Chronic exposure to zinc chromate induces centrosome amplification and spindle assembly checkpoint bypass in human lung fibroblasts

Chemical Research in Toxicology

Volumn 23, Issue 2, 2010, Pages 386-395

  Holmes, Amie L ^a   Wise, Sandra S ^a   Pelsue, Stephen C ^a   Aboueissa, Abou El Makarim ^a   Lingle, Wilma ^b   Salisbury, Jeffery ^b   Gallagher, Jamie ^a   Wise Sr , John Pierce ^a  

^a UNIVERSITY OF SOUTHERN MAINE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMIC ACID; UNCLASSIFIED DRUG; ZINC CHROMATE;

ANAPHASE; ANEUPLOIDY; ARTICLE; CENTROSOME; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DIPLOIDY; HUMAN; HUMAN CELL; INTERPHASE; LONG TERM EXPOSURE; LUNG FIBROBLAST; MITOSIS; SPINDLE CELL;

ANEUPLOIDY; CELL LINE; CENTROSOME; CHROMATES; CHROMOSOMAL INSTABILITY; FIBROBLASTS; HUMANS; LUNG; MITOTIC SPINDLE APPARATUS; PARTICLE SIZE; SOLUBILITY; ZINC COMPOUNDS;

EID: 77049101013     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx900360w     Document Type: Article

References (56)

