Abstract
Recent progress in risk assessment of nickel carcinogenicity and its correlation with occupational lung cancer in nickel-exposed workers is reviewed. Epidemiological investigations provide reliable data indicating the close relation between nickel exposure and high lung cancer risk, especially in nickel refineries. The nickel species-specific effects and the dose-response relationship between nickel exposure and lung cancer are among the main questions that are explored extensively. It is also suggested that some confounding factors such as cigarette smoking cannot be neglected. The determination of nickel concentration in lung tissue may be conducive to estimating the nickel exposure level, but it is uncertain whether the high nickel content in lung tissue indicates high lung cancer risk in nickel-exposed workers. Immunologic studies suggest that the suppressive effect of nickel on NK cell activity and interferon production may also be involved in the mechanisms of nickel carcinogenesis. As a potential mutagen, nickel can cause chromosome damage both in vitro and in vivo; and on a molecular basis, nickel is found to induce DNA damage (DNA strandbreaks and crosslinks, infidelity of DNA replication, inhibition of DNA repair, and the helical transition of B-DNA to Z-DNA) by binding of nickel ions to DNA and nuclear proteins. The discovery of oncogene promises both a challenge and an opportunity for nickel carcinogenesis research. It can be predicted that, with the rapid development of molecular biology and oncology, new approaches will be established for both understanding and controlling nickel-induced occupational lung cancer.
Full text
PDF







Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adachi S., Takemoto K., Ohshima S., Shimizu Y., Takahama M. Metal concentrations in lung tissue of subjects suffering from lung cancer. Int Arch Occup Environ Health. 1991;63(3):193–197. doi: 10.1007/BF00381568. [DOI] [PubMed] [Google Scholar]
- Akslen L. A., Myking A. O., Mørkve O., Gulsvik A., Raithel H. J., Schaller K. H. Increased content of chromium and nickel in lung tissues from patients with bronchial carcinoma. Pathol Res Pract. 1990 Dec;186(6):717–722. doi: 10.1016/S0344-0338(11)80261-X. [DOI] [PubMed] [Google Scholar]
- Andersen I., Svenes K. B. Determination of nickel in lung specimens of thirty-nine autopsied nickel workers. Int Arch Occup Environ Health. 1989;61(4):289–295. doi: 10.1007/BF00381428. [DOI] [PubMed] [Google Scholar]
- Bartsch P., Collignon A., Weber G., Robaye G., Delbrouck J. M., Roelandts I., Yujie J. Distribution of metals in human lung: analysis by particle induced x-ray emission. Arch Environ Health. 1982 Mar-Apr;37(2):111–117. doi: 10.1080/00039896.1982.10667546. [DOI] [PubMed] [Google Scholar]
- Brandt-Rauf P. W. New markers for monitoring occupational cancer: the example of oncogene proteins. J Occup Med. 1988 May;30(5):399–404. doi: 10.1097/00043764-198805000-00005. [DOI] [PubMed] [Google Scholar]
- Brandt-Rauf P. W. Oncogene proteins as biomarkers in the molecular epidemiology of occupational carcinogenesis. The example of the ras oncogene-encoded p21 protein. Int Arch Occup Environ Health. 1991;63(1):1–8. doi: 10.1007/BF00406190. [DOI] [PubMed] [Google Scholar]
- Brandt-Rauf P. W., Pincus M. R. Oncogenes and oncogene proteins. Occup Med. 1987 Jan-Mar;2(1):27–38. [PubMed] [Google Scholar]
- Brandt-Rauf P. W., Smith S., Perera F. P., Niman H. L., Yohannan W., Hemminki K., Santella R. M. Serum oncogene proteins in foundry workers. J Soc Occup Med. 1990 Spring;40(1):11–14. doi: 10.1093/occmed/40.1.11. [DOI] [PubMed] [Google Scholar]
