Genome-wide gene expression effects in B6C3F1 mouse intestinal epithelia following 7 and 90days of exposure to hexavalent chromium in drinking water

Toxicology and Applied Pharmacology

Volumn 259, Issue 1, 2012, Pages 13-26

  Kopec, Anna K ^a   Kim, Suntae ^a   Forgacs, Agnes L ^a   Zacharewski, Timothy R ^a   Proctor, Deborah M ^b   Harris, Mark A ^c   Haws, Laurie C ^d   Thompson, Chad M ^c  

^a Michigan State University   (United States)

^b ToxStrategies Inc   (United States)

^c ToxStrategies Inc   (United States)

^d ToxStrategies Inc   (United States)

Author keywords

Chromium; Cr(VI); Intestine; Microarray; Phenotypic anchoring; Toxicogenomics

Indexed keywords

CHROMIUM; DRINKING WATER; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE; CELL PROLIFERATION; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DUODENUM; ENVIRONMENTAL EXPOSURE; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; HISTOPATHOLOGY; IMMUNE RESPONSE; INTESTINE EPITHELIUM; JEJUNUM; LIPID METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; SIGMOID;

ANIMALS; CELL PROLIFERATION; CHROMIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRINKING WATER; DUODENUM; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME-WIDE ASSOCIATION STUDY; INTESTINAL MUCOSA; JEJUNUM; MICE; MICE, INBRED STRAINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; TIME FACTORS; WATER POLLUTANTS, CHEMICAL;

MUS;

EID: 84862777658     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.11.012     Document Type: Article

References (68)

