Transcriptomic analysis reveals early signs of liver toxicity in female MRL +/+ mice exposed to the acylating chemicals dichloroacetyl chloride and dichloroacetic anhydride

Chemical Research in Toxicology

Volumn 21, Issue 3, 2008, Pages 572-582

  König, Rolf ^a   Cai, Ping ^a   Guo, Xin ^a   Ansari, G A S ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICHLOROACETIC ACID; DICHLOROACETIC ANHYDRIDE; DICHLOROACETYL CHLORIDE; TRICHLOROETHYLENE; UNCLASSIFIED DRUG; ZINC ION;

ACUTE PHASE RESPONSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HOMEOSTASIS; INFLAMMATION; LIVER CELL CARCINOMA; LIVER TOXICITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; STRESS; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; UPREGULATION;

ACETIC ACIDS; ACETIC ANHYDRIDES; ACYLATION; ANIMALS; BIOTIN; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEPATITIS, TOXIC; IN SITU HYBRIDIZATION; INFLAMMATION; LIVER FUNCTION TESTS; METALLOTHIONEIN; MICE; MICE, INBRED MRL LPR; MULTIGENE FAMILY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; RNA, COMPLEMENTARY;

MUS; ZEA MAYS;

EID: 41849103807     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx7002728     Document Type: Article

References (82)

