Cell line-specific oxidative stress in cellular toxicity: A toxicogenomics-based comparison between liver and colon cell models

Toxicology in Vitro

Volumn 29, Issue 5, 2015, Pages 845-855

  Deferme, L ^a   Briede J J ^a   Claessen, S M H ^a   Cavill, R ^a   Kleinjans, J C S ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Colon; Liver; Oxidative stress; Pathway analysis; Toxicity; Transcriptomics

Indexed keywords

HYDROGEN PEROXIDE; MENADIONE;

ARTICLE; CACO 2 CELL LINE; CAT GENE; CELL CYCLE; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIAL MESENCHYMAL TRANSITION; GCLC GENE; GCLM GENE; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GSR GENE; HEPG2 CELL LINE; HMOX1 GENE; INTESTINE CELL; KEAP1 GENE; LIVER CELL; NF KAPPA B GENE; NRF2 GENE; OGG1 GENE; OXIDATIVE STRESS; TOXICOGENETICS; TRANSCRIPTOMICS; COLON; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HUMAN; LIVER;

CACO-2 CELLS; CELL CYCLE; COLON; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEP G2 CELLS; HUMANS; HYDROGEN PEROXIDE; LIVER; OXIDATIVE STRESS; TOXICOGENETICS; VITAMIN K 3;

EID: 84926326704     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.03.007     Document Type: Article

References (66)

