Proteomic analysis of cellular responses to different concentrations of anti-benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide in human amniotic epithelial FL cells

Journal of Proteome Research

Volumn 6, Issue 12, 2007, Pages 4737-4748

  Shen, Wenyan ^a   Liu, Hui ^a   Yu, Yingnian ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Anti benzo(a)pyrene 7,8 dihydrodiol 9,10 epoxide; Differentially expressed proteomic profile; Matrix assisted laser desorption ionization time of flight mass spectrometry; Two dimensional electrophoresis

Indexed keywords

ANTI BENZO(A)PYRENE 7,8 DIHYDRODIOL 9,10 EPOXIDE; BIOLOGICAL MARKER; EPOXIDE; UNCLASSIFIED DRUG;

AMNION CELL; ARTICLE; CELL CYCLE; CELL METABOLISM; CELL PROLIFERATION; CELL TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; INCUBATION TIME; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEOMICS; SIGNAL TRANSDUCTION; SILVER STAINING; TWO DIMENSIONAL ELECTROPHORESIS;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; AMNION; CARCINOGENS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EPITHELIAL CELLS; HUMANS; MASS SPECTROMETRY; PROTEOMICS;

EID: 38049073102     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr070406b     Document Type: Article

References (64)

1. Phillips, D. H. Fifty years of benzo(a)pyrene. Nature 1983, 303 (5917), 468-72.
2. Bartsch, H.; Hietanen, E. The role of individual susceptibility in cancer burden related to environmental exposure. Environ. Health Perspect. 1996, 104 (3), 569-77.
3. Conney, A. H.; Chang, R. L.; Jerina, D. M.; Wei, S. J. Studies on the metabolism of benzo[a]pyrene and dose-dependent differences in the mutagenic profile of its ultimate carcinogenic metabolite. Drug Metab. Rev. 1994, 26 (1-2), 125-63.
4. Shimada, T.; Gillam, E. M.; Oda, Y.; Tsumura, F.; Sutter, T. R.; Guengerich, F. P.; Inoue, K. Metabolism of benzo[a]pyrene to trans-7,8-dihydroxy-7, 8-dihydrobenzo[a]pyrene by recombinant human cytochrome P450 1B1 and purified liver epoxide hydrolase. Chem. Res. Toxicol. 1999, 12 (7), 623-9.
5. Boysen, G.; Hecht, S. S. Analysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutat. Res. 2003, 543 (1), 17-30.
6. van Steeg, H. The role of nucleotide excision repair and loss of p53 in mutagenesis and carcinogenesis. Toxicol. Lett. 2001, 120 (1-3), 209-19.
7. Wani, M. A.; El-Mahdy, M. A.; Hamada, F. M.; Wani, G.; Zhu, Q.; Wang, Q. E.; Wani, A. A. Efficient repair of bulky anti-BPDE DNA adducts from non-transcribed DNA strand requires functional p53 but not p21(waf1/cip1) and pRb. Mutat. Res. 2002, 505 (1-2), 13-25.
8. Zhao, B.; Wang, J.; Geacintov, N. E.; Wang, Z. Poleta, Polzeta and Rev1 together are required for G to T transversion mutations induced by the (+)- and (-)-trans-anti-BPDE-N2-dG DNA adducts in yeast cells. Nucleic Acids Res. 2006, 34 (2), 417-25.
9. Zhang, Y.; Wu, X.; Guo, D.; Rechkoblit, O.; Geacintov, N. E.; Wang, Z. Two-step error-prone bypass of the (+)- and (-)-trans-anti-BPDE-N2-dG adducts by human DNA polymerases eta and kappa. Mutat. Res. 2002, 510 (1-2), 23-35.
10. Shackelford, R. E.; Kaufmann, W. K.; Paules, R. S. Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ. Health Perspect. 1999, 107 (1), 5-24.
11. Jeffy, B. D.; Chen, E. J.; Gudas, J. M.; Romagnolo, D. F. Disruption of cell cycle kinetics by benzo[a]pyrene: inverse expression patterns of BRCA-1 and p53 in MCF-7 cells arrested in S and G2. Neoplasia 2000, 2 (5), 460-70.
