Functional & Integrative Genomics

, Volume 10, Issue 3, pp 417–424

Mammalian cytochrome CYP2E1 triggered differential gene regulation in response to trichloroethylene (TCE) in a transgenic poplar

  • Jun Won Kang
  • Hui-Wen Wilkerson
  • Federico M. Farin
  • Theo K. Bammler
  • Richard P. Beyer
  • Stuart E. Strand
  • Sharon L. Doty
Short Communication

Abstract

Trichloroethylene (TCE) is an important environmental contaminant of soil, groundwater, and air. Studies of the metabolism of TCE by poplar trees suggest that cytochrome P450 enzymes are involved. Using poplar genome microarrays, we report a number of putative genes that are differentially expressed in response to TCE. In a previous study, transgenic hybrid poplar plants expressing mammalian cytochrome P450 2E1 (CYP2E1) had increased metabolism of TCE. In the vector control plants for this construct, 24 h following TCE exposure, 517 genes were upregulated and 650 genes were downregulated over 2-fold when compared with the non-exposed vector control plants. However, in the transgenic CYP2E1 plant, line 78, 1,601 genes were upregulated and 1,705 genes were downregulated over 2-fold when compared with the non-exposed transgenic CYP2E1 plant. It appeared that the CYP2E1 transgenic hybrid poplar plants overexpressing mammalian CYP2E1 showed a larger number of differentially expressed transcripts, suggesting a metabolic pathway for TCE to metabolites had been initiated by activity of CYP2E1 on TCE. These results suggest that either the over-expression of the CYP2E1 gene or the abundance of TCE metabolites from CYP450 2E1 activity triggered a strong genetic response to TCE. Particularly, cytochrome p450s, glutathione S-transferases, glucosyltransferases, and ABC transporters in the CYP2E1 transgenic hybrid poplar plants were highly expressed compared with in vector controls.

Keywords

Cytochrome P450 Microarray Phytoremediation Poplar TCE (trichloroethylene) 

Supplementary material

10142_2010_165_MOESM1_ESM.xls (108 kb)
Supplemental Fig. 1(XLS 107 kb)
10142_2010_165_MOESM2_ESM.pptx (146 kb)
Supplemental Fig. 2(PPTX 146 kb)
10142_2010_165_MOESM3_ESM.xls (29 kb)
Supplemental Table 1(XLS 29 kb)
10142_2010_165_MOESM4_ESM.xls (46 kb)
Supplemental Table 2(XLS 46 kb)

