Biochem J 2007;402:261-269.
58. Tessier DM, Pascal LE. Activation of MAP kinases by hexavalent chromium, manganese and nickel in human lung epithelial cells. Toxicol Lett 2006;167:114-121.
59. O'Hara KA, Nemec AA, Alam J, Klei LR, Mossman BT, Barchowsky A. Chromium (VI) inhibits heme oxygenase-1 expression in vivo and in arsenic-exposed human airway epithelial cells. J Cell Physiol 2006;209:113-121.
60. Andrew AS, Warren AJ, Barchowsky A, et al. Genomic and proteomic profiling of responses to toxic metals in human lung cells. Environ Health Perspect 2003;111:825-838.
61. Pascal LE, Tessier DM. Cytotoxicity of chromium and manganese to lung epithelial cells in vitro. Toxicol Lett 2004;147:143-151.
62. Linzer DI, Levine AJ. Characterization of a 54K Dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells. Cell 1979;17:43-52. (Pubitemid 9188209)
63. Lane DP, Crawford LV. T-Antigen is bound to a host protein in SV-40 transformed cells. Nature 1979;278:261-263.
64. De Caprio JA, Ludlow JW, Figge J, et al. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 1988;54:275-283.
65. Finlay CA, Hinds PW, Levine AJ. The p53 proto-oncogene can act as a suppressor of transformation. Cell 1989;57:1083-1093.
66. Ke Y, Reddel RR, Gerwin BI, et al. Human bronchial epithelial cells with integrated SV40 virus T antigen genes retain the ability to undergo squamous differentiation. Differentiation 1988;38:60-66.
67. Gerwin BI, Spillare E, Forrester K, et al. Mutant p53 can induce tumorigenic conversion of human bronchial epithelial cells and reduce their responsiveness to a negative growth factor, transforming growth factor β1. Proc Natl Acad Sci USA 1992;89:2759-2763.
68. Reddel RR, Salghetti SE, Willey JC, et al. Development of tumorigenicity in simian virus 40-immortalized human bronchial epithelial cell lines. Cancer Res 1993;53:985-991.
69. Folkman J, Moscona A. Role of cell shape in growth control. Nature 1978;273:345-349. (Pubitemid 8344174)
70. Ermolli M, Menné C, Pozzi G, Serra M-A, Clerici LA. Nickel, cobalt and chromium-induced cytotoxicity and intracellular accumulation in human hacat keratinocytes. Toxicology 2001;159:23-31. (Pubitemid 32203701)
71. Sehlmeyer U, Hechtenberg S, Klyszcz H, Beyersmann D. Accumulation of chromium in Chinese hamster V79 cells and nuclei. Arch Toxicol 1990;64:506-508. (Pubitemid 20271399)
72. Messer J, Reynolds M, Stoddard L, Zhitkovich A. Causes of DNA single-strand breaks during reduction of chromate by glutathione in vitro and in cells. Free Radic Biol Med 2006; 40:1981-1992. (Pubitemid 43728867)
73. Alexander J, Aaseth J. Uptake of chromate in human redblood-cells and isolated rat-liver cells: The role of the anion carrier. Analyst 1995;120:931-933.
74. Huang S, Ingber DE. Cell tension, matrix mechanics, and cancer development. Cancer Cell 2005;8:175-176. (Pubitemid 41317587)
75. Borg TK. It's the matrix! ECM, proteases, and cancer. Am J Pathol 2004;164:1141-1142.
76. Tilghman RW, Parsons JT. Focal adhesion kinase as a regulator of cell tension in the progression of cancer. Semin Cancer Biol 2008;18:45-52. (Pubitemid 350266368)
77. Di Leonardo A, Linke SP, Clarkin K, Wahl GM. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev 1994;8:2540-2551. (Pubitemid 24347245)
78. INK4a enrichment and the premature senescence of normal fibroblasts. Oncogene 1998;16: 1113-1123.
79. Chang B-D, Broude EV, Dokmanovic M, et al. A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Res 1999;59:3761-3767. (Pubitemid 29381884)
80. INK4a. Cell 1997; 88:593-602.
81. Weinberg RA. The cat and mouse games that genes, viruses and cells play. Cell 1997;88:573-575.
82. Dimri GP. What has senescence got to do with cancer? Cancer Cell 2005;7:505-512.
83. Rajaraman R, Guernsey DL, Rajaraman MM, Rajaraman SR. Stem cells, senescence, neosis and self-renewal in cancer. Cancer Cell Int 2006;6:25-50. (Pubitemid 44869912)
84. Rajaraman R, Rajaraman MM, Rajaraman SR, Guernsey DL. Neosis - A paradigm of self-renewal in cancer. Cell Biol Int 2005;29:1084-1097.
85. Campisi J. Senescent cells, tumor suppression, and organismal aging: Good citizens, bad neighbors. Cell 2005;120: 513-522. (Pubitemid 40269765)
86. White LR, Jakobsen K, Eik-Nes KB. Response of a human tumor cell line to chronic potassium dichromate exposure. Toxicology 1981;22:211-218. (Pubitemid 12198148)
87. Rodrigues CFD, Urbano AM, Matoso E, et al. Human bronchial epithelial cells malignantly transformed by hexavalent chromium exhibit an aneuploid phenotype but no microsatellite instability. Mutat Res/Fundam Mol Mech Mutagen 2009;670:42-52.