12. Akerman, G. S.; Rosenzweig, B. A.; Domon, O. E.; McGarrity, L. J.; Blankenship, L. R.; Tsai, C. A.; Culp, S. J.; MacGregor, J. T.; Sistare, F. D.; Chen, J. J.; Morris, S. M. Gene expression profiles and genetic damage in benzo(a)pyrene diol epoxide-exposed TK6 cells. Mutat. Res. 2004, 549 (1-2), 43-64.
13. Yu, Z.; Ford, B. N.; Glickman, B. W. Identification of genes responsive to BPDE treatment in HeLa cells using cDNA expression assays. Environ. Mol. Mutagen. 2000, 36 (3), 201-5.
14. Tannheimer, S. L.; Ethier, S. P.; Caldwell, K. K.; Burchiel, S. W. Benzo[a]pyrene- and TCDD-induced alterations in tyrosine phosphorylation and insulin-like growth factor signaling pathways in the MCF-10A human mammary epithelial cell line. Carcinogenesis 1998, 19 (7), 1291-7.
15. Yoshii, S.; Tanaka, M.; Otsuki, Y.; Fujiyama, T.; Kataoka, H.; Arai, H.; Hanai, H.; Sugimura, H. Involvement of alpha-PAK-interacting exchange factor in the PAK1-c-Jun NH(2)-terminal kinase 1 activation and apoptosis induced by benzo[a]pyrene. Mol. Cell. Biol. 2001, 21 (20), 6796-807.
16. Shi, Q.; Wang, L. E.; Bondy, M. L.; Brewster, A.; Singletary, S. E.; Wei, Q. Reduced DNA repair of benzo[a]pyrene diol epoxide-induced adducts and common XPD polymorphisms in breast cancer patients. Carcinogenesis 2004, 25 (9), 1695-700.
17. Hussain, S. P.; Amstad, P.; Raja, K.; Sawyer, M.; Hofseth, L.; Shields, P. G.; Hewer, A.; Phillips, D. H.; Ryberg, D.; Haugen, A.; Harris, C. C. Mutability of p53 hotspot codons to benzo(a)pyrene diol epoxide (BPDE) and the frequency of p53 mutations in nontumorous human lung. Cancer Res. 2001, 61 (17), 6350-5.
18. Weisenberger, D. J.; Romano, L. J. Cytosine methylation in a CpG sequence leads to enhanced reactivity with Benzo[a]pyrene diol epoxide that correlates with a conformational change. J. Biol. Chem. 1999, 274 (34), 23948-55.
19. Olden, K.; Wilson, S. Environmental health and genomics: visions and implications. Nat. Rev. Genet. 2000, 1 (2), 149-53.
20. Luo, W.; Fan, W.; Xie, H.; Jing, L.; Ricicki, E.; Vouros, P.; Zhao, L. P.; Zarbl, H. Phenotypic anchoring of global gene expression profiles induced by N-hydroxy-4-acetylaminobiphenyl and benzo[a]pyrene diol epoxide reveals correlations between expression profiles and mechanism of toxicity. Chem. Res. Toxicol. 2005, 18 (4), 619-29.
21. Petricoin, E. F.; Zoon, K. C.; Kohn, E. C.; Barrett, J. C.; Liotta, L. A. Clinical proteomics: translating benchside promise into bedside reality. Nat. Rev. Drug Discovery 2002, 1 (9), 683-95.
22. Hegde, P. S.; White, I. R.; Debouck, C. Interplay of transcriptomics and proteomics. Curr. Opin. Biotechnol. 2003, 14 (6), 647-51.
23. Oh, S.; Im, H.; Oh, E.; Lee, J.; Khim, J. Y.; Mun, J.; Kim, Y.; Lee, E.; Kim, J.; Sul, D. Effects of benzo(a)pyrene on protein expression in Jurkat T-cells. Proteomics 2004, 4 (11), 3514-26.
24. Gao, Z.; Jin, J.; Yang, J.; Yu, Y. Zinc finger proteins and other transcription regulators as response proteins in benzo[a]pyrene exposed cells. Mutat. Res. 2004, 550 (1-2), 11-24.
25. Chen, S.; Nguyen, N.; Tamura, K.; Karin, M.; Tukey, R. H. The role of the Ah receptor and p38 in benzo[a]pyrene-7,8-dihydrodiol and benzo[a]pyrene-7,8- dihydrodiol-9,10-epoxide-induced apoptosis. J. Biol. Chem. 2003, 278 (21), 19526-33.
26. Liu, G.; Yin, Y.; Endoplasmic reticulum stress is involved in N-methyl-N′-nitro-N- nitrosoguanidine, benzo[a]pyrene-7,8-dihydrodiol-9, 10-epoxide and mitomycin-induced cellular response in FL cells. Chin. J. Pathophysiol. 2006, 22, 1-6.
27. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-54.
