Use of a low-density microarray for studying gene expression patterns induced by hepatotoxicants on primary cultures of rat hepatocytes

Toxicological Sciences

Volumn 75, Issue 2, 2003, Pages 378-392

  de Longueville, Francoise ^a   Atienzar, Franck A ^b   Marcq, Laurence ^a   Dufrane, Simon ^b   Evrard, Stéphanie ^a   Wouters, Lydia ^b   Leroux, Florence ^b   Bertholet, Vincent ^a   Gerin, Brigitte ^b   Whomsley, Rhys ^b   Arnould, Thierry ^c   Remacle, José ^a   Canning, Mickael ^b  

^a Eppendorf Array Technologies   (Belgium)

^b UCB PHARMA   (Belgium)

^c UNIVERSITY OF NAMUR   (Belgium)

Author keywords

Drug metabolism; Gene expression pattern; Hepatotoxicants; Low density microarray; Toxicogenomics

Indexed keywords

1 NAPHTHYL ISOTHIOCYANATE; 4 PENTENOIC ACID; AMIODARONE; BETA NAPHTHOFLAVONE; BIOLOGICAL MARKER; CLOFIBRATE; CYTOCHROME P450; ERYTHROMYCIN ESTOLATE; ISONIAZID; PARACETAMOL; PHENOBARBITAL; TETRACYCLINE; ZILEUTON;

ANIMAL CELL; ANIMAL EXPERIMENT; CHOLESTASIS; CLUSTER ANALYSIS; CONTROLLED STUDY; CYTOTOXICITY; DNA MICROARRAY; ENZYME ACTIVATION; EXPOSURE; GENE EXPRESSION PROFILING; IN VITRO STUDY; LIVER CELL CULTURE; LIVER NECROSIS; LIVER TOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RAT; REVIEW; STEATOSIS; UNINDEXED SEQUENCE;

ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INDUCTION; FORMAZANS; GENE EXPRESSION PROFILING; HEPATOCYTES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TETRAZOLIUM SALTS; XENOBIOTICS;

ANIMALIA;

EID: 10744233751     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/kfg196     Document Type: Review

References (65)