1. Aleksunes L.M., Manautou J.E. Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease. Toxicol. Pathol. 2007, 35:459-473.
2. Anwar-Mohamed A., Degenhardt O.S., El Gendy M.A., Seubert J.M., Kleeberger S.R., El-Kadi A.O. The effect of Nrf2 knockout on the constitutive expression of drug metabolizing enzymes and transporters in C57Bl/6 mice livers. Toxicol. In Vitro 2011, 25:785-795.
3. Aravinthan A., Shannon N., Heaney J., Hoare M., Marshall A., Alexander G.J. The senescent hepatocyte gene signature in chronic liver disease. Exp. Gerontol. 2014, 60:37-45.
4. Artursson P., Palm K., Luthman K. Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv. Drug Deliv. Rev. 2001, 46:27-43.
5. Banning A., Brigelius-Flohe R. NF-kappaB, Nrf2, and HO-1 interplay in redox-regulated VCAM-1 expression. Antioxid. Redox Signal. 2005, 7:889-899.
6. Beltran-Ramirez O., Sokol S., Le-Berre V., Francois J.M., Villa-Trevino S. An approach to the study of gene expression in hepatocarcinogenesis initiation. Transl. Oncol. 2010, 3:142-148.
7. Benhar M., Engelberg D., Levitzki A. ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep. 2002, 3:420-425.
8. Braun T., Carvalho G., Fabre C., Grosjean J., Fenaux P., Kroemer G. Targeting NF-kappaB in hematologic malignancies. Cell Death Differ. 2006, 13:748-758.
9. Briede J.J., van Delft J.M., de Kok T.M., van Herwijnen M.H., Maas L.M., Gottschalk R.W., Kleinjans J.C. Global gene expression analysis reveals differences in cellular responses to hydroxyl- and superoxide anion radical-induced oxidative stress in caco-2 cells. Toxicol. Sci. 2010, 114:193-203.
10. Bruix J., Boix L., Sala M., Llovet J.M. Focus on hepatocellular carcinoma. Cancer Cell 2004, 5:215-219.
11. Cavill R., Kleinjans J., Briede J.J. DTW4Omics: comparing patterns in biological time series. PLoS ONE 2013, 8:e71823.
12. Chan K., Han X.D., Kan Y.W. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. USA 2001, 98:4611-4616.
13. D'Autreaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 2007, 8:813-824.
14. Deferme L., Briede J.J., Claessen S.M., Jennen D.G., Cavill R., Kleinjans J.C. Time series analysis of oxidative stress response patterns in HepG2: a toxicogenomics approach. Toxicology 2013, 306:24-34.
15. Duthie S.J., Collins A.R. The influence of cell growth, detoxifying enzymes and DNA repair on hydrogen peroxide-mediated DNA damage (measured using the comet assay) in human cells. Free Radic. Biol. Med. 1997, 22:717-724.
16. Ernst J., Bar-Joseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 2006, 7:191.
17. Forman H.J., Maiorino M., Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010, 49:835-842.
18. Franke T.F., Kaplan D.R., Cantley L.C. PI3K: downstream AKTion blocks apoptosis. Cell 1997, 88:435-437.
19. Fredriksson L., Wink S., Herpers B., Benedetti G., Hadi M., de Bont H., Groothuis G., Luijten M., Danen E., de Graauw M., Meerman J., van de Water B. Drug-induced endoplasmic reticulum and oxidative stress responses independently sensitize toward TNFalpha-mediated hepatotoxicity. Toxicol. Sci. 2014, 140:144-159.
20. Furumatsu K., Nishiumi S., Kawano Y., Ooi M., Yoshie T., Shiomi Y., Kutsumi H., Ashida H., Fujii-Kuriyama Y., Azuma T., Yoshida M. A role of the aryl hydrocarbon receptor in attenuation of colitis. Dig. Dis. Sci. 2011, 56:2532-2544.
21. Ganan-Gomez I., Wei Y., Yang H., Boyano-Adanez M.C., Garcia-Manero G. Oncogenic functions of the transcription factor Nrf2. Free Radic. Biol. Med. 2013.
22. Giannoni E., Parri M., Chiarugi P. EMT and oxidative stress: a bidirectional interplay affecting tumor malignancy. Antioxid. Redox Signal. 2012, 16:1248-1263.
23. Gmeiner W.H., Hellmann G.M., Shen P. Tissue-dependent and -independent gene expression changes in metastatic colon cancer. Oncol. Rep. 2008, 19:245-251.
24. Grivennikov S.I. Inflammation and colorectal cancer: colitis-associated neoplasia. Semin. Immunopathol. 2013, 35:229-244.
25. Hebels D.G., Briede J.J., Khampang R., Kleinjans J.C., de Kok T.M. Radical mechanisms in nitrosamine- and nitrosamide-induced whole-genome gene expression modulations in Caco-2 cells. Toxicol. Sci. 2010, 116:194-205.
26. Hollensworth S.B., Shen C., Sim J.E., Spitz D.R., Wilson G.L., LeDoux S.P. Glial cell type-specific responses to menadione-induced oxidative stress. Free Radic. Biol. Med. 2000, 28:1161-1174.
27. Huo L., Li C.W., Huang T.H., Lam Y.C., Xia W., Tu C., Chang W.C., Hsu J.L., Lee D.F., Nie L., Yamaguchi H., Wang Y., Lang J., Li L.Y., Chen C.H., Mishra L., Hung M.C. Activation of Keap1/Nrf2 signaling pathway by nuclear epidermal growth factor receptor in cancer cells. Am. J. Transl. Res. 2014, 6:649-663.