28. Kirfel, J., Magin, T. M.; Reichelt, J. Keratins: a structural scaffold with emerging functions. Cell. Mol. Life Sci. 2003, 60 (1), 56-71.
29. Coulombe, P. A.; Omary, M. B. 'Hard' and 'soft' principles defining the structure, function and regulation of keratin intermediate filaments. Curr. Opin. Cell. Biol. 2002, 14 (1), 110-22.
30. Ku, N. O.; Zhou, X.; Toivola, D. M.; Omary, M. B. The cytoskeleton of digestive epithelia in health and disease. Am. J. Physiol. 1999, 277 (6Pt 1), G1108-37.
31. Zatloukal, K.; Stumptner, C.; Lehner, M.; Denk, H.; Baribault, H.; Eshkind, L. G.; Franke, W. W. Cytokeratin 8 protects from hepatotoxicity, and its ratio to cytokeratin 18 determines the ability of hepatocytes to form Mallory bodies. Am. J. Pathol. 2000, 156 (4), 1263-74.
32. Collard, C. D.; Montalto, M. C.; Reenstra, W. R.; Buras, J. A.; Stahl, G. L. Endothelial oxidative stress activates the lectin complement pathway: role of cytokeratin 1. Am. J. Pathol. 2001, 159 (3), 1045-54.
33. Li, R.; Liu, X. L.; Du, Q. F.; Zhang, S.; Luo, R. C.; Zhou, S. Y. [Proteome analysis of apoptotic K562 cells induced by harringtonine]. Zhonghua Xueyexue Zazhi 2004, 25 (6), 323-7.
34. Paramio, J. M.; Casanova, M. L.; Segrelles, C.; Mittnacht, S.; Lane, E. B.; Jorcano, J. L. Modulation of cell proliferation by cytokeratins K10 and K16. Mol. Cell. Biol. 1999, 19 (4), 3086-94.
35. Paramio, J. M.; Segrelles, C.; Ruiz, S.; Jorcano, J. L. Inhibition of protein kinase B (PKB) and PKCzeta mediates keratin K10-induced cell cycle arrest. Mol. Cell. Biol. 2001, 21 (21), 7449-59.
36. Santos, M.; Paramio, J. M.; Bravo, A.; Ramirez, A.; Jorcano, J. L. The expression of keratin k10 in the basal layer of the epidermis inhibits cell proliferation and prevents skin tumorigenesis. J. Biol. Chem. 2002, 277 (21), 19122-30.
37. Lucas, S. D.; Ek, B.; Rask, L.; Rastad, J.; Akerstrom, G.; Juhlin, C. Aberrantly expressed cytokeratin 1, a tumor-associated autoantigen in papillary thyroid carcinoma. Int. J. Cancer 1997, 73 (2), 171-7.
38. Urnov, F. D. A feel for the template: zinc finger protein transcription factors and chromatin. Biochem Cell Biol 2002, 80 (3), 321-33.
39. Ladomery, M.; Dellaire, G. Multifunctional zinc finger proteins in development and disease. Ann Hum Genet 2002, 66 (Pt 5-6), 331-42.
40. Sun, Y.; Shao, H.; Li, Z.; Liu, J.; Gao, L.; Peng, X.; Meng, Y.; Li, W. ZNF268, a novel kruppel-like zinc finger protein, is implicated in early human liver development. Int. J. Mol. Med. 2004, 14 (6), 971-5.
41. Krackhardt, A. M.; Witzens, M.; Harig, S.; Hodi, F. S.; Zauls, A. J.; Chessia, M.; Barrett, P.; Gribben, J. G. Identification of tumor-associated antigens in chronic lymphocytic leukemia by SEREX. Blood 2002, 100 (6), 2123-31.
42. Jung, M.; Kondratyev, A. D.; Dritschilo, A. Elongation factor 1 delta is enhanced following exposure to ionizing radiation. Cancer Res. 1994, 54 (10), 2541-3.
43. Joseph, P.; Lei, Y. X.; Whong, W. Z.; Ong, T. M. Oncogenic potential of mouse translation elongation factor-1 delta, a novel cadmium-responsive proto-oncogene. J. Biol. Chem. 2002, 277 (8), 6131-6.
44. Suh, K. S.; Mutoh, M.; Gerdes, M.; Crutchley, J. M.; Mutoh, T.; Edwards, L. E.; Dumont, R. A.; Sodha, P.; Cheng, C.; Glick, A.; Yuspa, S. H. Antisense suppression of the chloride intracellular channel family induces apoptosis, enhances tumor necrosis factor {alpha}-induced apoptosis, and inhibits tumor growth. Cancer Res. 2005, 65 (2), 562-71.