1. Amacher, D. E., and Martin, B. A. (1997). Tetracycline-induced steatosis in primary canine hepatocyte cultures. Fundam. Appl. Toxicol. 40, 256-263.
2. Aoshiba, K., Nagai, A., and Konno, K. (1995). Erythromycin shortens neutrophil survival by accelerating apoptosis. Antimicrob. Agents Chemother. 39, 872-877.
3. Baker, T. K., Carfagna, M. A., Gao, H., Dow, E. R., Li, Q., Searfoss, G. H., and Ryan, T. P. (2001). Temporal gene expression analysis of monolayer cultured rat hepatocytes. Chem. Res. Toxicol. 14, 1218-1231.
4. Baker, T. K., Higgins, M. A., Carfagna, M. A., and Ryan, T. P. (2003). Characterization of hepatocytes and their use as a model system in toxicogenomics. In An Introduction to Toxicogenomics (M. E. Burczynski, Ed.), pp. 117-143. CRC Press, Boca Raton, FL.
5. Bartosiewicz, M. J., 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.
6. Bulera, S. J., Eddy S. M., Ferguson, E., Jatkoe, T. A., Reindel, J. F., Bleavins, M. R., and De La Iglesia, F. A. (2001). RNA expression in the early characterization of hepatotoxicants in Wistar rats by high-density DNA microarrays. Hepatology 33, 1239-1258.
7. Burcham, P. C., and Harman, A. W. (1991). Acetaminophen toxicity results in site-specific mitochondrial damage in isolated mouse hepatocytes. J. Biol. Chem. 266, 5049-5054.
8. Burczynski, M. E., McMillian, M., Ciervo, J., Li, L., Parker, J. B., Dunn, R. T., Hicken, S., Farr, S., and Johnson, M. D. (2000). Toxicogenomics-based discrimination of toxic mechanism in HepG2 human hepatoma cells. Toxicol. Sci. 58, 399-415.
9. Celli, A., Que F. G., Gores, G. J., and LaRusso, N. F. (1998). Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am. J. Physiol. 275, G749-G757.
10. Chen, Y., Dougherty, E. R., and Bitmer, M. L. (1997). Ratio-based decisions and the quantitative analysis of cDNA microarray images. J. Biomed. Optics 2, 364-374.
11. Chung, W. H., Bennett B. M., Racz, W. J., Brien, J. F., and Massey, T. E. (2001). Induction of c-jun and TGF-beta 1 in Fischer 344 rats during amiodarone-induced pulmonary fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 281, L1180-L1188.
12. Corton, J. C., Lapinskas, P. J., and Gonzalez, F. J. (2000). Central role of PPARalpha in the mechanism of action of hepatocarcinogenic peroxisome proliferators. Mutat. Res. 448, 139-151.
13. de Longueville, F., Surry, D., Meneses-Lorente, G., Bertholet, V., Talbot, V., Evrard, S., Chandelier, N., Pike, A., Worboys, P., Rasson, J. P., et al. (2002). Gene expression profiling of drug metabolism and toxicology markers using a low-density DNA microarray. Biochem. Pharmacol. 64, 137-149.
14. Denison, M. S., and Heath-Pagliuso, S. (1998). The Ah receptor: A regulator of the biochemical and toxicological actions of structurally diverse chemicals. Bull. Environ. Contam. Toxicol. 61, 557-568.
15. Fielden, M. R., and Zacharewski, T. R. (2001). Challenges and limitations of gene expression profiling in mechanistic and predictive toxicology. Toxicol. Sci. 60, 6-10.
16. Fontanier-Razzaq, N. C., Hay, S. M., and Rees, W. D. (1999). Upregulation of CHOP-10 (gadd153) expression in the mouse blastocyst as a response to stress. Mol. Reprod. Dev. 54, 326-332.
17. Fromenty, B., and Pessayre, D. (1995). Inhibition of mitochondrial beta-oxidation as a mechanism of hepatotoxicity. Pharmacol. Ther. 67, 101-154.
18. Frueh, F. W., Zanger, U. M., and Meyer, U. A. (1997). Extent and character of phenobarbital-mediated changes in gene expression in the liver. Mol. Pharmacol. 51, 363-369.