28. Ijssennagger N., Rijnierse A., de Wit N.J., Boekschoten M.V., Dekker J., Schonewille A., Muller M., van der Meer R. Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis 2013, 34:1628-1635.
29. Itzkowitz S.H., Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G7-G17.
30. Iwanaga K., Yang Y., Raso M.G., Ma L., Hanna A.E., Thilaganathan N., Moghaddam S., Evans C.M., Li H., Cai W.W., Sato M., Minna J.D., Wu H., Creighton C.J., Demayo F.J., Wistuba I.I., Kurie J.M. Pten inactivation accelerates oncogenic K-ras-initiated tumorigenesis in a mouse model of lung cancer. Cancer Res. 2008, 68:1119-1127.
31. Jarrett S.G., Albon J., Boulton M. The contribution of DNA repair and antioxidants in determining cell type-specific resistance to oxidative stress. Free Radic. Res. 2006, 40:1155-1165.
32. Jennen D.G., Magkoufopoulou C., Ketelslegers H.B., van Herwijnen M.H., Kleinjans J.C., van Delft J.H. Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicol. Sci. 2010, 115:66-79.
33. Jin J., Xiong T., Hou X., Sun X., Liao J., Huang Z., Huang M., Zhao Z. Role of Nrf2 activation and NF-kappaB inhibition in valproic acid induced hepatotoxicity and in diammonium glycyrrhizinate induced protection in mice. Food Chem. Toxicol. 2014, 73:95-104.
34. Kay H.Y., Won Yang J., Kim T.H., Lee da Y., Kang B., Ryu J.H., Jeon R., Kim S.G. Ajoene, a stable garlic by-product, has an antioxidant effect through Nrf2-mediated glutamate-cysteine ligase induction in HepG2 cells and primary hepatocytes. J. Nutr. 2010, 140:1211-1219.
35. Kim J., Lee J.H., Iyer V.R. Global identification of Myc target genes reveals its direct role in mitochondrial biogenesis and its E-box usage in vivo. PLoS ONE 2008, 3:e1798.
36. Klaunig J.E., Kamendulis L.M., Hocevar B.A. Oxidative stress and oxidative damage in carcinogenesis. Toxicol. Pathol. 2010, 38:96-109.
37. Kundu J.K., Surh Y.J. Emerging avenues linking inflammation and cancer. Free Radic. Biol. Med. 2012, 52:2013-2037.
38. Lee J.M., Calkins M.J., Chan K., Kan Y.W., Johnson J.A. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J. Biol. Chem. 2003, 278:12029-12038.
39. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., Jakel R.J., Johnson J.A. Nrf2, a multi-organ protector?. FASEB J. 2005, 19:1061-1066.
40. Limonciel A., Monks K., Stanzel S., Truisi G.L., Parmentier C., Aschauer L., Wilmes A., Richert L., Hewitt P., Mueller S.O., Lukas A., Kopp-Schneider A., Leonard M.O., Jennings P. Transcriptomics hit the target: monitoring of ligand-activated and stress response pathways for chemical testing. Toxicol. In Vitro 2015.
41. Liu G.H., Qu J., Shen X. NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim. Biophys. Acta 2008, 1783:713-727.
42. Liu W., Baker S.S., Baker R.D., Nowak N.J., Zhu L. Upregulation of hemoglobin expression by oxidative stress in hepatocytes and its implication in nonalcoholic steatohepatitis. PLoS ONE 2011, 6:e24363.
43. Liu Z., Wu X., Zhang F., Han L., Bao G., He X., Xu Z. AhR expression is increased in hepatocellular carcinoma. J. Mol. Histol. 2013, 44:455-461.
44. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
45. Llovet J.M., Burroughs A., Bruix J. Hepatocellular carcinoma. Lancet 2003, 362:1907-1917.
46. Lu S.C. Glutathione synthesis. Biochim. Biophys. Acta 2013, 1830:3143-3153.
47. Malik N., Efthymiou A.G., Mather K., Chester N., Wang X., Nath A., Rao M.S., Steiner J.P. Compounds with species and cell type specific toxicity identified in a 2000 compound drug screen of neural stem cells and rat mixed cortical neurons. Neurotoxicology 2014, 45:192-200.
48. MAQC_Consortium, Shi L., Reid L.H., Jones W.D., Shippy R., Warrington J.A., Baker S.C., Collins P.J., de Longueville F., Kawasaki E.S., Lee K.Y., Luo Y., Sun Y.A., Willey J.C., Setterquist R.A., Fischer G.M., Tong W., Dragan Y.P., Dix D.J., Frueh F.W., Goodsaid F.M., Herman D., Jensen R.V., Johnson C.D., Lobenhofer E.K., Puri R.K., Schrf U., Thierry-Mieg J., Wang C., Wilson M., Wolber P.K., Zhang L., Amur S., Bao W., Barbacioru C.C., Lucas A.B., Bertholet V., Boysen C., Bromley B., Brown D., Brunner A., Canales R., Cao X.M., Cebula T.A., Chen J.J., Cheng J., Chu T.M., Chudin E., Corson J., Corton J.C., Croner L.J., Davies C., Davison T.S., Delenstarr G., Deng X., Dorris D., Eklund A.C., Fan X.H., Fang H., Fulmer-Smentek S., Fuscoe J.C., Gallagher K., Ge W., Guo L., Guo