Synchrotron-based imaging of chromium and γ-H2AX immunostaining in the duodenum following repeated exposure to Cr(VI) in drinking water

Toxicological Sciences

Volumn 143, Issue 1, 2015, Pages 16-25

  Thompson, Chad M ^a   Seiter, Jennifer ^b   Chappell, Mark A ^b   Tappero, Ryan V ^c   Proctor, Deborah M ^a   Suh, Mina ^a   Wolf, Jeffrey C ^d   Haws, Laurie C ^a   Vitale, Rock ^e   Mittal, Liz ^a   Kirman, Christopher R ^f   Hays, Sean M ^f   Harris, Mark A ^a  

^a ToxStrategies Inc   (United States)

^b US ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

^d EXPERIMENTAL PATHOLOGY LABORATORIES INC   (United States)

^e Environmental Standards Inc   (United States)

^f LLP   (United States)

Author keywords

Carcinogenesis; Cr(VI); Duodenum; H2AX; Hexavalent chromium; Mode of action; Synchrotron

Indexed keywords

CHROMIUM; CHROMIUM VI; DRINKING WATER; GAMMA H2AX; HISTONE H2AX; UNCLASSIFIED DRUG; CHROMIC ACID; CHROMIUM HEXAVALENT ION; DICHROMATE SODIUM; H2AX PROTEIN, MOUSE; HISTONE; WATER POLLUTANT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B6C3F1 MOUSE; CHRONIC WOUND; CONTROLLED STUDY; CRYPT CELL; DNA DAMAGE; DUODENUM; DUODENUM TUMOR; FEMALE; HISTOPATHOLOGY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINAL STEM CELL; INTESTINE MUCOSA; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; RAT; X RAY FLUORESCENCE; ANIMAL; CELL TRANSFORMATION; CHEMICALLY INDUCED; DRUG EFFECTS; FISCHER 344 RAT; GENETICS; INTESTINE ABSORPTION; METABOLISM; MICROSPECTROPHOTOMETRY; MICROVILLUS; PATHOLOGY; RISK ASSESSMENT; SPECTROMETRY; SYNCHROTRON; TIME FACTOR; TOXICITY; WATER POLLUTANT;

MUS; RODENTIA;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATES; CHROMIUM; DNA DAMAGE; DUODENAL NEOPLASMS; DUODENUM; FEMALE; HISTONES; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; MICE; MICROSPECTROPHOTOMETRY; MICROVILLI; RATS, INBRED F344; RISK ASSESSMENT; SPECTROMETRY, X-RAY EMISSION; SYNCHROTRONS; TIME FACTORS; WATER POLLUTANTS, CHEMICAL;

EID: 84928676214     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu206     Document Type: Article

References (49)