1. IARC (1990) Chromium, Nickel and Welding. IARC Monogr. EVal. Carcinog. Risk Hum. 49, 1-648.
2. Léonard, A., and Lauwerys, R. R. (1980) Carcinogenicity and mutagenicity of chromium. Mutat. Res. 76, 227-239.
3. Levy, L. S., and Vanitt, S. (1986) Carcinogenicity and mutagenicity of chromium compounds: The association between bronchial metaplasia and neoplasia. Carcinogenesis 7, 831-835.
4. Patierno, S. R., Banh, D., and Landolph, J. R. (1988) Transformation of C3H/10T1/2 mouse embryo cells by insoluble lead chromate but not soluble calcium chromate: Relationship to mutagenesis and internalization of lead chromate particles. Cancer Res. 47, 3815-3823.
5. Ishikawa, Y., Nakagawa, K., Satoh, Y., Kitagawa, T., Sugano, H, Hirano, T., and Tsuchiya, E. (1994) Characteristics of chromate workers' cancers, chromium lung deposition and precancerous bronchial lesions: An autopsy study. Br. J. Cancer 70, 160-166.
6. Ishikawa, Y., Nakagawa, K., Satoh, Y., Kitagawa, T., Sugano, H., Hirano, T., and Tsuchiya, E. (1994) "Hot spots" of chromium accumulation at bifurcations of chromate workers' bronchi. Cancer Res. 54, 2342-2346.
7. Holmes, A. L., Wise, S. S., and Wise, J. P., Sr. (2008) Carcinogenicity of hexavalent chromium. Indian J. Med. Res. 128, 353-372.
8. Wistuba, I. I., Bryant, D., Behrens, C., Milchgrub, S., Virmani, A. K., Ashfaq, R., Minna, J. D., and Gazdar, A. F. (1999) Comparison of features of human lung cancer cell lines and their corresponding tumors. Clin. Cancer Res. 5, 991-1000.
9. Hirose, T., Kondo, K., Takahashi, Y., Ishikura, H., Fujino, H., Tsuyuguchi, M., et al. (2002) Frequent microsatellite instability in lung cancer from chromate-exposed workers. Mol. Carcinog. 33, 172-180.
10. Takahashi, Y., Kondo, K., Hirose, T., Nakagawa, H., Tsuyuguchi, M., Hashimoto, M., et al. (2005) Microsatellite instability and protein expression of the DNA mismatch repair gene, hMLH1, of lung cancer in chromate-exposed workers. Mol. Carinog. 42, 150-158.
11. Reynolds, M., Stoddard, L., Bespalov, I., and Zhitkovich, A. (2007) 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. 35, 465-476.
12. Peterson-Roth, E., Reynolds, M., Quievryn, G., and Zhitkovich, A. (2005) Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Mol. Cell. Biol. 25, 3596-3607.
13. Wise, S. S., Holmes, A. L., Ketterer, M. E., Hartsock, W. J., Fomchenko, E., Katsfis, S. P., Thompson, W. D., and Wise, J. P., Sr. (2004) Chromium is the proximate clastogenic species for lead chromate-induced clastogenicity in human bronchial cells. Mutat. Res. 560, 79-89.
14. Wise, J. P., Sr., Wise, S. S., and Little, J. E. (2002) Thecytotoxicity and genotoxicity of particulate and soluble hexavalent chromium in human lung cells. Mutat. Res. 517, 221-229.
15. Wise, S. S., Schuler, J. H. C., and Katsifis, S. P., Sr. (2003) Barium chromate is cytotoxic and genotoxic to human lung cells. Environ. Mol. Mutagen. 42, 274-278.
16. Wise, S. S., Elmore, L. W., Holt, S. E., Little, J. E., and Bryant, B. H., Sr. (2004) Telomerase-mediated lifespan extension of human bronchial cells does not affect hexavalent chromium-induced cytotoxicity or genotoxicity. Mol. Cell. Biochem. 255, 103-111.
17. Wise, S. S., Schuler, J. H. C., Holmes, A. L., Katsifis, S. P., Ketterer, M. E., Hartsock, W. J., and Zheng, T., Sr. (2004) A comparison of two carcinogenic particulate hexavalent chromium compounds: Barium chromate is more genotoxic than lead chromate in human lung cells. Environ. Mol. Mutagen. 44, 156-162.
18. Xie, H., Wise, S. S., Holmes, A. L., Xu, B., Wakeman, T., Pelsue, S. C., and Singh, N. P., Sr. (2005) Carcinogenic lead chromate induces DNA double-strand breaks in human lung cells. Mutat. Res. 586, 160-172.
19. The Final Standard on Hexavalent Chromium. (2006) Effective and Practical Protection for Workers, Occupational Safety & Health Administration, Washington, DC.
20. Holmes, A. L., Wise, S. S., Sandwick, S. J., Lingle, W. L., Negron, V. C., Thompson, W. D., and Wise, J. P., Sr. (2006) Chronic exposure to lead chromate causes centrosome abnormalities and aneuploidy in human lung cells. Cancer Res. 4041-4048.
21. Wise, S. S., Holmes, A. L., Xie, H., Thompson, W. D., and Wise, J. P., Sr. (2006) Chronic exposure to particulate chromate induces spindle assembly checkpoint bypass in human lung cells. Chem. Res. Toxicol. 19, 1492-1498.
22. Masuda, A., and Takahashi, T. (2002) Chromosome instability in human lung cancers: possible underlying mechanisms and potential consequences in the pathogenesis. Oncogene 21, 6884-6897.
23. Taylor, S. S., Scott, M. I., and Holland, A. J. (2004) The spindle checkpoint: A quality control mechanism which ensures accurate chromosome segregation. Chromosome Res. 12, 599-616.
24. Fukasaw, K. (2005) Centrosome amplification, chromosome instability and cancer development. Cancer Lett. 230, 6-19.
25. D'Assoro, A. B., Lingle, W. L., and Salisbury, J. L. (2002) Centrosome amplification and the development of cancer. Oncogene 21, 4146-6153.
26. Dalager, N. A., Mason, T. J., Jr., Hoover, R., and Payne, W. W. (1980) Cancer mortality among workers exposed to zinc chromate paints. J. Occup. Med. 22, 25-29.
27. Davies, J. M. (1984) Lung cancer mortality among workers making lead chromate and zinc chromate pigments at three English factories. Br. J. Ind. Med. 41, 158-169.
28. Langard, S., and Norseth, T. (1975) A cohort study of bronchial carcinomas in workers producing chromate pigments. Br. J. Ind. Med. 32, 62-65.
29. Langård, S., and Vigander, T. (1983) Occurrence of lung cancer in workers producing chromium pigments. Br. J. Ind. Med. 40, 71-74.
30. Sheffet, A., Thind, I., Miller, A. M., and Louria, D. B. (1982) Cancer mortality in a pigment plant utilizing lead and zinc chromates. Arch. Environ. Health 37, 44-52.