1. Forkert, P., Lash, L., Tardif, R., Tanphaichitr, N., Vandevoort, C., and Moussa, M. (2003) Identification of trichloroethylene and its metabolites in human seminal fluid of workers exposed to trichloroethylene. Drug Metab. Dispos. 31, 306-311.
2. Byers, V., Levin, A., Ozonoff, D., and Baldwin, R. (1988) Association between clinical symptoms and lymphocyte abnormalities in a population with chronic domestic exposure to industrial solvent-contaminated domestic water supply and a high incidence of leukaemia. Cancer Immunol. Immunother. 27, 77-81.
3. Kilburn, K., and Warshaw, R. (1992) Prevalence of symptoms of systemic lupus erythematosus (SLE) and of fluorescent antinuclear antibodies associated with chronic exposure to trichloroethylene and other chemicals in well water. Environ. Res. 57, 1-9.
4. Brautbar, N., and Williams, J., II. (2002) Industrial solvents and liver toxicity: risk assessment, risk factors and mechanisms. Int. J. Hyg. Environ. Health 205, 479-491.
5. Wong, O. (2004) Carcinogenicity of trichloroethylene: an epidemiologic assessment. Clin. Occup. Environ. Med. 4, 557-589.
6. Thiele, D., Eigenbrodt, E., and Ware, A. (1982) Cirrhosis after repeated trichloroethylene and 1,1,1-trichloroethane exposure. Gastroenterology 83, 926-929.
7. Pantucharoensri, S., Boontee, P., Likhitsan, P., Padungtod, C., and Prasartsansoui, S. (2004) Generalized eruption accompanied by hepatitis in two Thai metal cleaners exposed to trichloroethylene. Ind. Health 42, 385-388.
8. Raaschou-Nielsen, O., Hansen, J., McLaughlin, J., Kolstad, H., Christensen, J., Tarone, R., and Olsen, J. (2003) Cancer risk among workers at Danish companies using trichloroethylene: a cohort study. Am. J. Epidemiol. 158, 1182-1192.
9. Lee, L., Chung, C., Ma, Y., Wang, G., Chen, P., Hwang, Y., and Wang, J. (2003) Increased mortality odds ratio of male liver cancer in a community contaminated by chlorinated hydrocarbons in groundwater. Occup. Environ. Med. 60, 364-369.
10. Bull, R., Sanchez, I., Nelson, M., Larson, J., and Lansing, A. (1990) Liver tumor induction in B6C3F1 mice by dichloroacetate and trichloroacetate. Toxicology 63, 341-359.
11. Daniel, F., DeAngelo, A., Stober, J., Olson, G., and Page, N. (1992) Hepatocarcinogenicity of chloral hydrate, 2-chloroacetaldehyde, and dichloroacetic acid in the male B6C3F1 mouse. Fundam. Appl. Toxicol. 19, 159-168.
12. Carter, J., Carter, H., and DeAngelo, A. (1995) Biochemical, pathologic and morphometric alterations induced in male B6C3F1 mouse liver by short-term exposure to dichloroacetic acid. Toxicol. Lett. 81, 55-71.
13. Miller, R., and Guengerich, F. (1982) Oxidation of trichloroethylene by liver microsomal cytochrome P-450: evidence for chlorine migration in a transition state not involving trichloroethylene oxide. Biochemistry 21, 1090-1097.
14. Lipscomb, J., Garrett, C., and Snawder, J. (1997) Cytochrome P450-dependent metabolism of trichloroethylene: interindividual differences in humans. Toxicol. Appl. Pharmacol. 142, 311-318.
15. Clewell, H. J., Gentry, P., Covington, T. R., and Gearhart, J. (2000) Development of a physiologically based pharmacokinetic model of trichloroethylene and its metabolites for use in risk assessment. Environ. Health Perspect. 108 (Suppl 2), 283-305.
16. Lash, L., Fisher, J., Lipscomb, J., and Parker, J. (2000) Metabolism of trichloroethylene. Environ. Health Perspect. 108 (Suppl 2), 177-200.
17. Cole, W., Mitchell, R., and Salamonsen, R. (1975) Isolation, characterization and quantitation of chloral hydrate as a transient metabolite of trichloroethylene in man using electron capture gas chromatography and mass fragmentography. J. Pharm. Pharmacol. 27, 167-171.
18. Butler, T. (1949) Metabolic transformation of trichloroethylene. J. Pharmacol. Exp. Ther. 97, 84-92.
19. Miller, R., and Guengerich, F. (1983) Metabolism of trichloroethylene in isolated hepatocytes, microsomes, and reconstituted enzyme systems containing cytochrome P-450. Cancer Res. 43, 1145-1152.
20. Dekant, W., Metzler, M., and Henschler, D. (1984) Novel metabolites of trichloroethylene through dechlorination reactions in rats, mice and humans. Biochem. Pharmacol. 33, 2021-2027.
21. Green, T., and Prout, M. (1985) Species differences in response to trichloroethylene. II. Biotransformation in rats and mice. Toxicol. Appl. Pharmacol. 79, 401-411.
22. Khan, M., Kaphalia, B., and Ansari, G. (1997) Time-dependent autoimmune response of dichloroacetyl chloride in female MRL +/+ mice. Immunopharmacol. Immunotoxicol. 19, 265-277.