1. Arivarasu N.A., Fatima S., Mahmood R. Oral administration of potassium dichromate inhibits brush border membrane enzymes and alters anti-oxidant status of rat intestine. Arch. Toxicol. 2008, 82:951-958.
2. AWWA Low-level hexavalent chromium treatment options: bench-scale evaluation 2004, AWWA Research Foundation, Denver, CO. P. Brandhuber, M. Frey, M. McGuire, J.P. Chao, C. Seidel, G. Amy, J. Yoon, L. McNeill, K. Banerjee (Eds.).
3. Azad N., Iyer A.K., Wang L., Lu Y., Medan D., Castranova V., Rojanasakul Y. Nitric oxide-mediated bcl-2 stabilization potentiates malignant transformation of human lung epithelial cells. Am. J. Respir. Cell. Mol. Biol. 2010, 42:578-585.
4. Boulton S.J. Cellular functions of the BRCA tumour-suppressor proteins. Biochem. Soc. Trans. 2006, 34:633-645.
5. Burgoon L.D., Eckel-Passow J.E., Gennings C., Boverhof D.R., Burt J.W., Fong C.J., Zacharewski T.R. Protocols for the assurance of microarray data quality and process control. Nucleic Acids Res. 2005, 33:e172.
6. Burgoon L.D., Zacharewski T.R. dbZach toxicogenomic information management system. Pharmacogenomics 2007, 8:287-291.
7. Burgoon L.D., Zacharewski T.R. Automated quantitative dose-response modeling and point of departure determination for large toxicogenomic and high-throughput screening data sets. Toxicol. Sci. 2008, 104:412-418.
8. CDHS Chromium-6 in drinking water: an overview of sampling results 2009.
9. Chowdhury S.R., King D.E., Willing B.P., Band M.R., Beever J.E., Lane A.B., Loor J.J., Marini J.C., Rund L.A., Schook L.B., Van Kessel A.G., Gaskins H.R. Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics 2007, 8:215.
10. D'Agostini F., Izzotti A., Bennicelli C., Camoirano A., Tampa E., De Flora S. Induction of apoptosis in the lung but not in the liver of rats receiving intra-tracheal instillations of chromium(VI). Carcinogenesis 2002, 23:587-593.
11. Dahm L.J., Jones D.P. Rat jejunum controls luminal thiol-disulfide redox. J. Nutr. 2000, 130:2739-2745.
12. Dayan A.D., Paine A.J. Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Hum. Exp. Toxicol. 2001, 20:439-451.
13. De Flora S., D'Agostini F., Balansky R., Micale R., Baluce B., Izzotti A. Lack of genotoxic effects in hematopoietic and gastrointestinal cells of mice receiving chromium(VI) with the drinking water. Mutat. Res. 2008, 659:60-67.
14. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003, 4:P3.
15. Di Bona K.R., Love S., Rhodes N.R., McAdory D., Sinha S.H., Kern N., Kent J., Strickland J., Wilson A., Beaird J., Ramage J., Rasco J.F., Vincent J.B. Chromium is not an essential trace element for mammals: effects of a "low-chromium" diet. J. Biol. Inorg. Chem. 2011, 16:381-390.
16. Dickinson D.A., Forman H.J. Glutathione in defense and signaling: lessons from a small thiol. Ann. N. Y. Acad. Sci. 2002, 973:488-504.
17. Dos Santos Ferreira V., Rocchetta I., Conforti V., Bench S., Feldman R., Levin M.J. Gene expression patterns in Euglena gracilis: insights into the cellular response to environmental stress. Gene 2007, 389:136-145.
18. Ebert B., Kisiela M., Malatkova P., El-Hawari Y., Maser E. Regulation of human carbonyl reductase 3 (CBR3; SDR21C2) expression by Nrf2 in cultured cancer cells. Biochemistry 2010, 49:8499-8511.
19. Eckel J.E., Gennings C., Chinchilli V.M., Burgoon L.D., Zacharewski T.R. Empirical Bayes gene screening tool for time-course or dose-response microarray data. J. Biopharm. Stat. 2004, 14:647-670.
20. Eckel J.E., Gennings C., Therneau T.M., Burgoon L.D., Boverhof D.R., Zacharewski T.R. Normalization of two-channel microarray experiments: a semiparametric approach. Bioinformatics 2005, 21:1078-1083.
21. Elliott P.J., Zollner T.M., Boehncke W.H. Proteasome inhibition: a new anti-inflammatory strategy. J. Mol. Med. 2003, 81:235-245.
22. Franco R., Cidlowski J.A. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 2009, 16:1303-1314.
23. Gavin I.M., Gillis B., Arbieva Z., Prabhakar B.S. Identification of human cell responses to hexavalent chromium. Environ. Mol. Mutagen. 2007, 48:650-657.