1. Barker, N., Ridgway, R. A., van Es, J. H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A. R., Sansom, O. J., and Clevers, H. (2009). Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-612.
2. Bonner, W. M., Redon, C. E., Dickey, J. S., Nakamura, A. J., Sedelnikova, O. A., Solier, S., and Pommier, Y. (2008). GammaH2AX and cancer. Nat. Rev. Cancer 8, 957-967.
3. Cohen, S. M. (2010). An enhanced thirteen-week bioassay as an alternative for screening for carcinogenesis factors. Asian Pac. J. Cancer Prev. 11, 15-17.
4. Cohen, S. M., Gordon, E. B., Singh, P., Arce, G. T., and Nyska, A. (2010). Carcinogenic mode of action of folpet in mice and evaluation of its relevance to humans. Crit. Rev. Toxicol. 40, 531-545.
5. De Flora, S. (1978). Metabolic deactivation of mutagens in the Salmonella-microsome test. Nature 271, 455-456.
6. De Flora, S., Camoirano, A., Bagnasco, M., Bennicelli, C., Corbett, G. E., and Kerger, B. D. (1997). Estimates of the chromium(VI) reducing capacity in human body compartments as a mechanism for attenuating its potential toxicity and carcinogenicity. Carcinogenesis 18, 531-537.
7. DeSesso, J. M., and Jacobson, C. F. (2001). Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem. Toxicol. 39, 209-228.
8. Ellis, A. S., Johnson, T. M., and Bullen, T. D. (2002). Chromium isotopes and the fate of hexavalent chromium in the environment. Science 295, 2060-2062.
9. Gaylor, D. W. (2005). Are tumor incidence rates from chronic bioassays telling us what we need to know about carcinogens? Regul. Toxicol. Pharmacol. 41, 128-133.
10. Gordon, E. (2007). Captan: Transition from 'B2' to 'not likely'. How pesticide registrants affected the EPA Cancer Classification Update. J. Appl. Toxicol. 27, 519-526.
11. Greaves, P. (2012). Histopathology of Preclinical Toxicity Studies 4th ed. Elsevier-Academic Press, London.
12. Greenfield, R. E., Ellwein, L. B., and Cohen, S. M. (1984). A general probabilistic model of carcinogenesis: Analysis of experimental urinary bladder cancer. Carcinogenesis 5, 437-445.
13. Hixon, G., and Bichteler, A. (2013). drsmooth: Dose-response modeling with smoothing splines. R package version 1.0. Available at: http://cran.r-project.org/web/packages/drsmooth/index.html. Accessed October 16, 2014.
14. Kinner, A., Wu, W., Staudt, C., and Iliakis, G. (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36, 5678-5694.
15. Kirman, C. R., Hays, S. M., Aylward, L. L., Suh, M., Harris, M. A., Thompson, C. M., Haws, L. C., and Proctor, D. M. (2012). Physiologically based pharmacokinetic model for rats andmice orally exposed to chromium. Chem. Biol. Interact. 200, 45-64.
16. Kirman, C. R., Aylward, L. L., Suh, M., Harris, M. A., Thompson, C. M., Haws, L. C., Proctor, D. M., Lin, S. S., Parker, W., and Hays, S. M. (2013). Physiologically based pharmacokinetic model for humans orally exposed to chromium. Chem. Biol. Interact.204, 13-27.
17. Kopec, A. K., Kim, S., Forgacs, A. L., Zacharewski, T. R., Proctor, D.M., Harris, M. A., Haws, L. C., and Thompson, C. M. (2012). Genome-wide gene expression effects in B6C3F1 mouse intestinal epithelia following 7 and 90days of exposure to hexavalent chromium in drinking water. Toxicol. Appl. Pharmacol.259, 13-26.
18. Lanzirotti, L., and Sutton, S. (2002). Hard X-ray microprobe. National Synchrotron Light Source. Available at: http://www.bnl.gov/ps/nsls/newsroom/publications/otherpubs/imaging/hardxraymicroprobe.pdf. Accessed October 16, 2014.
19. Mackenzie, R. D., Byerrum, R. U., Decker, C. F., Hoppert, C. A., and Langham, R. F. (1958). Chronic toxicity studies. II. Hexavalent and trivalent chromium administered in drinking water to rats. AMA Arch. Ind. Health 18, 232-234.
20. McCarroll, N., Keshava, N., Chen, J., Akerman, G., Kligerman, A., and Rinde, E. (2010). An evaluation of the mode of action framework for mutagenic carcinogens case study II: Chromium (VI). Environ. Mol. Mutagen. 51, 89-111.
21. McNeill, L. S., Mclean, J. E., Parks, J. L., and Edwards, M. A. (2012). Hexavalent chromium review, part 2: Chemistry, occurrence, and treatment. J. Am. Waterworks Assoc. 104, E395-E405.
22. Moolgavkar, S. H., and Knudson, A. G., Jr. (1981). Mutation and cancer: A model for human carcinogenesis. J. Natl Cancer Inst.66, 1037-1052.
23. Nickens, K. P., Patierno, S. R., and Ceryak, S. (2010). Chromium genotoxicity: A double-edged sword. Chem. Biol. Interact. 188, 276-288.
24. NTP (2007). National Toxicology Program technical report on the toxicity studies of sodium dichromate dihydrate (CAS No. 7789-12-0) administered in drinking water to male and female F344/N rats and B6C3F1 mice and male BALB/c and am3-C57BL/6 mice. NTP Toxicity Report Series Number 72, NIH Publication No. 07-5964.
25. NTP (2008a). National Toxicology Program technical report on the toxicology and carcinogenesis studies of chromium picolinate monohydrate (CAS NO. 27882-76-4) in F344/N rats and B6C3F1 mice (feed studies). NIH Publication No. 08-5897.
26. NTP (2008b). National Toxicology Program technical report on the toxicology and carcinogenesis studies of sodium dichromate dihydrate (CAS No. 7789-12-0) in F344/N rats and B6C3F1 mice (drinking water studies), NTP TR 546. NIHPublication No08-5887.