23. Khan, M., Kaphalia, B., Prabhakar, B., Kanz, M., and Ansari, G. (1995) Trichloroethene-induced autoimmune response in female MRL +/+ mice. Toxicol. Appl. Pharmacol. 134, 155-160.
24. Griffin, J., Blossom, S., Jackson, S., Gilbert, K., and Pumford, N. (2000) Trichloroethylene accelerates an autoimmune response by Th1 T cell activation in MRL +/+ mice. Immunopharmacology 46, 123-137.
25. Gilbert, K., Griffin, J., and Pumford, N. (1999) Trichloroethylene activates CD4+ T cells: potential role in an autoimmune response. Drug Metab. Rev. 31, 901-916.
26. Gilbert, K., Whitlow, A., and Pumford, N. (2004) Environmental contaminant and disinfection by-product trichloroacetaldehyde stimulates T cells in vitro. Int. Immunopharmacol. 4, 25-36.
27. Cai, P., König, R., Khan, M., Qiu, S., Kaphalia, B., and Ansari, G. (2006) Autoimmune response in MRL+/+ mice following treatment with dichloroacetyl chloride or dichloroacetic anhydride. Toxicol. Appl. Pharmacol. 216, 248-255.
28. Griffin, J., Gilbert, K., Lamps, L., and Pumford, N. (2000) CD4(+) T-cell activation and induction of autoimmune hepatitis following trichloroethylene treatment in MRL+/+ mice. Toxicol. Sci. 57, 345-352.
29. Cai, P., König, R., Boor, P., Khan, M., Kaphalia, B., and Ansari, G. (2007) Immuno- and hepato-toxicity of dichloroacetic acid in MRL +/+ and B6C3F1 mice. J. Immunotoxicol. 4, 107-115.
30. Stierum, R., Heijne, W., Kienhuis, A., van Ommen, B., and Groten, J. (2005) Toxicogenomics concepts and applications to study hepatic effects of food additives and chemicals. Toxicol. Appl. Pharmacol. 207, 179-188.
31. Olden, K. (2006) Toxicogenomics - a new systems toxicology approach to understanding of gene-environment interactions. Ann. N.Y. Acad. Sci. 1076, 703-706.
32. Brazma, A., Hingamp, P., Quackenbush, J., Sherlock, G., Spellman, P., Stoeckert, C., Aach, J., Ansorge, W., Ball, C., Causton, H., Gaasterland, T., Glenisson, P., Holstege, F., Kim, I., Markowitz, V., Matese, J., Parkinson, H., Robinson, A., Sarkans, U., Schulze-Kremer, S., Stewart, J., Taylor, R., Vilo, J., and Vingron, M. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 29, 365-371.
33. Livak, K., and Schmittgen, T. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
34. Cardozo, A., Heimberg, H., Heremans, Y., Leeman, R., Kutlu, B., Kruhøffer, M., Ørntoft, T., and Eizirik, D. (2001) A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta-cells. J. Biol. Chem. 276, 48879-48886.
35. Matin, S., Rackley, R., Sadhukhan, P., Kim, M., Novick, A., and Bandyopadhyay, S. (2001) Impaired alpha-interferon signaling in transitional cell carcinoma: lack of p48 expression in 5637 cells. Cancer Res. 61, 2261-2266.
36. Dobrovolsky, V., Bowyer, J., Pabarcus, M., Heflich, R., Williams, L., Doerge, D., Arvidsson, B., Bergquist, J., and Casida, J. (2005) Effect of arylformamidase (kynurenine formamidase) gene inactivation in mice on enzymatic activity, kynurenine pathway metabolites and phenotype. Biochim. Biophys. Acta 1724, 163-172.
37. Aksoy, S., Szumlanski, C., and Weinshilboum, R. (1994) Human liver nicotinamide N-methyltransferase. cDNA cloning, expression, and biochemical characterization. J. Biol. Chem. 269, 14835-14840.
38. Shen, X., Hong, F., Nguyen, V., and Gao, B. (2000) IL-10 attenuates IFN-alpha-activated STAT1 in the liver: involvement of SOCS2 and SOCS3. FEBS Lett. 480, 132-136.
39. Faderl, S., Harris, D., Van, Q., Kantarjian, H., Talpaz, M., and Estrov, Z. (2003) Granulocyte-macrophage colony-stimulating factor (GM-CSF) induces antiapoptotic and proapoptotic signals in acute myeloid leukemia. Blood 102, 630-637.
40. Yu, C., Mahdi, R., Ebong, S., Vistica, B., Chen, J., Guo, Y., Gery, I., and Egwuagu, C. (2004) Cell proliferation and STAT6 pathways are negatively regulated in T cells by STAT1 and suppressors of cytokine signaling. J. Immunol. 173, 737-746.
41. Greenhalgh, C., Rico-Bautista, E., Lorentzon, M., Thaus, A., Morgan, P., Willson, T., Zervoudakis, P., Metcalf, D., Street, I., Nicola, N., Nash, A., Fabri, L., Norstedt, G., Ohlsson, C., Flores-Morales, A., Alexander, W., and Hilton, D. (2005) SOCS2 negatively regulates growth hormone action in vitro and in vivo. J. Clin. Invest. 115, 397-406.
42. Miyakawa, Y., Rojnuckarin, P., Habib, T., and Kaushansky, K. (2001) Thrombopoietin induces phosphoinositol 3-kinase activation through SHP2, Gab, and insulin receptor substrate proteins in BAF3 cells and primary murine megakaryocytes. J. Biol. Chem. 276, 2494-2502.
