Identification of potential protein targets of isothiocyanates by proteomics

Chemical Research in Toxicology

Volumn 24, Issue 10, 2011, Pages 1735-1743

  Mi, Lixin ^a   Hood, Brian L ^b,c   Stewart, Nicolas A ^b,d   Xiao, Zhen ^b   Govind, Sudha ^a   Wang, Xiantao ^a   Conrads, Thomas P ^b,c   Veenstra, Timothy D ^b   Chung, Fung Lung ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b SAIC FREDERICK INC   (United States)

^c BETTY AND GUY BEATTY CENTER FOR INTEGRATED RESEARCH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAZOLENE SODIUM; CARBON 14; CELL PROTEIN; CYTOSKELETON PROTEIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHENETHYL ISOTHIOCYANATE; PROTEASOME; RAF PROTEIN; SULFORAPHANE; TUBULIN;

ARTICLE; CANCER PREVENTION; CELL LYSATE; DRUG BINDING; DRUG MECHANISM; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TARGETING; PROTEOMICS; RADIOACTIVITY; TWO DIMENSIONAL GEL ELECTROPHORESIS; X RAY FILM;

ANTICARCINOGENIC AGENTS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HUMANS; ISOTHIOCYANATES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY; TUBULIN;

EID: 80054731134     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx2002806     Document Type: Article

References (52)