19. Fujita, T., Shirasawa, T., and Maruyama, N. (1999). Expression and structure of senescence marker protein-30 (SMP30) and its biological significance. Mech. Ageing Dev. 107, 271-280.
20. Gerhold, D., Lu, M., Xu, J., Austin, C., Caskey, C. T., and Rushmore, T. (2001). Monitoring expression of genes involved in drug metabolism and toxicology using DNA microarrays. Physiol. Genomics 5, 161-170.
21. Gibson, G. G., Orton, T. C., and Tamburini, P. P. (1982). Cytochrome P-450 induction by clofibrate. Purification and properties of a hepatic cytochrome P-450 relatively specific for the 12- and 11-hydroxylation of dodecanoic acid (lauric acid). Biochem. J. 203, 161-168.
22. Gottlieb, E., Vander Heiden, M. G., and Thompson, C. B. (2000). Bcl-x(L) prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol. Cell Biol. 20, 5680-5689.
23. Hamadeh, H. K., Bushel, P. R., Jayadev, S., DiSorbo, O., Bennett, L., Li, L., Tennant, R., Stoll, R., Barrett, J. C., Paules, R. S., et al. (2002a). Prediction of compound signature using high density gene expression profiling. Toxicol. Sci. 67, 232-240.
24. Hamadeh, H. K., Bushel, P. R., Jayadev, S., Martin, K., DiSorbo, O., Sieber, S., Bennett, L., Tennant, R., Stoll, R., Barrett, J. C., et al. (2002b). Gene expression analysis reveals chemical-specific profiles. Toxicol. Sci. 67, 219-231.
25. Honkakoski, P., Zelko, I., Sueyoshi, T., and Negishi, M. (1998). The nuclear orphan receptor CAR-retinoid X receptor heterodimer activates the phenobarbital-responsive enhancer module of the CYP2B gene. Mol. Cell. Biol. 18, 5652-5658.
26. Ishigami, A., Fujita, T., Handa, S., Shirasawa, T., Koseki, H., Kitamura, T., Enomoto, N., Sato, N., Shimosawa, T., and Maruyama, N. (2002). Senescence marker protein-30 knockout mouse liver is highly susceptible to tumor necrosis factor-alpha- and Fas-mediated apoptosis. Am. J. Pathol. 161, 1273-1281.
27. Jemnitz, K., Veres, Z., Monostory, K., and Vereczkey, L. (2000). Glucuronidation of thyroxine in primary monolayer cultures of rat hepatocytes: In vitro induction of UDP-glucuronosyltranferases by methylcholanthrene, clofibrate, and dexamethasone alone and in combination. Drug Metab. Dispos. 28, 34-37.
28. Johnson, D. E., and Wolfgang, G. H. (2000). Predicting human safety: Screening and computational approaches. Drug Discovery Today 5, 445-454.
29. Kovary, K., and Bravo, R. (1991). Expression of different Jun and Fos proteins during the G0-to-G1 transition in mouse fibroblasts: in vitro and in vivo associations. Mol. Cell Biol. 11, 2451-2459.
30. Lesage, G., Glaser, S., Ueno, Y., Alvaro, D., Baiocchi, L., Kanno, N., Phinizy, J. L., Francis, H., and Alpini, G. (2001). Regression of cholangiocyte proliferation after cessation of ANIT feeding is coupled with increased apoptosis. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G182-190.
31. Lindquist, P. J., Svensson, L. T., and Alexson, S. E. (1998). Molecular cloning of the peroxisome proliferator-induced 46-kDa cytosolic acyl-CoA thioesterase from mouse and rat liver-recombinant expression in Escherichia coli, tissue expression, and nutritional regulation. Eur. J. Biochem. 251, 631-640.
32. Loscher, W., Nau, H., Wahnschaffe, U., Honack, D., Rundfeldt, C., Wittfoht, W., and Bojic, U. (1993). Effects of valproate and E-2-en-valproate on functional and morphological parameters of rat liver. II. Influence of phenobarbital comedication. Epilepsy Res. 15, 113-131.
33. Maheo, K., J. Antras-Ferry, J., Morel, F., Langouet, S., and Guillouzo, A. (1997). Modulation of glutathione S-transferase subunits A2, M1, and P1 expression by interleukin-1beta in rat hepatocytes in primary culture. J. Biol. Chem. 272, 16125-16132.