43. Fruman, D., and Cantley, L. (2002) Phosphoinositide 3-kinase in immunological systems. Semin. Immunol. 14, 7-18.
44. Cho, Y., Park, Y., Lee, Y., Kim, M., Bates, S., Tan, L., and Cho-Chung, Y. (2000) Extracellular protein kinase A as a cancer biomarker: its expression by tumor cells and reversal by a myristate-lacking Calpha and RIIbeta subunit overexpression. Proc. Natl. Acad. Sci. U.S.A. 97, 835-840.
45. De, A., Kodys, K., Yeh, B., and Miller-Graziano, C. (2000) Exaggerated human monocyte IL-10 concomitant to minimal TNF-alpha induction by heat-shock protein 27 (Hsp27) suggests Hsp27 is primarily an antiinflammatory stimulus. J. Immunol. 165, 3951-3958.
46. Rajeevan, M., Vernon, S., Taysavang, N., and Unger, E. (2001) Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR. J. Mol. Diagn. 3, 26-31.
47. Laé, M., Ahn, E., Mercado, G., Chuai, S., Edgar, M., Pawel, B., Olshen, A., Barr, F., and Ladanyi, M. (2007) Global gene expression profiling of PAX-FKHR fusion-positive alveolar and PAX-FKHR fusion-negative embryonal rhabdomyosarcomas. J. Pathol. 212, 143-151.
48. Myant, N., and Mitropoulos, K. (1977) Cholesterol 7 alpha-hydroxylase. J. Lipid Res. 18, 135-153.
49. Kawanishi, S., Hiraku, Y., and Oikawa, S. (2001) Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mutat. Res. 488, 65-76.
50. Lee, H., Yin, P., Lu, C., Chi, C., and Wei, Y. (2000) Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem. J. 348 (Pt 2), 425-432.
51. Ye, B., Maret, W., and Vallee, B. (2001) Zinc metallothionein imported into liver mitochondria modulates respiration. Proc. Natl. Acad. Sci. U.S.A. 98, 2317-2322.
52. Bruey, J., Ducasse, C., Bonniaud, P., Ravagnan, L., Susin, S., Diaz-Latoud, C., Gurbuxani, S., Arrigo, A., Kroemer, G., Solary, E., and Garrido, C. (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat. Cell Biol. 2, 645-652.
53. Kumar, S., McDonnell, P., Lehr, R., Tierney, L., Tzimas, M., Griswold, D., Capper, E., Tal-Singer, R., Wells, G., Doyle, M., and Young, P. (2000) Identification and initial characterization of four novel members of the interleukin-1 family. J. Biol. Chem. 275, 10308-10314.
54. Honda, K., Mizutani, T., and Taniguchi, T. (2004) Negative regulation of IFN-alpha/beta signaling by IFN regulatory factor 2 for homeostatic development of dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 101, 2416-2421.
55. Cuesta, N., Salkowski, C., Thomas, K., and Vogel, S. (2003) Regulation of lipopolysaccharide sensitivity by IFN regulatory factor-2. J. Immunol. 170, 5739-5747.
56. Kim, I., Kim, H., Kim, H., Kim, H., Park, S., Uhm, C., Lee, Z., and Koh, G. (2000) Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem. J. 346 (Pt 3), 603-610.
57. Chami, M., Gozuacik, D., Lagorce, D., Brini, M., Falson, P., Peaucellier, G., Pinton, P., Lecoeur, H., Gougeon, M., le Maire, M., Rizzuto, R., Bréchot, C., and Paterlini-Bréchot, P. (2001) SERCA1 truncated proteins unable to pump calcium reduce the endoplasmic reticulum calcium concentration and induce apoptosis. J. Cell Biol. 153, 1301-1314.
58. Leclercq, I., Farrell, G., Field, J., Bell, D., Gonzalez, F., and Robertson, G. (2000) CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J. Clin. Invest. 105, 1067-1075.
59. Barclay, T., Peters, J., Sewer, M., Ferrari, L., Gonzalez, F., and Morgan, E. (1999) Modulation of cytochrome P-450 gene expression in endotoxemic mice is tissue specific and peroxisome proliferator-activated receptor-alpha dependent. J. Pharmacol. Exp. Ther. 290, 1250-1257.
60. Bauman, J., Madhu, C., McKim, J. J., Liu, Y., and Klaassen, C. (1992) Induction of hepatic metallothionein by paraquat. Toxicol. Appl. Pharmacol. 117, 233-241.
61. Bauman, J., McKim, J. J., Liu, J., and Klaassen, C. (1992) Induction of metallothionein by diethyl maleate. Toxicol. Appl. Pharmacol. 114, 188-196.
62. Kim, J., Lee, K., Kim, D., Jeong, T., Lee, E., Choi, Y., and Jeong, H. (2004) Cytokine-mediated induction of metallothionein in Hepa-1c1c7 cells by oleanolic acid. Biochem. Biophys. Res. Commun. 325, 792-797.
63. Sato, M., Sasaki, M., and Hojo, H. (1995) Antioxidative roles of metallothionein and manganese superoxide dismutase induced by tumor necrosis factor-alpha and interleukin-6. Arch. Biochem. Biophys. 316, 738-744.
64. Srivastava, R., Hasan, S., Gupta, J., and Gupta, S. (1993) Protective role of metallothionein in nickel induced oxidative damage. Biochem. Mol. Biol. Int. 30, 261-270.