- Chovil A., Sutherland R. B., Halliday M. Respiratory cancer in a cohort of nickel sinter plant workers. Br J Ind Med. 1981 Nov;38(4):327–333. doi: 10.1136/oem.38.4.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ciccarelli R. B., Hampton T. H., Jennette K. W. Nickel carbonate induces DNA-protein crosslinks and DNA strand breaks in rat kidney. Cancer Lett. 1981 May;12(4):349–354. doi: 10.1016/0304-3835(81)90178-6. [DOI] [PubMed] [Google Scholar]
- Ciccarelli R. B., Wetterhahn K. E. Nickel distribution and DNA lesions induced in rat tissues by the carcinogen nickel carbonate. Cancer Res. 1982 Sep;42(9):3544–3549. [PubMed] [Google Scholar]
- Conway K., Costa M. Nonrandom chromosomal alterations in nickel-transformed Chinese hamster embryo cells. Cancer Res. 1989 Nov 1;49(21):6032–6038. [PubMed] [Google Scholar]
- Conway K., Costa M. The involvement of heterochromatic damage in nickel-induced transformation. Biol Trace Elem Res. 1989 Jul-Sep;21:437–444. doi: 10.1007/BF02917286. [DOI] [PubMed] [Google Scholar]
- Conway K., Wang X. W., Xu L. S., Costa M. Effect of magnesium on nickel-induced genotoxicity and cell transformation. Carcinogenesis. 1987 Aug;8(8):1115–1121. doi: 10.1093/carcin/8.8.1115. [DOI] [PubMed] [Google Scholar]
- Costa M. Perspectives on the mechanism of nickel carcinogenesis gained from models of in vitro carcinogenesis. Environ Health Perspect. 1989 May;81:73–76. doi: 10.1289/ehp.898173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Datta A. K., Riggs C. W., Fivash M. J., Jr, Kasprzak K. S. Mechanisms of nickel carcinogenesis. Interaction of Ni(II) with 2'-deoxynucleosides and 2'-deoxynucleotides. Chem Biol Interact. 1991;79(3):323–334. doi: 10.1016/0009-2797(91)90112-k. [DOI] [PubMed] [Google Scholar]
- Doll R., Mathews J. D., Morgan L. G. Cancers of the lung and nasal sinuses in nickel workers: a reassessment of the period of risk. Br J Ind Med. 1977 May;34(2):102–105. doi: 10.1136/oem.34.2.102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edelman D. A., Roggli V. L. The accumulation of nickel in human lungs. Environ Health Perspect. 1989 May;81:221–224. doi: 10.1289/ehp.8981221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elias Z., Mur J. M., Pierre F., Gilgenkrantz S., Schneider O., Baruthio F., Danière M. C., Fontana J. M. Chromosome aberrations in peripheral blood lymphocytes of welders and characterization of their exposure by biological samples analysis. J Occup Med. 1989 May;31(5):477–483. [PubMed] [Google Scholar]
- Enterline P. E., Marsh G. M. Mortality among workers in a nickel refinery and alloy manufacturing plant in West Virginia. J Natl Cancer Inst. 1982 Jun;68(6):925–933. [PubMed] [Google Scholar]
- Evans R. M., Davies P. J., Costa M. Video time-lapse microscopy of phagocytosis and intracellular fate of crystalline nickel sulfide particles in cultured mammalian cells. Cancer Res. 1982 Jul;42(7):2729–2735. [PubMed] [Google Scholar]
- Farber E. Possible etiologic mechanisms in chemical carcinogenesis. Environ Health Perspect. 1987 Nov;75:65–70. [PMC free article] [PubMed] [Google Scholar]
- Grandjean P., Andersen O., Nielsen G. D. Carcinogenicity of occupational nickel exposures: an evaluation of the epidemiological evidence. Am J Ind Med. 1988;13(2):193–209. doi: 10.1002/ajim.4700130202. [DOI] [PubMed] [Google Scholar]
- Haley P. J., Shopp G. M., Benson J. M., Cheng Y. S., Bice D. E., Luster M. I., Dunnick J. K., Hobbs C. H. The immunotoxicity of three nickel compounds following 13-week inhalation exposure in the mouse. Fundam Appl Toxicol. 1990 Oct;15(3):476–487. doi: 10.1016/0272-0590(90)90034-h. [DOI] [PubMed] [Google Scholar]