27. O'Brien, T. J., Ceryak, S., and Patierno, S. R. (2003). Complexities of chromium carcinogenesis: Role of cellular response, repair and recovery mechanisms. Mutat. Res. 533, 3-36.
28. O'Brien, T. J., Ding, H., Suh, M., Thompson, C. M., Parsons, B. L., Harris, M. A., Winkelman, W. A., Wolf, J. C., Hixon, J. G., Schwartz, A. M., Myers, M. B., Haws, L. C., and Proctor, D. M. (2013). Assessment of K-Ras mutant frequency and micronucleus incidence in the mouse duodenum following 90-days of exposure to Cr(VI) in drinking water. Mutat. Res. 754, 15-21.
29. OEHHA (2011). Final technical support document on public health goal for hexavalent chromium in drinking water. Pesticide and Environmental Toxicology Branch, Office of Environmental Health Hazard Assessment, California Environmental Protection Agency.
30. Oze, C., Bird, D. K., and Fendorf, S. (2007). Genesis of hexavalent chromium from natural sources in soil and groundwater. Proc. Natl Acad. Sci. USA 104, 6544-6549.
31. Potten, C. S., and Loeffler, M. (1990). Stem cells: Attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020.
32. Proctor, D. M., Suh, M., Aylward, L. L., Kirman, C. R., Harris, M. A., Thompson, C. M., Gurleyuk, H., Gerads, R., Haws, L. C., and Hays, S. M. (2012). Hexavalent chromium reduction kinetics in rodent stomach contents. Chemosphere 89, 487-493.
33. Rizk, P., and Barker, N. (2012). Gut stem cells in tissue renewal and disease: Methods, markers, and myths. Wiley interdisciplinary reviews. Sys. Biol. Med. 4, 475-496.
34. Rousseau, R. M. (2001). Detection limit and estimate of uncertainty of analytical XRF results. Rigaku 18, 33-47.
35. Schuijers, J., and Clevers, H. (2012). Adult mammalian stem cells: The role of Wnt, Lgr5 and R-spondins. Embo J. 31, 3031-3032.
36. Schwitalla, S., Fingerle, A. A., Cammareri, P., Nebelsiek, T., Goktuna, S. I., Ziegler, P. K., Canli, O., Heijmans, J., Huels, D. J., Moreaux, G., et al. (2013). Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152, 25-38.
37. Stout, M. D., Herbert, R. A., Kissling, G. E., Collins, B. J., Travlos, G.S., Witt, K. L., Melnick, R. L., Abdo, K. M., Malarkey, D. E., and Hooth, M. J. (2009a). Hexavalent chromium is carcinogenic to F344/N rats and B6C3F1 mice after chronic oral exposure. Environ. Health Perspect. 117, 716-722.
38. Stout, M. D., Nyska, A., Collins, B. J., Witt, K. L., Kissling, G. E., Malarkey, D. E., and Hooth, M. J. (2009b). Chronic toxicity and carcinogenicity studies of chromium picolinate monohydrate administered in feed to F344/N rats and B6C3F1 mice for 2 years. Food Chem. Toxicol. 47, 729-733.
39. Thompson, C. M., Proctor, D. M., Haws, L. C., Hebert, C. D., Grimes, S. D., Shertzer, H. G., Kopec, A. K., Hixon, J. G., Zacharewski, T. R., and Harris, M. A. (2011). Investigation of the mode of action underlying the tumorigenic response induced in B6C3F1 mice exposed orally to hexavalent chromium. Toxicol. Sci. 123, 58-70.
40. Thompson, C. M., Fedorov, Y., D., B. D., Suh, M., Proctor, D. M., Kuriakose, L., Haws, L. C., and Harris, M. A. (2012a). Assessment of Cr(VI)-induced cytotoxicity and genotoxicity using high content analysis. PLoS One 7, e42720.
41. Thompson, C. M., Proctor, D. M., Suh, M., Haws, L. C., Hebert, C.D., Mann, J. F., Shertzer, H. G., Hixon, J. G., and Harris, M. A. (2012b). Comparison of the effects of hexavalent chromium in the alimentary canal of F344 rats and B6C3F1 mice following exposure in drinking water: Implications for carcinogenic modes of action. Toxicol. Sci. 125, 79-90.
42. Thompson, C. M., Proctor, D. M., Suh, M., Haws, L. C., Kirman, C. R., and Harris, M. A. (2013). Assessment of the mode of action underlying development of rodent small intestinal tumors following oral exposure to hexavalent chromium and relevance to humans. Crit. Rev. Toxicol. 43, 244-274.
43. U.S. EPA (1991). National primary drinking water regulationssynthetic organic chemicals and inorganic chemicals; monitoring for unregulated contaminants; national primary drinking water regulations implementation; national secondary drinking water regulations. Final rule. Fed. Reg. 56, 3526-3597.
44. U.S. Environmental Protection Agency (EPA) (1998). Toxicological review of hexavalent chromium in support of summary information on the integrated risk information system (IRIS). U.S. Environmental Protection Agency, Washinton, D.C.
45. U.S. EPA (2004). Captan; cancer reclassification; Amendment of reregistration eligibility decision; notice of availability. Fed.Reg. 69, 68357-68360.
46. U.S. EPA (2013). Regional Screening Levels. Available at: http://www.epa.gov/region9/superfund/prg/. Accessed October 16, 2014.
47. U.S. EPA (2014). The Third Unregulated Contaminant Monitoring Rule (UCMR3): Occurrence Data. Available at: http://water.epa.gov/lawsregs/rulesregs/sdwa/ucmr/data.cfm. Accessed August 14, 2014.
48. van der Flier, L. G., and Clevers, H. (2009). Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu.Rev. Physiol. 71, 241-260.
49. Zhitkovich, A. (2011). Chromium in drinking water: Sources, metabolism, and cancer risks. Chem. Res. Toxicol. 24, 1617-1629.