65. Miesel, R., and Zuber, M. (1993) Copper-dependent antioxidase defenses in inflammatory and autoimmune rheumatic diseases. Inflammation 17, 283-294.
66. Sasagawa, S., Matsubara, J., and Satow, Y. (1993) Stress-related induction of hepatic metallothionein synthesis and increase in peripheral polymorphonuclear leukocytes in mice. Immunopharmacol. Immunotoxicol. 15, 217-226.
67. Chubatsu, L., and Meneghini, R. (1993) Metallothionein protects DNA from oxidative damage. Biochem. J. 291 (Pt 1), 193-198.
68. Li, K., Prow, T., Lemon, S., and Beard, M. (2002) Cellular response to conditional expression of hepatitis C virus core protein in Huh7 cultured human hepatoma cells. Hepatology 35, 1237-1246.
69. Okuda, M., Li, K., Beard, M., Showalter, L., Scholle, F., Lemon, S., and Weinman, S. (2002) Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 122, 366-375.
70. Heineke, J., Ruetten, H., Willenbockel, C., Gross, S., Naguib, M., Schaefer, A., Kempf, T., Hilfiker-Kleiner, D., Caroni, P., Kraft, T., Kaiser, R., Molkentin, J., Drexler, H., and Wollert, K. (2005) Attenuation of cardiac remodeling after myocardial infarction by muscle LIM protein-calcineurin signaling at the sarcomeric Z-disc. Proc. Natl. Acad. Sci. U.S.A: 102, 1655-1660.
71. Haguenauer, A., Raimbault, S., Masscheleyn, S., Gonzalez-Barroso, M. M., Criscuolo, F., Plamondon, J., Miroux, B., Ricquier, D., Richard, D., Bouillaud, F., and Pecqueur, C. (2005) A new renal mitochondrial carrier, KMCP1, is up-regulated during tubular cell regeneration and induction of antioxidant enzymes. J. Biol. Chem. 280, 22036-22043.
72. Sunada, F., Itabashi, M., Ohkura, H., and Okumura, T. (2005) p53 negativity, CDC25B positivity, and metallothionein negativity are predictors of a response of esophageal squamous cell carcinoma to chemoradiotherapy. World J. Gastroenterol. 11, 5696-5700.
73. Surowiak, P., Matkowski, R., Materna, V., Györffy, B., Wojnar, A., Pudelko, M., Dziegiel, P., Kornafel, J., and Zabel, M. (2005) Elevated metallothionein (MT) expression in invasive ductal breast cancers predicts tamoxifen resistance. Histol. Histopathol. 20, 1037-1044.
74. Galizia, G., Ferraraccio, F., Lieto, E., Orditura, M., Castellano, P., Imperatore, V., La Manna, G., Pinto, M., Ciardiello, F., La Mura, A., and De Vita, F. (2006) p27 downregulation and metallothionein overexpression in gastric cancer patients are associated with a poor survival rate. J. Surg. Oncol. 93, 241-252.
75. Weinlich, G., Eisendle, K., Hassler, E., Baltaci, M., Fritsch, P., and Zeiger, B. (2006) Metallothionein - overexpression as a highly significant prognostic factor in melanoma: a prospective study on 1270 patients. Br. J. Cancer 94, 835-841.
76. Zagorianakou, N., Stefanou, D., Makrydimas, G., Zagorianakou, P., Briasoulis, E., Karavasilis, V., Pavlidis, N., and Agnantis, N. (2006) Clinicopathological study of metallothionein immunohistochemical expression, in benign, borderline and malignant ovarian epithelial tumors. Histol. Histopathol. 21, 341-347.
77. Zhou, X., Sens, D., Sens, M., Namburi, V., Singh, R., Garrett, S., and Somji, S. (2006) Metallothionein-1 and -2 expression in cadmium-or arsenic-derived human malignant urothelial cells and tumor heterotransplants and as a prognostic indicator in human bladder cancer. Toxicol. Sci. 91, 467-475.
78. Maeda, S., Kamata, H., Luo, J., Leffert, H., and Karin, M. (2005) IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121, 977-990.
79. Bartosiewicz, M., Jenkins, D., Penn, S., Emery, J., and Buckpitt, A. (2001) Unique gene expression patterns in liver and kidney associated with exposure to chemical toxicants. J. Pharmacol. Exp. Ther. 297, 895-905.
80. Thai, S., Allen, J., DeAngelo, A., George, M., and Fuscoe, J. (2003) Altered gene expression in mouse livers after dichloroacetic acid exposure. Mutat. Res. 543, 167-180.
81. Laughter, A., Dunn, C., Swanson, C., Howroyd, P., Cattley, R., and Cotton, J. (2004) Role of the peroxisome proliferator-activated receptor alpha (PPARalpha) in responses to trichloroethylene and metabolites, trichloroacetate and dichloroacetate in mouse liver. Toxicology 203, 83-98.
82. Bartosiewicz, M., Penn, S., and Buckpitt, A. (2001) Applications of gene arrays in environmental toxicology: fingerprints of gene regulation associated with cadmium chloride, benzo(a)pyrene, and trichloroethylene. Environ. Health Perspect. 109, 71-74.