34. Masahiko, N., and Honkakoski, P. (2000). Induction of drug metabolism by nuclear receptor CAR: Molecular mechanisms and implications for drug research. Eur. J. Pharm. Sci. 11, 259-264.
35. Meyer, U. A., and Hoffmann, K. (1999). Phenobarbital-mediated changes in gene expression in the liver. Drug Metab. Rev. 31, 365-373.
36. Morgan, K. T., Ni, H., Brown, H. R., Yoon, L., Qualls, C. W., Crosby, L. M., Reynolds, R., Gaskill, B., Anderson, S. P., Kepler, T. B., et al. (2002). Application of cDNA microarray technology to in vitro toxicology and the selection of genes for a real-time RT-PCR-based screen for oxidative stress in Hep-G2 cells. Toxicol. Pathol. 30, 435-451.
37. Ohta, Y., Kongo, M., and Kishikawa, T. (2001). Effect of melatonin on changes in hepatic antioxidant enzyme activities in rats treated with alpha-naphthylisothiocyanate. J. Pineal. Res. 31, 370-377.
38. Orsler, D. J., Ahmed-Choudhury, J., Chipman, J. K., Hammond, T., and Coleman, R. (1999). ANIT-induced disruption of biliary function in rat hepatocyte couplets. Toxicol. Sci. 47, 203-210.
39. Otoguro, K., Komiyama, K., Omura, S., and Tyson, C. A. (1991). An in vitro cytotoxicity assay using rat hepatocytes and MTT and Coomassie blue dye as indicators. ATLA 19, 352-360.
40. Que, F. G., Gores, G. J., and LaRusso, N. F. (1997). Development and initial application of an in vitro model of apoptosis in rodent cholangiocytes. Am. J. Physiol. 272, G106-G115.
41. Rajeevan, M. S., Vernon, S. D., Taysavang, N., and Unger, E. R. (2001). Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR. J. Mol. Diagnostics 3, 26-31
42. Ranganna, K., Yatsu, F. M., Hayes, B. E., Milton, S. G., and Jayakumar, A. (2000). Butyrate inhibits proliferation-induced proliferating cell nuclear antigen expression (PCNA) in rat vascular smooth muscle cells. Mol. Cell. Biochem. 205, 149-161.
43. Ray, S. D., and Jena, N. (2000). A hepatotoxic dose of acetaminophen modulates expression of BCL-2, BCL-X(L), and BCL-X(S) during apoptotic and necrotic death of mouse liver cells in vivo. Arch. Toxicol. 73, 594-606.
44. Reilly, T., Bourdi, M., Brady, J. N., Pise-Masison, C. A., Radonovich, M. F., George, J. W., and Pohl, L. R. (2001). Expression profiling of acetaminophen liver toxicity in mice using microarray technology. Biochem. Biophys. Res. Commun. 282, 321-328.
45. Ritter, J. K., and Franklin, M. R. (1987). Clotrimazole induction of cytochrome P-450: Dose-differentiated isozyme induction. Mal. Pharmacol. 31, 135-139.
46. Robertson, G., Leclercq, I., and Farrell, G. C. (2001). Nonalcoholic steatosis and steatohepatitis. II. Cytochrome P-450 enzymes and oxidative stress. Am. J. Physiol. Gastrointest. Liver Physiol. 281, G1135-G1139.
47. Rodrigues, A. D., and Machinist, J. M. (1996). Hepatic peroxisomal and drug metabolizing activity in CD-1 mice after oral treatment with a novel 5-lipoxygenase inhibitor. Toxicol. Appl. Pharmacol. 137, 193-201.
48. Ronis, M. J., Ingelman-Sundberg, M., and Badger, T. M. (1994). Induction, suppression and inhibition of multiple hepatic cytochrome P450 isozymes in the male rat and bobwhite quail (Colinus virginianus) by ergosterol biosynthesis inhibiting fungicides (EBIFs). Biochem. Pharmacol. 48, 1953-1965.
49. Saarikoski, S. T., Ikonen, T. S., Oinonen, T., Lindros, K. O., Ulmanen, I., and Husgafvel-Pursiainen, K. (1998). Induction of UDP-glycosyltransferase family 1 genes in rat liver: Different patterns of mRNA expression with two inducers, 3-methylcholanthrene and beta-naphthoflavone. Biochem. Pharmacol. 56, 569-575.