31. Levy, L. S., Martin, P. A., and Bidstrup, P. L. (1986) Investigation of the potential carcinogenicity of a range of chromium containing materials on rat lung. Br. J. Ind. Med. 43, 243-256.
32. Elias, Z., Poirot, O., Pezerat, H., Suquet, H., Schneider, O., Danière, M. C., Terzetti, F., Baruthio, F., Fournier, M., and Cavelier, C. (1989) Cytotoxic and neoplastic transforming effects of industrial hexavalent chromium pigments in Syrian hamster embryo cells. Carcinogenesis 10, 2043-2052.
33. Myers, J. M., Antholine, W. E., and Myers, C. R. (2008) Hexavalent chromium causes the oxidation of thioredoxin in human bronchial epithelial cells. Toxicology 246, 222-233.
34. Xie, H., Holmes, A. L., Young, J. L., Qin, Q., Joyce, K., Pelsue, S. C., Peng, C., Wise, S. S., Jeevarajan, A. S., Wallace, W. T., Hammond, D., and Wise, J. P., Sr. (2009) Zinc chromate induces chromosome instability and DNA double strand breaks in human lung cells. Toxicol. Appl. Pharmacol. 234, 293-299.
35. Wise, S. S., Holmes, A. L., Moreland, J. A., Xie, H., Sandwick, S. J., Stackpole, M. M., Fomchenko, E., Teufack, S., May, A.J. Jr., Katsifis, S. P., and Wise, J. P., Sr. (2005) Human lung cell growth is not stimulated by lead ions after lead chromate-induced genotoxicity. Mol. Cell. Biochem. 279, 75-84.
36. Guerci, A., Seoane, A., and Dulout, F. N. (2000) Aneugenic effects of some metal compounds assessed by chromosome counting in MRChuman cells. Mutat. Res. 469, 35-40.
37. Seoase, A. I., Guerci, A. M., and Dulout, F. N. (2002) Malsegregation as a possible mechanism of aneuploidy induction by metal salts in MRC-5 human cells. Environ. Mol. Mutagen. 40, 200-206.
38. Dobson, J. H., Bourke, E., Jeffers, L. J., Vagnarelli, P., Sonoda, E., Takeda, S., Earnshaw, W. C., Merdes, A., and Morrison, C. (2003) Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J. 23, 3864-3873.
39. Balczon, R., Bao, L., Zimmer, W., Brown, K., Zinkowski, R. P., and Brinkley, B. R. (1995) Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyureaarrested Chinese hamster ovary cells. J. Cell. Biol. 130, 105-115.
40. Xie, H., Holmes, A. L., Wise, S. S., Gordon, N., and Wise, J. P., Sr. (2004) Lead chromate-induced chromosome damage requires extracellular dissolution to liberate chromium ions but does not require particle internalization or intracellular dissolution. Chem. Res. Toxicol. 17, 1362-1367.
41. Holmes, A. L., Wise, S. S., Sandwick, S. J., and Wise, J. P., Sr. (2006) The clastogenic effects of chronic exposure to particulate and soluble Cr(VI) in human lung cells. Mutat. Res. 610, 8-13.
42. Wise, S. S., Holmes, A. L., and Wise, J. P., Sr. (2006) Particulate and soluble hexavalent chromium are cytotoxic and genotoxic to human lung epithelial cells. Mutat. Res. 610, 2-7.
43. Yih, L. H., and Lee, T. C. (2003) Induction of C-anaphase and diplochromosome through dysregulation of spindle assembly checkpoint by sodium arsenite in human fibroblasts. Cancer Res. 63 (20), 6680-6688.
44. Yih, L. H., Ho, I. C., and Lee, T. C. (1997) Sodium arsenite disturbs mitosis and induces chromosome loss in human fibroblasts. Cancer Res. 57, 5051-5059.
45. Pihan, G. A., Purohit, A., Wallace, J., Knecht, H., Woda, B., Quesenberry, P., and Doxsey, S. J. (1998) Centrosome defects and genetic instability in malignant tumors. Cancer Res. 58, 3974-3985.
46. Ochi, T. (2002) Induction of centrosome injury, multipolar spindles and multipolar division in cultured V79 cells exposed to dimethylarsinic acid: Role for microtubules in centrosome dynamics. Mutat. Res. 454, 21-33.
47. Ochi, T. (2002) Role of mitotic motors, dynein and kinesin, in the induction of abnormal centrosome integrity and multipolar spindles in cultured V79 cells exposed to dimethylarsinic acid. Mutat. Res. 499, 73-84.
48. Ochi, T., Suzuki, T., Barrett, J. C., and Tsutsui, T. (2004) A trivalent dimethylarsenic compound, dimethylarsine iodide, induces cellular transformation, aneuploidy, centrosome abnormality and multipolar spindle formation in Syrian hamster embryo cells. Toxicology 203, 155-163.
49. Ochi, T. (2002) Methylmercury, but not inorganic mercury, causes abnormality of centrosome integrity (multiple foci of ?-tubulin), multipolar spindles and multinucleated cells without microtubule disruption in cultured Chinese hamster V79 cells. Toxicology 175, 111-121.
50. Taylor, B. F., McNeely, S. C., Miller, H. L., and States, J. C. (2008) Arsenite-induced mitotic death involves stress response and is independent of tubulin polymerization. Toxicol. Appl. Pharmacol. 230, 235-246.
51. Wakeman, T. P., Wyczechowska, D., and Xu, B. (2005) Involvement of the p38 MAP kinase in Cr(VI)-induced growth arrest and apoptosis. Mol. Cell. Biochem. 279, 69-73.
52. Zhang, Z., Leonard, S. S., Wang, S., Vallyathan, V., Castranova, V., and Shi, X. (2001) Cr (VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol. Cell. Biochem. 222, 77-83.
53. Wise, J. P., Sr., Leonard, J. C., and Patierno, S. R. (1992) Clastogenicity of lead chromate particles in hamster and human cells. Mutat. Res. 278, 69-79.
54. Singh, J., Pritchard, D. E., Carlisle, D. L., Mclean, J. A., Montaser, A., Orenstein, J. M., and Patierno, S. R. (1999) 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. 161, 240-248.
55. Holmes, A. L., Wise, S. S., Xie, H., Gordon, N., and Thompson, W. D., Sr. (2005) Lead ions do not cause human lung cells to escape chromateinduced cytotoxicity. Toxicol. Appl. Pharmacol. 303, 167-176.
56. Wise, J. P., Stearns, D. M., Wetterhahn, K. E., and Patierno, S. R. (1994) Cell-enhanced dissolution of carcinogenic lead chromate particles: The role of individual dissolution products in clastogenesis. Carcinogenesis 15, 2249-2254.