Abstract
Depleted uranium (DU) is a dense heavy metal used primarily in military applications. Although the health effects of occupational uranium exposure are well known, limited data exist regarding the long-term health effects of internalized DU in humans. We established an in vitro cellular model to study DU exposure. Microdosimetric assessment, determined using a Monte Carlo computer simulation based on measured intracellular and extracellular uranium levels, showed that few (0.0014%) cell nuclei were hit by alpha particles. We report the ability of DU-uranyl chloride to transform immortalized human osteoblastic cells (HOS) to the tumorigenic phenotype. DU-uranyl chloride-transformants are characterized by anchorage-independent growth, tumor formation in nude mice, expression of high levels of the k-ras oncogene, reduced production of the Rb tumor-suppressor protein, and elevated levels of sister chromatid exchanges per cell. DU-uranyl chloride treatment resulted in a 9.6 (+/- 2.8)-fold increase in transformation frequency compared to untreated cells. In comparison, nickel sulfate resulted in a 7.1 (+/- 2.1)-fold increase in transformation frequency. This is the first report showing that a DU compound caused human cell transformation to the neoplastic phenotype. Although additional studies are needed to determine if protracted DU exposure produces tumors in vivo, the implication from these in vitro results is that the risk of cancer induction from internalized DU exposure may be comparable to other biologically reactive and carcinogenic heavy-metal compounds (e.g., nickel).
MeSH Terms
Animals
Carcinogenicity Tests
Cell Transformation, Neoplastic/chemically induced
Chlorides/toxicity
Dose-Response Relationship, Drug
Female
Humans
Mice
Mice, Nude
Mutagenicity Tests
Osteoblasts/drug effects
Sister Chromatid Exchange
Tumor Cells, Cultured
Uranium Compounds/toxicity
Chemicals
Chlorides
Uranium Compounds
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Miller A C
Applied Cellular Radiobiology Department, Armed Forces Radiobiology Research Institute, Bethesda, MD 20889-5603 USA.
Blakely W F
Livengood D
Whittaker T
Xu J
Ejnik J W
Hamilton M M
Parlette E
John T S
Gerstenberg H M
Hsu H
References (30)
30 references, click to expand
-
Quantitative and qualitative studies of chemical transformation of cloned C3H mouse embryo cells sensitive to postconfluence inhibition of cell division.
Cancer Res. 1973 Dec;33(12):3239-49
PMID: 4796800
-
Malignant transformation of human prostate epithelial cells by N-nitroso-N-methylurea.
Cancer Res. 1997 Feb 15;57(4):576-80
PMID: 9044828
-
Fission-spectrum neutrons at reduced dose rates enhance neoplastic transformation.
Nature. 1982 Jul 1;298(5869):67-9
PMID: 7088163
-
Cellular transforming genes.
Science. 1982 Aug 27;217(4562):801-6
PMID: 6285471
-
Recent advances in metal carcinogenesis.
Ann Clin Lab Sci. 1984 Mar-Apr;14(2):93-122
PMID: 6201124
-
Activation of a c-K-ras oncogene by somatic mutation in mouse lymphomas induced by gamma radiation.
Science. 1984 Sep 14;225(4667):1159-62
PMID: 6474169
-
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):2320-5
PMID: 3986775
-
Metabolism of ingested U and Ra.
Health Phys. 1985 May;48(5):601-33
PMID: 3988524
-
Activation of c-myc and c-K-ras oncogenes in primary rat tumors induced by ionizing radiation.
Mol Cell Biol. 1987 Feb;7(2):932-5
PMID: 3547086
-
Tissue and subcellular distribution of bismuth radiotracer in the rat: considerations of cytotoxicity and microdosimetry for bismuth radiopharmaceuticals.
Radiat Res. 1987 Jul;111(1):119-29
PMID: 3602349
-
A microdosimetric model of astatine-211 labeled antibodies for radioimmunotherapy.
Int J Radiat Oncol Biol Phys. 1987 Nov;13(11):1767-73
PMID: 3667382
-
Transformation of C3H/10T1/2 mouse embryo cells to focus formation and anchorage independence by insoluble lead chromate but not soluble calcium chromate: relationship to mutagenesis and internalization of lead chromate particles.
Cancer Res. 1988 Sep 15;48(18):5280-8
PMID: 3409252
-
Genetic toxicology of lead compounds.
Carcinogenesis. 1988 Oct;9(10):1727-32
PMID: 3168150
-
Incidence of second neoplasms in patients with bilateral retinoblastoma.
Ophthalmology. 1988 Nov;95(11):1583-7
PMID: 3211467
-
Identification and characterization of a p53 gene mutation in a human osteosarcoma cell line.
Oncogene. 1989 Dec;4(12):1483-8
PMID: 2531855
-
Hydrogen peroxide-induced base damage in deoxyribonucleic acid.
Radiat Res. 1990 Mar;121(3):338-43
PMID: 2315450
-
Sister chromatid exchanges and inhibition of DNA synthesis in irradiated human cells.
Acta Biol Hung. 1990;41(1-3):209-13
PMID: 2151241
-
Tumor suppressor genes.
Science. 1991 Nov 22;254(5035):1138-46
PMID: 1659741
-
Transmission of chromosomal instability after plutonium alpha-particle irradiation.
Nature. 1992 Feb 20;355(6362):738-40
PMID: 1741061
-
Mutations of p53 and ras genes in radon-associated lung cancer from uranium miners.
Lancet. 1992 Mar 7;339(8793):576-80
PMID: 1347094
-
Induction of sister chromatid exchanges by extremely low doses of alpha-particles.
Cancer Res. 1992 Nov 15;52(22):6394-6
PMID: 1423287
-
Increased radioresistance of EJras-transformed human osteosarcoma cells and its modulation by lovastatin, an inhibitor of p21ras isoprenylation.
Int J Cancer. 1993 Jan 21;53(2):302-7
PMID: 8425769
-
Transformation of immortal, non-tumorigenic osteoblast-like human osteosarcoma cells to the tumorigenic phenotype by nickel sulfate.
Carcinogenesis. 1993 May;14(5):947-53
PMID: 8504488
-
Mechanisms of multistep carcinogenesis and carcinogen risk assessment.
Environ Health Perspect. 1993 Apr;100:9-20
PMID: 8354184
-
Plutonium-catalyzed oxidative DNA damage in the absence of significant alpha-particle decay.
Radiat Res. 1994 Jan;137(1):114-7
PMID: 8265780
-
Nickel-induced transformation of human cells causes loss of the phosphorylation of the retinoblastoma protein.
Cancer Res. 1994 May 15;54(10):2751-4
PMID: 8168106
-
Transformation of human osteoblasts to anchorage-independent growth by insoluble nickel particles.
Environ Health Perspect. 1994 Sep;102 Suppl 3:289-92
PMID: 7843117
-
Genomic instability induced by ionizing radiation.
Radiat Res. 1996 Sep;146(3):247-58
PMID: 8752302
-
Genomic instability in Chinese hamster cells after exposure to X rays or alpha particles of different mean linear energy transfer.
Radiat Res. 1997 Jan;147(1):22-8
PMID: 8989365
-
New Giemsa method for the differential staining of sister chromatids.
Nature. 1974 Sep 13;251(5471):156-8
PMID: 4138930