50. Sadaphal, P., Astemborski, J., Graham, N. M., Sheely, L., Bonds, M., Madison, A., Vlahov, D., Thomas, D. L., and Sterling, T. R. (2001). Isoniazid preventive therapy, hepatitis C virus infection, and hepatotoxicity among injection drug users infected with Mycobacterium tuberculosis. Clin. Infect. Dis. 33, 1687-1691.
51. Salas, V. M., and Corcoran, G. B. (1997). Calcium-dependent DNA damage and adenosine 3′,5′-cyclic monophosphate-independent glycogen phosphorylase activation in an in vitro model of acetaminophen-induced liver injury. Hepatology 25(6), 1432-1438.
52. Schuchhardt, J., Beule, D., Malik, A., Wolski, E., Eickhoff, H., Lehrach, H., and Herzel, H. (2000). Normalization strategies for cDNA microarrays. Nucleic Acids Res. 28, E47.
53. Seglen, P. O. (1976). Preparation of isolated rat liver cells. Methods Cell. Biol. 13, 29-83.
54. Simpson, A. E. (1997). The cytochrome P450 4 (CYP4) family. Gen. Pharmacol. 28, 351-359.
55. Storck, T., von Brevern, M. C., Behrens, C. K., Scheel, J., and Bach, A. (2002). Transcriptomics in predictive toxicology. Curr. Opin. Drug Discov. Devel. 5, 90-97.
56. Sundseth, S. S., and Waxman, D. J. (1992). Sex-dependent expression and clofibrate inducibility of cytochrome P450 4A fatty acid omega-hydroxylases. Male specificity of liver and kidney CYP4A2 mRNA and tissue-specific regulation by growth hormone and testosterone. J. Biol. Chem. 267, 3915-3921.
57. Surry, D. D., Meneses-Lorente, G., Heavens, R., Jack, A., and Evans, D. C. (2000). Rapid determination of rat hepatocyte mRNA induction potential using oligonucleotide probes for CYP1A1, 1A2, 3A and 4A1. Xenobiotica 30, 441-456.
58. Tang, W., Borel, A. G., Fujimiya, T., and Abbott, F. S. (1995). Fluorinated analogues as mechanistic probes in valproic acid hepatotoxicity: Hepatic microvesicular steatosis and glutathione status. Chem. Res. Toxicol, 8, 671-82.
59. Tarloff, J. B., Khairallah, E. A., Cohen, S. D., and Goldstein, R. S. (1996). Sex-and age-dependent acetaminophen hepato- and nephrotoxicity in Sprague-Dawley rats: Role of tissue accumulation, nonprotein sulfhydryl depletion, and covalent binding. Fundam. Appl. Toxicol. 30, 13-22.
60. Tygstrup, N., Bangert, K., Ott, P., and Bisgaard, H. C. (2002). Messenger RNA profiles in liver injury and stress: A comparison of lethal and nonlethal rat models. Biochem. Biophys. Res. Commun. 290, 518-525.
61. Van Custem, B. (1994). Classification and dissimilarity analysis. In Lecture Notes in Statistics (P. Bickel, P. Diggle, S. Fienberg, K. Krickeberg, I. Olkin, N. Wermuth, and S. Zeger, Eds.), Vol. 93, pp. 1-238. Springer-Verlag, Heidelberg, Germany.
62. Waring, J. F., Ciurlionis, R., Jolly, R. A., Heindel, M., and Ulrich, R. G. (2001a). Microarray analysis of hepatotoxins in vitro reveals a correlation between gene expression profiles and mechanisms of toxicity. Toxicol. Lett. 120, 359-368.
63. Waring, J. F., Jolly, R. A., Ciurlionis, R., Lum, P. Y., Praestgaard, J. T., Morfitt, D. C., Buratto, B., Roberts, C., Schadt, E., and Ulrich, R. G. (2001b). Clustering of hepatotoxins based on mechanism of toxicity using gene expression profiles. Toxicol. Appl. Pharmacol. 175, 28-42.
64. Yuen, T., Wurmbach, E., Pfeffer, R., Ebersole, B. J., and Sealfon, S. C. (2002). Accurary and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleid Acid Res. 30(10), e48.
65. Zhang, J., W. Huang, W., Chua, S. S., Wei, P., and Moore, D. D. (2002). Modulation of acetaminophen-induced hepatotoxicity by the xenobiotic receptor CAR. Science 298, 422-424.