- Hamm R. D. Occupational cancer in the oncogene era. Br J Ind Med. 1990 Apr;47(4):217–220. doi: 10.1136/oem.47.4.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haugen A., Ryberg D., Hansteen I. L., Dalen H. Transformation of human kidney epithelial cells to tumorigenicity by nickel(II) and V-HA-RAS oncogene. Biol Trace Elem Res. 1989 Jul-Sep;21:451–458. doi: 10.1007/BF02917288. [DOI] [PubMed] [Google Scholar]
- Huebner K., Isobe M., Gasson J. C., Golde D. W., Croce C. M. Localization of the gene encoding human erythroid-potentiating activity to chromosome region Xp11.1----Xp11.4. Am J Hum Genet. 1986 Jun;38(6):819–826. [PMC free article] [PubMed] [Google Scholar]
- Huebner R. J., Todaro G. J. Oncogenes of RNA tumor viruses as determinants of cancer. Proc Natl Acad Sci U S A. 1969 Nov;64(3):1087–1094. doi: 10.1073/pnas.64.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaramillo A., Sonnenfeld G. Effects of amorphous and crystalline nickel sulfide on induction of interferons-alpha/beta and -gamma and interleukin-2. Environ Res. 1989 Apr;48(2):275–286. doi: 10.1016/s0013-9351(89)80040-4. [DOI] [PubMed] [Google Scholar]
- Judde J. G., Breillout F., Clemenceau C., Poupon M. F., Jasmin C. Inhibition of rat natural killer cell function by carcinogenic nickel compounds: preventive action of manganese. J Natl Cancer Inst. 1987 Jun;78(6):1185–1190. [PubMed] [Google Scholar]
- Kasprzak K. S., Quander R. V., Poirier L. A. Effects of calcium and magnesium salts on nickel subsulfide carcinogenicity in Fischer rats. Carcinogenesis. 1985 Aug;6(8):1161–1166. doi: 10.1093/carcin/6.8.1161. [DOI] [PubMed] [Google Scholar]
- Kasprzak K. S., Ward J. M. Prevention of nickel subsulfide carcinogenesis by local administration of Mycobacterium bovis antigen in male F344/NCr rats. Toxicology. 1991 Mar 25;67(1):97–105. doi: 10.1016/0300-483x(91)90167-y. [DOI] [PubMed] [Google Scholar]
- Kollmeier H., Seemann J. W., Müller K. M., Rothe G., Wittig P., Schejbal V. B. Increased chromium and nickel content in lung tissue and bronchial carcinoma. Am J Ind Med. 1987;11(6):659–669. doi: 10.1002/ajim.4700110607. [DOI] [PubMed] [Google Scholar]
- Kollmeier H., Seemann J. W., Rothe G., Müller K. M., Wittig P. Age, sex, and region adjusted concentrations of chromium and nickel in lung tissue. Br J Ind Med. 1990 Oct;47(10):682–687. doi: 10.1136/oem.47.10.682. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kollmeier H., Witting C., Seemann J., Wittig P., Rothe R. Increased chromium and nickel content in lung tissue. J Cancer Res Clin Oncol. 1985;110(2):173–176. doi: 10.1007/BF00402735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kotlar H. K., Boysen M., Sanner T. A serum immune factor in detection of an occupational group with increased risk for lung and nose cancer. Eur J Cancer Clin Oncol. 1982 Oct;18(10):957–965. doi: 10.1016/0277-5379(82)90244-9. [DOI] [PubMed] [Google Scholar]
- Kreyberg L. Lung cancer in workers in a nickel refinery. Br J Ind Med. 1978 May;35(2):109–116. doi: 10.1136/oem.35.2.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Langer A. M., Rohl A. N., Selikoff I. J., Harlow G. E., Prinz M. Asbestos as a cofactor in carcinogenesis among nickel-processing workers. Science. 1980 Jul 18;209(4454):420–422. doi: 10.1126/science.7384817. [DOI] [PubMed] [Google Scholar]
- Lee J. E., Ciccarelli R. B., Jennette K. W. Solubilization of the carcinogen nickel subsulfide and its interaction with deoxyribonucleic acid and protein. Biochemistry. 1982 Feb 16;21(4):771–778. doi: 10.1021/bi00533a030. [DOI] [PubMed] [Google Scholar]