45. Doan, L.; Yagi, H.; Jerina, D. M.; Whalen, D. L. Chloride ion catalyzed conformational inversion of carbocation intermediates in the hydrolysis of a benzo[a]pyrene 7,8-diol 9,10-epoxide. J. Am. Chem. Soc. 2002, 124 (48), 14382-7.
46. Wolfe, A. R.; Yamamoto, J.; Meehan, T. Chloride ions catalyze the formation of cis adducts in the binding of anti-benzo[a]pyrene diol epoxide to nucleic acids. Proc. Natl. Acad. Sci. U.S.A. 1994, 91 (4), 1371-5.
47. Umbricht, C. B.; Evron, E.; Gabrielson, E.; Ferguson, A.; Marks, J.; Sukumar, S. Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene 2001, 20 (26), 3348-53.
48. Cheng, L.; Pan, C. X.; Zhang, J. T.; Zhang, S.; Kinch, M. S.; Li, L.; Baldridge, L. A.; Wade, C.; Hu, Z.; Koch, M. O.; Ulbright, T. M.; Eble, J. N. Loss of 14-3-3sigma in prostate cancer and its precursors. Clin. Cancer Res. 2004, 10 (9), 3064-8.
49. Hermeking, H.; Lengauer, C.; Polyak, K.; He, T. C.; Zhang, L.; Thiagalingam, S.; Kinzler, K. W.; Vogelstein, B. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell 1997, 1 (1), 3-11.
50. Wang, A.; Gu, J.; Judson-Kremer, K.; Powell, K. L.; Mistry, H.; Simhambhatla, P.; Aldaz, C. M.; Gaddis, S.; MacLeod, M. C. Response of human mammary epithelial cells to DNA damage induced by BPDE: involvement of novel regulatory pathways. Carcinogenesis 2003, 24 (2), 225-34.
51. Meyer, B. K.; Perdew, G. H. Characterization of the AhR-hsp90-XAP2 core complex and the role of the immunophilin-related protein XAP2 in AhR stabilization. Biochemistry 1999, 38 (28), 8907-17.
52. Ma, Q.; Whitlock, J. P. Jr., A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J. Biol. Chem. 1997, 272 (14), 8878-84.
53. Rowlands, J. C.; Gustafsson, J. A. Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 1997, 27 (2), 109-34.
54. Griffith, O. W.; Mulcahy, R. T. The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase. Adv. Enzymol. Relat. Areas Mol. Biol. 1999, 73, 209-67, xii
55. Meister, A. Glutathione, ascorbate, and cellular protection. Cancer Res. 1994, 54 (7 Suppl.), 1969s-75s.
56. Fahey, R. C.; Sundquist, A. R. Evolution of glutathione metabolism. Adv. Enzymol. Relat. Areas Mol. Biol. 1991, 64, 1-53.
57. Yuan, J. W.; Krieger, J. A.; Maples, K. R.; Born, J. L.; Burchiel, S. W. Polycyclic aromatic hydrocarbons decrease intracellular glutathione levels in the A20.1 murine B cell lymphoma. Fundam. Appl. Toxicol. 1994, 23 (3), 336-41.
58. Maniatis, T. A ubiquitin ligase complex essential for the NF-kappaB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 1999, 13 (5), 505-10.
59. Peters, J. M. Emil proteolysis: how SCF(beta-Trcp1) helps to activate the anaphase-promoting complex. Mol. Cell 2003, 11 (6), 1420-1.
60. Weng, M. W.; Hsiao, Y. M.; Chen, C. J.; Wang, J. P.; Chen, W. C.; Ko, J. L. Benzo[a]pyrene diol epoxide up-regulates COX-2 expression through NF-kappaB in rat astrocytes. Toxicol. Lett. 2004, 151 (2), 345-55.
61. Keshava, C.; Whipkey, D.; Weston, A. Transcriptional signatures of environmentally relevant exposures in normal human mammary epithelial cells: benzo[a]pyrene. Cancer Lett. 2005, 221 (2), 201-11.
62. Wittmann-Liebold, B.; Graack, H. R.; Pohl, T. Two-dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics 2006, 6 (17), 4688-703.
63. Morandell, S.; Stasyk, T.; Grosstessner-Hain, K.; Roitinger, E.; Mechtler, K.; Bonn, G. K.; Huber, L. A. Phosphoproteomics strategies for the functional analysis of signal transduction. Proteomics 2006, 6 (14), 4047-56.
64. Raggiaschi, R.; Gotta, S.; Terstappen, G. C. Phosphoproteome analysis. Biosci. Rep. 2005, 25 (1-2), 33-44.