1. WHO (2004) Cruciferous Vegetables, Isothiocyanates and Indoles, IARC Handbook on Cancer Prevention, Vol. 9, IARC, Lyon, France.
2. Hecht, S. S. (2003) Inhibition of carcinogenesis by isothiocyanates Drug Metab. Rev. 32, 395-411 (Pubitemid 32001915)
3. London, S. J., Yuan, J. M., Chung, F. L., Gao, Y. T., Coetzee, G. A., Ross, R. K., and Yu, M. C. (2000) Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: a prospective study of men in Shanghai, China Lancet 356, 724-729 (Pubitemid 30663242)
4. Mi, L., Di Pasqua, A. J., and Chung, F. L. Proteins as binding targets of isothiocyanates in cancer prevention. Carcinogenesis 2011, not supplied.
5. Conaway, C. C., Wang, C. X., Pittman, B., Yang, Y. M., Schwartz, J. E., Tian, D., McIntee, E. J., Hecht, S. S., and Chung., F. L. (2005) Phenethyl isothiocyanate and sulforaphane and their N-acetylcysteine conjugates inhibit malignant progression of lung adenomas induced by tobacco carcinogens in A/J mice Cancer Res. 65, 8548-8557 (Pubitemid 41330624)
6. Chung, F. L., Conaway, C. C., Rao, C. V., and Reddy, B. S. (2000) Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate Carcinogenesis 21, 2287-2291 (Pubitemid 32049237)
7. Keum, Y. S., Jeong, W. S., and Kong, A. N. (2004) Chemoprevention by isothiocyanates and their underlying molecular signaling mechanisms Mutat. Res. 555, 191-202 (Pubitemid 39345404)
8. Xiao, D., Choi, S., Lee, Y. J., and Singh, S. V. (2005) Role of mitogen-activated protein kinases in phenethyl isothiocyanate-induced apoptosis in human prostate cancer cells Mol. Carcinog. 43, 130-40 (Pubitemid 40944238)
9. Chen, Y. R., Wang, W., Kong, A. N., and Tan, T. H. (1998) Molecular mechanisms of c-Jun N-terminal kinase-mediated apoptosis induced by anticarcinogenic isothiocyanates J. Biol. Chem. 273, 1769-1775 (Pubitemid 28133709)
10. Gamet-Payrastre, L., Li, P., Lumeau, S., Cassar, G., Dupont, M. A., Chevolleau, S., Gasc, N., Tulliez, J., and Tercé, F. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells Cancer Res. 60, 1426-1433 (Pubitemid 30152017)
11. Yang, Y. M., Conaway, C. C., Chiao, J. W., Wang, C. W., Amin, S., Whysner, J., Dai, W., Reinhardt, J., and Chung, F. L. (2002) Inhibition of benzo(a)pyrene-induced lung tumorigenesis in A/J mice by dietary N-acetylcysteine conjugates of benzyl and phenethyl isothiocyanates during the postinitiation phase is associated with activation of mitogen-activated protein kinases and p53 activity and induction of apoptosis Cancer Res. 62, 2-7 (Pubitemid 34073975)
12. Zhang, Y. and Talalay, P. (1998) Mechanism of differential potencies of isothiocyanates as inducers of anticarcinogenic Phase 2 enzymes Cancer Res. 58, 4632-4639 (Pubitemid 28480628)
13. Xiao, D., Lew, K. L., Zeng, Y., Xiao, H., Marynowski, S. W., Dhir, R., and Singh, S. V. (2006) Phenethyl isothiocyanate-induced apoptosis in PC-3 human prostate cancer cells is mediated by reactive oxygen species-dependent disruption of the mitochondrial membrane potential Carcinogenesis 27, 2223-2234 (Pubitemid 44644811)
14. Podhradský, D., Drobnica, L., and Kristian, P. (1979) Reactions of cysteine, its derivatives, glutathione coenzyme A, and dihydrolipoic acid with isothiocyanates Experientia 35, 154-155 (Pubitemid 9118408)
15. Von Weymarn, L. B., Chun, J. A., and Hollenberg, P. F. (2006) Effects of benzyl and phenethyl isothiocyanate on P450s 2A6 and 2A13: potential for chemoprevention in smokers Carcinogenesis 27, 782-790
16. Dinkova-Kostova, A. T., Holtzclaw, W. D., Cole, R. N., Itoh, K., Wakabayashi, N., Katoh, Y., Yamamoto, M., and Talalay, P. (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proc. Natl. Acad. Sci. U.S.A. 99, 11908-11913 (Pubitemid 34994497)
17. Mi, L., Wang, X., Govind, G., Hood, B. L., Veenstra, T. D., Conrads, T. P., Saha, D. T., Goldman, R., and Chung, F. L. (2007) The role of protein binding in induction of apoptosis by phenethyl isothiocyanate and sulforaphane in human non-small lung cancer cells Cancer Res. 67, 6409-6416 (Pubitemid 47037525)