- Liquier J., Bourtayre P., Pizzorni L., Sournies F., Labarre J. F., Taillandier E. Spectroscopic studies of conformational transitions in double stranded DNAs in the presence of carcinogenic nickel compounds and an antitumoral drug (SOAZ). Anticancer Res. 1984 Jan-Apr;4(1-2):41–44. [PubMed] [Google Scholar]
- Littlefield N. A., Fullerton F. R., Poirier L. A. Hydroxylation and deglycosylation of 2'-deoxyguanosine in the presence of magnesium and nickel. Chem Biol Interact. 1991;79(2):217–228. doi: 10.1016/0009-2797(91)90084-k. [DOI] [PubMed] [Google Scholar]
- Léonard A., Gerber G. B., Jacquet P. Carcinogenicity, mutagenicity and teratogenicity of nickel. Mutat Res. 1981 Jul;87(1):1–15. doi: 10.1016/0165-1110(81)90002-6. [DOI] [PubMed] [Google Scholar]
- Magnus K., Andersen A., Høgetveit A. C. Cancer of respiratory organs among workers at a nickel refinery in Norway. Int J Cancer. 1982 Dec 15;30(6):681–685. doi: 10.1002/ijc.2910300602. [DOI] [PubMed] [Google Scholar]
- Martin Mateo M. C., Rabadan J., Boustamante J. Comparative analysis of certain metals and tumor markers in bronchopulmonary cancer and colorectal cancers. Metals and tumor markers in the neoplastic process. Clin Physiol Biochem. 1990;8(5):261–266. [PubMed] [Google Scholar]
- Mastromatteo E. Yant memorial lecture. Nickel. Am Ind Hyg Assoc J. 1986 Oct;47(10):589–601. doi: 10.1080/15298668691390304. [DOI] [PubMed] [Google Scholar]
- Newman S. M., Summitt R. L., Nunez L. J. Incidence of nickel-induced sister-chromatid exchange. Mutat Res. 1982 Mar;101(1):67–75. doi: 10.1016/0165-1218(82)90166-5. [DOI] [PubMed] [Google Scholar]
- Nishimura M., Umeda M. Inducation of chromosomal aberrations in cultured mammalian cells by nickel compounds. Mutat Res. 1979 Dec;68(4):337–349. doi: 10.1016/0165-1218(79)90166-6. [DOI] [PubMed] [Google Scholar]
- Ono H., Wada O., Ono T. Distribution of trace metals in nuclei and nucleoli of normal and regenerating rat liver with special reference to the different behavior of nickel and chromium. J Toxicol Environ Health. 1981 Nov-Dec;8(5-6):947–957. doi: 10.1080/15287398109530129. [DOI] [PubMed] [Google Scholar]
- Patierno S. R., Costa M. DNA-protein cross-links induced by nickel compounds in intact cultured mammalian cells. Chem Biol Interact. 1985 Oct;55(1-2):75–91. doi: 10.1016/s0009-2797(85)80121-6. [DOI] [PubMed] [Google Scholar]
- Patierno S. R., Sugiyama M., Basilion J. P., Costa M. Preferential DNA-protein cross-linking by NiCl2 in magnesium-insoluble regions of fractionated Chinese hamster ovary cell chromatin. Cancer Res. 1985 Nov;45(11 Pt 2):5787–5794. [PubMed] [Google Scholar]
- Pedersen E., Hogetveit A. C., Andersen A. Cancer of respiratory organs among workers at a nickel refinery in Norway. Int J Cancer. 1973 Jul 15;12(1):32–41. doi: 10.1002/ijc.2910120104. [DOI] [PubMed] [Google Scholar]
- Raithel H. J., Schaller K. H., Akslen L. A., Myking A. O., Mørkve O., Gulsvik A. Analyses of chromium and nickel in human pulmonary tissue. Investigations in lung cancer patients and a control population under special consideration of medical expertise aspects. Int Arch Occup Environ Health. 1989;61(8):507–512. doi: 10.1007/BF00683120. [DOI] [PubMed] [Google Scholar]
- Raithel H. J., Schaller K. H., Reith A., Svenes K. B., Valentin H. Investigations on the quantitative determination of nickel and chromium in human lung tissue. Industrial medical, toxicological, and occupational medical expertise aspects. Int Arch Occup Environ Health. 1988;60(1):55–66. doi: 10.1007/BF00409380. [DOI] [PubMed] [Google Scholar]
- Reddy E. P., Reynolds R. K., Santos E., Barbacid M. A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene. Nature. 1982 Nov 11;300(5888):149–152. doi: 10.1038/300149a0. [DOI] [PubMed] [Google Scholar]