24. Gelin A., Redrejo-Rodriguez M., Laval J., Fedorova O.S., Saparbaev M., Ishchenko A.A. Genetic and biochemical characterization of human AP endonuclease 1 mutants deficient in nucleotide incision repair activity. PLoS One 2010, 5:e12241.
25. Go Y.M., Craige S.E., Orr M., Gernert K.M., Jones D.P. Gene and protein responses of human monocytes to extracellular cysteine redox potential. Toxicol. Sci. 2009, 112:354-362.
26. Han D., Hanawa N., Saberi B., Kaplowitz N. Mechanisms of liver injury. III. Role of glutathione redox status in liver injury. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291:G1-G7.
27. Henics T., Wheatley D.N. Cytoplasmic vacuolation, adaptation and cell death: a view on new perspectives and features. Biology of the cell/under the auspices of the European Cell Biology Organization 1999, 91:485-498.
28. Hook S.E., Skillman A.D., Gopalan B., Small J.A., Schultz I.R. Gene expression profiles in rainbow trout, Onchorynchus mykiss, exposed to a simple chemical mixture. Toxicol. Sci. 2008, 102:42-60.
29. IARC Chromium, nickel and welding. IARC Monogr Eval Carcinog Risks Hum. 1990, 49-256. Lyon.
30. Izzotti A., Cartiglia C., Balansky R., D'Agostini F., Longobardi M., De Flora S. Selective induction of gene expression in rat lung by hexavalent chromium. Mol. Carcinog. 2002, 35:75-84.
31. Joseph P., He Q., Umbright C. Heme-oxygenase 1 gene expression is a marker for hexavalent chromium-induced stress and toxicity in human dermal fibroblasts. Toxicol. Sci. 2008, 103:325-334.
32. Kass E.M., Jasin M. Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett. 2010, 584:3703-3708.
33. Katz S.A., Salem H. The toxicology of chromium with respect to its chemical speciation: a review. J. Appl. Toxicol. 1993, 13:217-224.
34. Mannery Y.O., Ziegler T.R., Hao L., Shyntum Y., Jones D.P. Characterization of apical and basal thiol-disulfide redox regulation in human colonic epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G523-G530.
35. Mayrhofer G. Absorption and presentation of antigens by epithelial cells of the small intestine: hypotheses and predictions relating to the pathogenesis of coeliac disease. Immunol. Cell Biol. 1995, 73:433-439.
36. McCarroll N., Keshava N., Chen J., Akerman G., Kligerman A., Rinde E. An evaluation of the mode of action framework for mutagenic carcinogens case study II: chromium (VI). Environ. Mol. Mutagen. 2010, 51:89-111.
37. Mimnaugh E.G., Xu W., Vos M., Yuan X., Neckers L. Endoplasmic reticulum vacuolization and valosin-containing protein relocalization result from simultaneous hsp90 inhibition by geldanamycin and proteasome inhibition by velcade. Mol. Cancer Res. 2006, 4:667-681.
38. Moriarty-Craige S.E., Jones D.P. Extracellular thiols and thiol/disulfide redox in metabolism. Annu. Rev. Nutr. 2004, 24:481-509.
39. Myers J.M., Antholine W.E., Myers C.R. The intracellular redox stress caused by hexavalent chromium is selective for proteins that have key roles in cell survival and thiol redox control. Toxicology 2011, 281:37-47.
40. Nemec A.A., Zubritsky L.M., Barchowsky A. Chromium(VI) stimulates Fyn to initiate innate immune gene induction in human airway epithelial cells. Chem. Res. Toxicol. 2010, 23:396-404.
41. Neurath M.F., Becker C., Barbulescu K. Role of NF-kappaB in immune and inflammatory responses in the gut. Gut 1998, 43:856-860.
42. NTP NTP 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. Natl Toxicol Program Tech Rep Ser 2007, 1-144.
43. NTP NTP 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). Natl Toxicol Program Tech Rep Ser 2008, 1-192.
44. O'Brien T.J., Ceryak S., Patierno S.R. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res. 2003, 533:3-36.
45. Oze C., Bird D.K., Fendorf S. Genesis of hexavalent chromium from natural sources in soil and groundwater. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6544-6549.
46. Powell C.L., Kosyk O., Ross P.K., Schoonhoven R., Boysen G., Swenberg J.A., Heinloth A.N., Boorman G.A., Cunningham M.L., Paules R.S., Rusyn I. Phenotypic anchoring of acetaminophen-induced oxidative stress with gene expression profiles in rat liver. Toxicol. Sci. 2006, 93:213-222.