18. Mi, L., Xiao, Z., Hood, B. L., Dakshanamurthy, S., Wang, X., Govind, S., Conrads, T. P., Veenstra, T. D., and Chung, F. L. (2008) Covalent binding to tubulin by isothiocyanates: a mechanism of cell growth arrest and apoptosis J. Biol. Chem. 283, 22136-22146
19. Mi, L., Gan, N., Cheema, A., Dakshanamurthy, S., Yang, D. C. H., and Chung, F. L. (2009) Cancer preventive isothiocyanates induce selective degradation of cellular alpha- and beta-tubulins by proteasomes J. Biol. Chem. 284, 17039-17051
20. Mi, L., Gan, N., and Chung, F. L. (2009) Aggresome-like structure induced by isothiocyanates is novel proteasome-dependent degradation machinery Biochem. Biophys. Res. Commun. 388, 456-462
21. Mi, L., Gan, N., and Chung, F. L. (2011) Isothiocyanates inhibit proteasome activity and proliferation of multiple myeloma cells Carcinogenesis 32, 216-223
22. Conaway, C. C., Jiao, D., Kohri, T., Liebes, L., and Chung, F. L. (1999) Disposition and pharmacokinetics of phenethyl isothiocyanate and 6-phenylhexyl isothiocyanate in F344 rats Drug Metab. Dispos. 27, 13-20 (Pubitemid 29060994)
23. D'Souza, C. A., Amin, S., and Desai, D. (2003) A facile and efficient synthesis of 14C-labelled sulforaphane J. Labelled Compd. Radiopharm. 46, 851-859 (Pubitemid 37047673)
24. Simpson, R. J. (2003) Proteins and Proteomics, pp 143-218, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P. G. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis Electrophoresis 25, 1327-1333 (Pubitemid 38801651)
26. Conrads, T. P., Tocci, G. M., Hood, B. L., Zhang, C. O., Guo, L., Koch, K. R., Michejda, C. J., Veenstra, T. D., and Keay, S. K. (2006) CKAP4/p63 is a receptor for the frizzled-8 protein-related antiproliferative factor from interstitial cystitis patients J. Biol. Chem. 49, 37836-37843 (Pubitemid 46042086)
27. Suh, S. K., Hood, B. L., Kim, B. J., Conrads, T. P., Veenstra, T. D., and Song, B. J. (2004) Identification of oxidized mitochondrial proteins in alcohol-exposed human hepatoma cells and mouse liver Proteomics 4, 3401-3412 (Pubitemid 39525289)
28. Dalle-Donne, I., Rossi, R., Milzani, A., Di Simplicio, P., and Colombo, R. (2001) The actin cytoskeleton response to oxidants: from small heat shock protein phosphorylation to changes in the redox state of actin itself Free Radical Biol. Med. 31, 1624-1632 (Pubitemid 34024985)
29. Malm, B. (1984) Chemical modification of Cys-374 of actin interferes with the formation of the profilactin complex FEBS Lett. 173, 399-402 (Pubitemid 14067830)
30. Al-Saad, S., Al-Shibli, K., Donnem, T., Persson, M., Bremnes, R. M., and Busund, L. T. (2008) The prognostic impact of NF-kappaB p105, vimentin, E-cadherin and Par6 expression in epithelial and stromal compartment in non-small-cell lung cancer Br. J. Cancer 99, 1476-1483
31. Liu, L. K., Jiang, X. Y., Zhou, X. X., Wang, D. M., Song, X. L., and Jiang, H. B. (2010) Upregulation of vimentin and aberrant expression of E-cadherin/β-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome Mod. Pathol. 23, 213-224
32. Stamatakis, K., Sánchez-Gómez, F. J., and Pérez-Sala, D. (2006) Identification of Novel Protein Targets for Modification by 15-Deoxy-12,14-Prostaglandin J2 in Mesangial Cells Reveals Multiple Interactions with the Cytoskeleton J. Am. Soc. Nephrol. 17, 89-98
33. Hu, Y., Urig, S., Koncarevic, S., Wu, X., Fischer, M., Rahlfs, S., Mersch-Sundermann, V., and Becker, K. (2007) Glutathione- and thioredoxin-related enzymes are modulated by sulfur-containing chemopreventive agents Biol. Chem. 388, 1069-1081 (Pubitemid 47584309)
34. Haendeler, J. (2006) Thioredoxin-1 and posttranslational modifications Antioxid. Redox Signaling 8, 1723-1728 (Pubitemid 44726344)
35. Hashemy, S. I., Johansson, C., Berndt, C., Lillig, C. H., and Holmgren, A. (2007) Oxidation and S-nitrosylation of cysteines in human cytosolic and mitochondrial glutaredoxins: effects on structure and activity J. Biol. Chem. 282, 14428-14436 (Pubitemid 47100442)