- Reynolds S. H., Anderson M. W. Activation of proto-oncogenes in human and mouse lung tumors. Environ Health Perspect. 1991 Jun;93:145–148. doi: 10.1289/ehp.9193145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rezuke W. N., Knight J. A., Sunderman F. W., Jr Reference values for nickel concentrations in human tissues and bile. Am J Ind Med. 1987;11(4):419–426. doi: 10.1002/ajim.4700110404. [DOI] [PubMed] [Google Scholar]
- Roberts R. S., Julian J. A., Muir D. C., Shannon H. S. A study of mortality in workers engaged in the mining, smelting, and refining of nickel. II: Mortality from cancer of the respiratory tract and kidney. Toxicol Ind Health. 1989 Dec;5(6):975–993. doi: 10.1177/074823378900500606. [DOI] [PubMed] [Google Scholar]
- Roberts R. S., Julian J. A., Sweezey D., Muir D. C., Shannon H. S., Mastromatteo E. A study of mortality in workers engaged in the mining, smelting, and refining of nickel. I: Methodology and mortality by major cause groups. Toxicol Ind Health. 1989 Dec;5(6):957–974. doi: 10.1177/074823378900500605. [DOI] [PubMed] [Google Scholar]
- Robison S. H., Cantoni O., Costa M. Analysis of metal-induced DNA lesions and DNA-repair replication in mammalian cells. Mutat Res. 1984 Mar-Apr;131(3-4):173–181. doi: 10.1016/0167-8817(84)90058-0. [DOI] [PubMed] [Google Scholar]
- Robison S. H., Cantoni O., Costa M. Strand breakage and decreased molecular weight of DNA induced by specific metal compounds. Carcinogenesis. 1982;3(6):657–662. doi: 10.1093/carcin/3.6.657. [DOI] [PubMed] [Google Scholar]
- Robison S. H., Cantoni O., Heck J. D., Costa M. Soluble and insoluble nickel compounds induce DNA repair synthesis in cultured mammalian cells. Cancer Lett. 1983 Jan;17(3):273–279. doi: 10.1016/0304-3835(83)90164-7. [DOI] [PubMed] [Google Scholar]
- Robison S. H., Costa M. The induction of DNA strand breakage by nickel compounds in cultured Chinese hamster ovary cells. Cancer Lett. 1982 Jan;15(1):35–40. doi: 10.1016/0304-3835(82)90073-8. [DOI] [PubMed] [Google Scholar]
- Saxholm H. J., Reith A., Brøgger A. Oncogenic transformation and cell lysis in C3H/10T 1/2 cells and increased sister chromatid exchange in human lymphocytes by nickel subsulfide. Cancer Res. 1981 Oct;41(10):4136–4139. [PubMed] [Google Scholar]
- Schaaper R. M., Koplitz R. M., Tkeshelashvili L. K., Loeb L. A. Metal-induced lethality and mutagenesis: possible role of apurinic intermediates. Mutat Res. 1987 Apr;177(2):179–188. doi: 10.1016/0027-5107(87)90001-7. [DOI] [PubMed] [Google Scholar]
- Seeburg P. H., Colby W. W., Capon D. J., Goeddel D. V., Levinson A. D. Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature. 1984 Nov 1;312(5989):71–75. doi: 10.1038/312071a0. [DOI] [PubMed] [Google Scholar]
- Sen P., Conway K., Costa M. Comparison of the localization of chromosome damage induced by calcium chromate and nickel compounds. Cancer Res. 1987 Apr 15;47(8):2142–2147. [PubMed] [Google Scholar]
- Sen P., Costa M. Incidence and localization of sister chromatid exchanges induced by nickel and chromium compounds. Carcinogenesis. 1986 Sep;7(9):1527–1533. doi: 10.1093/carcin/7.9.1527. [DOI] [PubMed] [Google Scholar]
- Sen P., Costa M. Induction of chromosomal damage in Chinese hamster ovary cells by soluble and particulate nickel compounds: preferential fragmentation of the heterochromatic long arm of the X-chromosome by carcinogenic crystalline NiS particles. Cancer Res. 1985 May;45(5):2320–2325. [PubMed] [Google Scholar]
- Sen P., Costa M. Pathway of nickel uptake influences its interaction with heterochromatic DNA. Toxicol Appl Pharmacol. 1986 Jun 30;84(2):278–285. doi: 10.1016/0041-008x(86)90135-3. [DOI] [PubMed] [Google Scholar]