References

  1. Ada AO, Yilmazer M, Suzen S, Demiroglu C, Demirbag AE, EfeI S, Alemdar Y, Burgaz S, Iscan M (2007) Cytochrome P450 (CYP) and glutathione S-transferases (GST) polymorphisms (CYP1A1, CYP1B1, GSTM1, GSTP1 and GSTT1) and urinary levels of 1-hydroxypyrene in Turkish coke oven workers. Genet Mol Biol 30:511–519Google Scholar
  2. Anzenbacher P, Anzenbacherová E (2001) Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci (CMLS) 58:737–747CrossRefGoogle Scholar
  3. Bollag JM, Shuttleworth KL, Anderson DH (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54:3086–3091PubMedGoogle Scholar
  4. Brazier M, Cole DJ, Edwards R (2002) O-Glucosyltransferase activities toward phenolic natural products and xenobiotics in wheat and herbicide-resistant and herbicide-susceptible black-grass (Alopecurus myosuroides). Phytochemistry 59:149–156CrossRefPubMedGoogle Scholar
  5. Cai H, Guengerich FP (2001) Reaction of trichloroethylene and trichloroethylene oxide with cytochrome P450 enzymes: inactivation and sites of modification. Chem Res Toxicol 14:451–458CrossRefPubMedGoogle Scholar
  6. DeRidder BP, Dixon DP, Beussman DJ, Edwards R, Goldsbrough PB (2002) Induction of glutathione S-transferases in Arabidopsis by herbicide safeners. Plant Physiol 130:1497–1505CrossRefPubMedGoogle Scholar
  7. Didierjean L, Laurence G, Roberta P, Sze-Mei Cindy L et al (2002) Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytchrome P450 enzyme for Jerusalem artichoke. Plant Physiol 130:179CrossRefPubMedGoogle Scholar
  8. Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266CrossRefPubMedGoogle Scholar
  9. Doty SL, James CA, Moore AL, Vajzovic A, Singleton GL, Ma C, Khan Z, Xin G, Kang JW, Park JY, Meilan R, Strauss SH, Wilkerson J, Farin F, Strand SE (2007) Enhanced phytoremediation of volatile environmental pollutants with transgenic trees. Proc Natl Acad Sci 104:16816–16821CrossRefPubMedGoogle Scholar
  10. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198CrossRefPubMedGoogle Scholar
  11. Ehlting J, Hamberger B, Million-Rousseau R, Werck-Reichhart D (2006) Cytochromes P450 in phenolic metabolism. Phytochem Rev 5:239–270CrossRefGoogle Scholar
  12. Ekman DR, Lorenz WW, Przybyla AE, Wolfe NL, Dean JFD (2003) SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2, 4, 6-trinitrotoluene. Plant Physiol 133:1397–1406CrossRefPubMedGoogle Scholar
  13. Ferguson JF, Pietari JMH (2000) Anaerobic transformations and bioremediation of chlorinated solvents. Environ Pollut 107:209–215CrossRefPubMedGoogle Scholar
  14. Gandia-Herrero F, Lorenz A, Larson T, Graham IA, Bowles DJ, Rylott EL, Bruce NC (2008) Detoxification of the explosive 2, 4, 6-trinitrotoluene in Arabidopsis: discovery of bifunctional O- and C-glucosyltransferases. Plant J 56:963–974CrossRefPubMedGoogle Scholar
  15. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling SD M, Ellis B, Gautier L, Ge JG Y, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li MM C, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:1–16CrossRefGoogle Scholar
  16. Gordon M, Choe N, Duffy J, Gordon E, Heilman P, Muiznieks I, Ruszaj M, Shurtleff BB, Strand S, Wilmoth J, Newman LA (1998) Phytoremediation of trichloroethylene with hybrid poplars. Environ Health Perspect 106:1001–1004CrossRefPubMedGoogle Scholar
  17. Hefner T, Arend J, Warzecha H, Siems K, Stöckigt J (2002) Arbutin synthase, a novel member of the NRD1[beta] glycosyltransferase family, is a unique multifunctional enzyme converting various natural products and xenobiotics. Bioorg Med Chem 10:1731–1741CrossRefPubMedGoogle Scholar
  18. Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, Hanley D, Kiphart D, Zhuang M, Huang W, Mueller LA, Bhattacharyya D, Bhaya D, Sobral BW, Beavis W, Meinke DW, Town CD, Somerville C, Rhee SY (2001) The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 29:102–105CrossRefPubMedGoogle Scholar
  19. Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837PubMedGoogle Scholar
  20. Khatisashvili G, Gordeziani M, Kvesitadze G, Korte F (1997) Plant monooxygenases: participation in xenobiotic oxidation. Ecotoxicol Environ Saf 36:118–122CrossRefPubMedGoogle Scholar
  21. Komives T, Gullner G, Rennenberg H, Casida JE (2003) Ability of poplar (Populus spp.) to detoxify chloroacetanilide herbicides. Water, Air, & Soil Pollution: Focus 3:277–283Google Scholar
  22. Lee W, Wood TK, Chen W (2006) Engineering TCE-degrading rhizobacteria for heavy metal accumulation and enhanced TCE degradation. Biotechnol Bioeng 95:399–403CrossRefPubMedGoogle Scholar