X., Hager J., Haje P.K., Han J., Han T., Harbottle H.C., Harris S.C., Hatchwell E., Hauser C.A., Hester S., Hong H., Hurban P., Jackson S.A., Ji H., Knight C.R., Kuo W.P., LeClerc J.E., Levy S., Li Q.Z., Liu C., Liu Y., Lombardi M.J., Ma Y., Magnuson S.R., Maqsodi B., McDaniel T., Mei N., Myklebost O., Ning B., Novoradovskaya N., Orr M.S., Osborn T.W., Papallo A., Patterson T.A., Perkins R.G., Peters E.H., Peterson R., Philips K.L., Pine P.S., Pusztai L., Qian F., Ren H., Rosen M., Rosenzweig B.A., Samaha R.R., Schena M., Schroth G.P., Shchegrova S., Smith D.D., Staedtler F., Su Z., Sun H., Szallasi Z., Tezak Z., Thierry-Mieg D., Thompson K.L., Tikhonova I., Turpaz Y., Vallanat B., Van C., Walker S.J., Wang S.J., Wang Y., Wolfinger R., Wong A., Wu J., Xiao C., Xie Q., Xu J., Yang W., Zhang L., Zhong S., Zong Y., Slikker W. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 2006, 24:1151-1161.
49. Nakajima S., Kitamura M. Bidirectional regulation of NF-kappaB by reactive oxygen species: a role of unfolded protein response. Free Radic. Biol. Med. 2013, 65C:162-174.
50. Patterson T.A., Lobenhofer E.K., Fulmer-Smentek S.B., Collins P.J., Chu T.M., Bao W., Fang H., Kawasaki E.S., Hager J., Tikhonova I.R., Walker S.J., Zhang L., Hurban P., de Longueville F., Fuscoe J.C., Tong W., Shi L., Wolfinger R.D. Performance comparison of one-color and two-color platforms within the MicroArray Quality Control (MAQC) project. Nat. Biotechnol. 2006, 24:1140-1150.
51. Pavlick K.P., Laroux F.S., Fuseler J., Wolf R.E., Gray L., Hoffman J., Grisham M.B. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic. Biol. Med. 2002, 33:311-322.
52. Pez F., Lopez A., Kim M., Wands J.R., Fromentel C.C., Merle P. Wnt signaling and hepatocarcinogenesis: molecular targets for the development of innovative anticancer drugs. J. Hepatol. 2013.
53. Quan X., Lim S.O., Jung G. Reactive oxygen species downregulate catalase expression via methylation of a CpG island in the Oct-1 promoter. FEBS Lett. 2011, 585:3436-3441.
54. Ramos-Gomez M., Kwak M.K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., Kensler T.W. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. USA 2001, 98:3410-3415.
55. Ramos-Gomez M., Dolan P.M., Itoh K., Yamamoto M., Kensler T.W. Interactive effects of nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice. Carcinogenesis 2003, 24:461-467.
56. Rangasamy T., Cho C.Y., Thimmulappa R.K., Zhen L., Srisuma S.S., Kensler T.W., Yamamoto M., Petrache I., Tuder R.M., Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 2004, 114:1248-1259.
57. Rauch J., Kolch W., Mahmoudi M. Cell type-specific activation of AKT and ERK signaling pathways by small negatively-charged magnetic nanoparticles. Sci. Rep. 2012, 2:868.
58. Reuter S., Gupta S.C., Chaturvedi M.M., Aggarwal B.B. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 2010.
59. Sauer H., Wartenberg M., Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell. Physiol. Biochem. 2001, 11:173-186.
60. Staal Y.C., Hebels D.G., van Herwijnen M.H., Gottschalk R.W., van Schooten F.J., van Delft J.H. Binary PAH mixtures cause additive or antagonistic effects on gene expression but synergistic effects on DNA adduct formation. Carcinogenesis 2007, 28:2632-2640.
61. Sun X.F., Zhang H. NFKB and NFKBI polymorphisms in relation to susceptibility of tumour and other diseases. Histol. Histopathol. 2007, 22:1387-1398.
62. Sun Z., Wu T., Zhao F., Lau A., Birch C.M., Zhang D.D. KPNA6 (Importin {alpha}7)-mediated nuclear import of Keap1 represses the Nrf2-dependent antioxidant response. Mol. Cell. Biol. 2011, 31:1800-1811.
63. Tilton S.C., Karin N.J., Tolic A., Xie Y., Lai X., Hamilton R.F., Waters K.M., Holian A., Witzmann F.A., Orr G. Three human cell types respond to multi-walled carbon nanotubes and titanium dioxide nanobelts with cell-specific transcriptomic and proteomic expression patterns. Nanotoxicology 2014, 8:533-548.
64. Tudek B., Winczura A., Janik J., Siomek A., Foksinski M., Olinski R. Involvement of oxidatively damaged DNA and repair in cancer development and aging. Am. J. Transl. Res. 2010, 2:254-284.
65. Wang Z., Li Y., Sarkar F.H. Signaling mechanism(s) of reactive oxygen species in Epithelial-Mesenchymal Transition reminiscent of cancer stem cells in tumor progression. Curr. Stem Cell Res. Ther. 2010, 5:74-80.
66. Xie J., Shaikh Z.A. Cadmium-induced apoptosis in rat kidney epithelial cells involves decrease in nuclear factor-kappa B activity. Toxicol. Sci. 2006, 91:299-308.