- Shannon H. S., Julian J. A., Roberts R. S. A mortality study of 11,500 nickel workers. J Natl Cancer Inst. 1984 Dec;73(6):1251–1258. [PubMed] [Google Scholar]
- Sirover M. A., Loeb L. A. Infidelity of DNA synthesis in vitro: screening for potential metal mutagens or carcinogens. Science. 1976 Dec 24;194(4272):1434–1436. doi: 10.1126/science.1006310. [DOI] [PubMed] [Google Scholar]
- Smialowicz R. J., Rogers R. R., Riddle M. M., Garner R. J., Rowe D. G., Luebke R. W. Immunologic effects of nickel. II. Suppression of natural killer cell activity. Environ Res. 1985 Feb;36(1):56–66. doi: 10.1016/0013-9351(85)90007-6. [DOI] [PubMed] [Google Scholar]
- Smialowicz R. J., Rogers R. R., Riddle M. M., Stott G. A. Immunologic effects of nickel: I. Suppression of cellular and humoral immunity. Environ Res. 1984 Apr;33(2):413–427. doi: 10.1016/0013-9351(84)90039-2. [DOI] [PubMed] [Google Scholar]
- Smialowicz R. J., Rogers R. R., Rowe D. G., Riddle M. M., Luebke R. W. The effects of nickel on immune function in the rat. Toxicology. 1987 Jun;44(3):271–281. doi: 10.1016/0300-483x(87)90029-1. [DOI] [PubMed] [Google Scholar]
- Sorahan T., Burges D. C., Waterhouse J. A. A mortality study of nickel/chromium platers. Br J Ind Med. 1987 Apr;44(4):250–258. doi: 10.1136/oem.44.4.250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sorahan T. Mortality from lung cancer among a cohort of nickel cadmium battery workers: 1946-84. Br J Ind Med. 1987 Dec;44(12):803–809. doi: 10.1136/oem.44.12.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sunderman F. W., Jr Mechanisms of nickel carcinogenesis. Scand J Work Environ Health. 1989 Feb;15(1):1–12. doi: 10.5271/sjweh.1888. [DOI] [PubMed] [Google Scholar]
- Swierenga S. H., Gilman J. P., McLean J. R. Cancer risk from inorganics. Cancer Metastasis Rev. 1987;6(2):113–154. doi: 10.1007/BF00052846. [DOI] [PubMed] [Google Scholar]
- Taillandier E., Taboury J. A., Adam S., Liquier J. Left-handed helical structure of poly[d(A-C)].poly[d(G-T)] studied by infrared spectroscopy. Biochemistry. 1984 Nov 20;23(24):5703–5706. doi: 10.1021/bi00319a007. [DOI] [PubMed] [Google Scholar]
- Taylor J. A. Oncogenes and their applications in epidemiologic studies. Am J Epidemiol. 1989 Jul;130(1):6–13. doi: 10.1093/oxfordjournals.aje.a115323. [DOI] [PubMed] [Google Scholar]
- Treagan L., Furst A. Inhibition of interferon synthesis in mammalian cell cultures after nickel treatment. Res Commun Chem Pathol Pharmacol. 1970 May;1(3):395–402. [PubMed] [Google Scholar]
- Waksvik H., Boysen M. Cytogenetic analyses of lymphocytes from workers in a nickel refinery. Mutat Res. 1982 Feb;103(2):185–190. doi: 10.1016/0165-7992(82)90027-6. [DOI] [PubMed] [Google Scholar]
- Waksvik H., Boysen M., Høgetveit A. C. Increased incidence of chromosomal aberrations in peripheral lymphocytes of retired nickel workers. Carcinogenesis. 1984 Nov;5(11):1525–1527. doi: 10.1093/carcin/5.11.1525. [DOI] [PubMed] [Google Scholar]
- Wittinghofer F., Krengel U., John J., Kabsch W., Pai E. F. Three-dimensional structure of p21 in the active conformation and analysis of an oncogenic mutant. Environ Health Perspect. 1991 Jun;93:11–15. doi: 10.1289/ehp.919311. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wulf H. C. Sister chromatid exchanges in human lymphocytes exposed to nickel and lead. Preliminary communication. Dan Med Bull. 1980 Feb;27(1):40–42. [PubMed] [Google Scholar]
- Zakour R. A., Tkeshelashvili L. K., Shearman C. W., Koplitz R. M., Loeb L. A. Metal-induced infidelity of DNA synthesis. J Cancer Res Clin Oncol. 1981;99(1-2):187–196. doi: 10.1007/BF00412453. [DOI] [PMC free article] [PubMed] [Google Scholar]