36. Vembar, S. S. and Brodsky, J. L. (2008) One step at a time: endoplasmic reticulum-associated degradation Nat. Rev. Mol. Cell Biol. 9, 944-957
37. Noguchi, M., Takata, T., Kimura, Y., Manno, A., Murakami, K., Koike, M., Ohizumi, H., Hori, S., and Kakizuka, A. (2005) ATPase activity of p97/valosin-containing protein is regulated by oxidative modification of the evolutionally conserved cysteine 522 residue in Walker A motif J. Biol. Chem. 280, 41332-41341 (Pubitemid 41832190)
38. Yamamoto, S., Tomita, Y., Uruno, T., Hoshida, Y., Qiu, Y., Iizuka, N., Nakamichi, I., Miyauchi, A., and Aozasa, K. (2004) Increased expression of valosin-containing protein (p97) is correlated with disease recurrence in follicular thyroid cancer Clin. Cancer Res. 10, 5558-5565
39. Yamamoto, S., Tomita, Y., Hoshida, Y., Nagano, H., Dono, K., Umeshita, K., Sakon, M., Ishikawa, O., Ohigashi, H., Nakamori, S., Monden, M., and Aozasa, K. (2004) Expression level of hepatoma-derived growth factor correlates with tumor recurrence of esophageal carcinoma Ann. Surg. Oncol. 11, 697-704
40. Liu, Q., Levy, E. J., and Chirico, W. J. (1996) N-Ethylmaleimide inactivates a nucleotide-free Hsp70 molecular chaperone J. Biol. Chem. 271, 29937-29944 (Pubitemid 26389630)
41. Pasupuleti, N., Gangadhariah, M., Padmanabha, S., Santhoshkumar, P., and Nagaraj, R. H. (2010) The role of the cysteine residue in the chaperone and anti-apoptotic functions of human Hsp27 J. Cell Biochem. 110, 408-419
42. Viitanen, P. V., Lorimer, G., Bergmeier, W., Weiss, C., Kessel, M., and Goloubinoff, P. (1998) Purification of mammalian mitochondrial chaperonin 60 through in vitro reconstitution of active oligomers Methods Enzymol. 290, 203-217 (Pubitemid 28157752)
43. Nagumo, Y., Kakeya, H., Shoji, M., Hayashi, Y., Dohmae, N., and Osada, H. (2005) Epolactaene binds human Hsp60 Cys442 resulting in the inhibition of chaperone activity Biochem. J. 387, 835-840 (Pubitemid 40685719)
44. Nakamura, Y., Kawakami, M., Yoshihiro, A., Miyoshi, N., Ohigashi, H., Kawai, K., Osawa, T., and Uchida, K. (2002) Involvement of the mitochondrial death pathway in chemopreventive benzyl isothiocyanate-induced apoptosis J. Biol. Chem. 277, 8492-8499 (Pubitemid 34968311)
45. Tang, L. and Zhang, Y. (2005) Mitochondria are the primary target in isothiocyanate-induced apoptosis in human bladder cancer cells Mol. Cancer Ther. 4, 1250-1259 (Pubitemid 41149573)
46. Galkin, A. and Moncada, S. (2007) S-nitrosation of mitochondrial complex I depends on its structural conformation J. Biol. Chem. 282, 37448-37453
47. Xiao, D., Powolny, A. A., Moura, M. B., Kelley, E. E., Bommareddy, A., Kim, S. H., Hahm, E. R., Normolle, D., Van Houten, B., and Singh, S. V. (2010) Phenethyl isothiocyanate inhibits oxidative phosphorylation to trigger reactive oxygen species-mediated death of human prostate cancer cells J. Biol. Chem. 285, 26558-26569
48. Tzivion, G., Luo, Z. J., and Avruch, J. (2000) Calyculin A-induced vimentin phosphorylation sequesters 14-3-3 and displaces other 14-3-3 partners in vivo J. Biol. Chem. 275, 29772-29778 (Pubitemid 32043861)
49. Tzivion, G., Gupta, V. S., Kaplun, L., and Balan, V. (2006) 14-3-3 proteins as potential oncogenes Semin. Cancer Biol. 16, 203-213 (Pubitemid 43810260)
50. Greco, T. M., Hodara, R., Parastatidis, I., Heijnen, H. F., Dennehy, M. K., and Liebler, D. C. (2006) Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells Proc. Natl. Acad. Sci. U.S.A. 103, 7420-7425 (Pubitemid 43727848)
51. Cross, J. V., Rady, J. M., Foss, F. W., Lyons, C. E., Macdonald, T. L., and Templeton, D. J. (2009) Nutrient isothiocyanates covalently modify and inhibit the inflammatory cytokine macrophage migration inhibitory factor (MIF) Biochem. J. 423, 315-321
52. Brown, K. K., Blaikie, F. H., Smith, R. A., Tyndall, J. D., Lue, H., Bernhagen, J., Winterbourn, C. C., and Hampton, M. B. (2009) Direct modification of the proinflammatory cytokine macrophage migration inhibitory factor by dietary isothiocyanates J. Biol. Chem. 284, 32425-32433