  23. Ma X, Richter AR, Albers S, Burken JG (2004) Phytoremediation of MTBE with hybrid poplar trees. Int J Phytoremediation 6:157–167CrossRefPubMedGoogle Scholar
  24. McCutcheon SC, Schnoor JL (2003) Phytoremediation: transformation and control of contaminants. Wiley, HobokenGoogle Scholar
  25. McLean KJ, Sabri M, Marshall KR, Lawson RJ, Lewis DG, Clift D, Balding PR, Dunford AJ, Warman AJ, McVey JP, Quinn AM, Sutcliffe MJ, Scrutton NS, Munro AW (2005) Biodiversity of cytochrome P450 redox systems. Biochem Soc Trans 33:796–801CrossRefPubMedGoogle Scholar
  26. Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162CrossRefPubMedGoogle Scholar
  27. Milton G, Choe N, Duffy J, Gordon E, Heilman P, Muiznieks I, Ruszaj M, Shurtleff BB, Strand S, Wilmoth J, Newman LA (1998) Phytoremediation of trichloroethylene with hybrid poplars. Environ Health Perspect 106:1001–1004CrossRefGoogle Scholar
  28. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  29. Nelson D (2006) Plant cytochrome P450s from moss to poplar. Phytochem Rev 5:193–204CrossRefGoogle Scholar
  30. Newman LA, Strand SE, Choe N, Duffy J, Ekuan G, Ruszaj M, Shurtleff BB, Wilmoth J, Heilman P, Gordon MP (1997) Uptake and biotransformation of trichloroethylene by hybrid poplars. Environ Sci Technol 31:1062–1067CrossRefGoogle Scholar
  31. Orchard BJ, Doucette WJ, Chard JK, Bugbee B (2000) Uptake of trichloroethylene by hybrid poplar trees grown hydroponically in flow-through plant growth chambers. Environ Toxicol Chem 19:895–903CrossRefGoogle Scholar
  32. Peng X, Wood C, Blalock E, Chen K, Landfield P, Stromberg A (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4:26CrossRefPubMedGoogle Scholar
  33. Rawls R (1996) Turning on carcinogens: research on several fronts reveals how humans metabolize cancer-causing substances. Chem Eng News 74:31–34Google Scholar
  34. Rennenberg ADPH (2005) Phytoremediation EMBO reports 6:497–501Google Scholar
  35. Ross J, Li Y, Lim E, Bowles D (2001) Higher plant glycosyltransferases. Genome Biol 2:3004.3001–3004.3006, reviewsCrossRefGoogle Scholar
  36. Sandermann H Jr (1994) Higher plant metabolism of xenobiotics: the 'green liver' concept. Pharmacogenetics 4:225–241CrossRefPubMedGoogle Scholar
  37. Schröder P (2002) The role of glutathione and glutathione S-transferases in plant reaction and adaptation to Xenobiotics. In: Grill D, Tausz M, de Kok L (eds) Significance of glutathione to plant adaptation to the environment. Kluwer, Dordrecht, pp 155–183CrossRefGoogle Scholar
  38. Shang TQ, Doty SL, Wilson AM, Howald WN, Gordon MP (2001) Trichloroethylene oxidative metabolism in plants: the trichloroethanol pathway. Phytochemistry 58:1055–1065CrossRefPubMedGoogle Scholar
  39. Siminszky B, Corbin FT, Ward ER, Fleischmann TJ, Dewey RE (1999) Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenylurea herbicides. Proc Natl Acad Sci 96:1750–1755CrossRefPubMedGoogle Scholar
  40. Smyth GK (2004) Linear models and empirical bayes methods for assessing dierential expression in microarray experiments. Stat Appl Genet Mol Biol 3:1–26Google Scholar
  41. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  42. Van Aken B (2008) Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Trends Biotechnol 26:225–227CrossRefPubMedGoogle Scholar
  43. Wang G-D, Chen X-Y (2007) Detoxification of soil phenolic pollutants by plant secretory enzyme. In: Willey N (ed) Phytoremediation: methods and reviews. Humana Press, Totowa, pp 49–57CrossRefGoogle Scholar
  44. Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1:3003.3001–3003.3009, reviewsCrossRefGoogle Scholar
  45. Williams PA, Cosme J, Ward A, Angove HC, Vinkovi DM, Jhoti H (2003) Crystal structure of human cytochrome P450 2C9 with bound warfarin. Nature 424:464–468CrossRefPubMedGoogle Scholar
  46. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917CrossRefGoogle Scholar
  47. Xiang C, Werner BL, Christensen ELM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jun Won Kang
    • 1
  • Hui-Wen Wilkerson
    • 2
  • Federico M. Farin
    • 2
  • Theo K. Bammler
    • 2
  • Richard P. Beyer
    • 2
  • Stuart E. Strand
    • 1
    • 3
  • Sharon L. Doty
    • 1
  1. 1.School of Forest Resources, College of the EnvironmentUniversity of WashingtonSeattleUSA
  2. 2.Department of Environmental and Occupational Health SciencesUniversity of WashingtonSeattleUSA
  3. 3.Department of Civil and Environmental EngineeringUniversity of WashingtonSeattleUSA

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