47. Pritchard D.E., Ceryak S., Ramsey K.E., O'Brien T.J., Ha L., Fornsaglio J.L., Stephan D.A., Patierno S.R. Resistance to apoptosis, increased growth potential, and altered gene expression in cells that survived genotoxic hexavalent chromium [Cr(VI)] exposure. Mol. Cell. Biochem. 2005, 279:169-181.
48. Proctor D.M., Otani J.M., Finley B.L., Paustenbach D.J., Bland J.A., Speizer N., Sargent E.V. Is hexavalent chromium carcinogenic via ingestion? A weight-of-evidence review. J. Toxicol. Environ. Health A 2002, 65:701-746.
49. Reinstein E. Immunologic aspects of protein degradation by the ubiquitin-proteasome system. Isr. Med. Assoc. J. 2004, 6:420-424.
50. Rusyn I., Asakura S., Pachkowski B., Bradford B.U., Denissenko M.F., Peters J.M., Holland S.M., Reddy J.K., Cunningham M.L., Swenberg J.A. Expression of base excision DNA repair genes is a sensitive biomarker for in vivo detection of chemical-induced chronic oxidative stress: identification of the molecular source of radicals responsible for DNA damage by peroxisome proliferators. Cancer Res. 2004, 64:1050-1057.
51. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
52. Shi X., Chiu A., Chen C.T., Halliwell B., Castranova V., Vallyathan V. Reduction of chromium(VI) and its relationship to carcinogenesis. J. Toxicol. Environ. Health B Crit. Rev. 1999, 2:87-104.
53. Shrivastava R., Kannan A., Upreti R.K., Chaturvedi U.C. Effects of chromium on the resident gut bacteria of rat. Toxicol. Mech. Methods 2005, 15:211-218.
54. Sun H., Clancy H.A., Kluz T., Zavadil J., Costa M. Comparison of gene expression profiles in chromate transformed BEAS-2B cells. PLoS One 2011, 6:e17982.
55. Thomas R.S., Allen B.C., Nong A., Yang L., Bermudez E., Clewell H.J., Andersen M.E. A method to integrate benchmark dose estimates with genomic data to assess the functional effects of chemical exposure. Toxicol. Sci. 2007, 98:240-248.
56. Thompson C.M., Haws L.C., Harris M.A., Gatto N.M., Proctor D.M. Application of the U.S. EPA mode of action. Framework for purposes of guiding future research: a case study involving the oral carcinogenicity of hexavalent chromium. Toxicol. Sci. 2011, 119:20-40.
57. Thompson C.M., Proctor D.M., Haws L.C., Hébert C.D., Grimer S.D., Shertzer H.G., Kopec A.K., Hixon G., Zacharewski T.R., Harris M.A. Investigation of the mode of action underlying the tumorigenic response induced in B6C3F1 mice exposed orally to hexavalent chromium. Toxicol. Sci. 2011, 123:58-70.
58. Townsend D.M. S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol. Interv. 2007, 7:313-324.
59. Upreti R.K., Shrivastava R., Kannan A., Chaturvedi U.C. A comparative study on rat intestinal epithelial cells and resident gut bacteria: (I) effect of hexavalent chromium. Toxicol. Mech. Methods 2005, 15:331-338.
60. U.S.EPA IRIS Toxicological Review of Hexavalent Chromium (External Review Draft), EPA/635/R-10/004A 2010, U.S. Environmental Protection Agency, Washinton, D.C.
61. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. RESEARCH0034.
62. Vincent J.B. Recent advances in the nutritional biochemistry of trivalent chromium. Proc. Nutr. Soc. 2004, 63:41-47.
63. Watson J.D., Oster S.K., Shago M., Khosravi F., Penn L.Z. Identifying genes regulated in a Myc-dependent manner. J. Biol. Chem. 2002, 277:36921-36930.
64. Yamada K., Sato K., Morishita S., Kaminogawa S., Totsuka M. Establishment of a primary culture method for mouse intestinal epithelial cells by organ culture of fetal small intestine. Biosci. Biotechnol. Biochem. 2009, 73:1849-1855.
65. Yang L., Allen B.C., Thomas R.S. BMDExpress: a software tool for the benchmark dose analyses of genomic data. BMC Genomics 2007, 8:387.
66. Ye J., Shi X. Gene expression profile in response to chromium-induced cell stress in A549 cells. Mol. Cell. Biochem. 2001, 222:189-197.
67. Yusof A.M., Malek N.A. Removal of Cr(VI) and As(V) from aqueous solutions by HDTMA-modified zeolite Y. J. Hazard. Mater. 2009, 162:1019-1024.
68. Zhitkovich A. Chromium in drinking water: sources, metabolism and cancer risks. Chem. Res. Toxicol. 2011, 24:1617-1629.