Phenethyl isothiocyanate-induced cytoskeletal changes and cell death in lung cancer cells

Food and Chemical Toxicology

Volumn 50, Issue 10, 2012, Pages 3577-3594

  Pawlik, Andrzej ^a   Szczepanski, Mariusz Andrzej ^a   Klimaszewska, Anna ^a   Gackowska, Lidia ^a   Zuryn, Agnieszka ^a   Grzanka, Alina ^a  

^a NICOLAUS COPERNICUS UNIVERSITY   (Poland)

Author keywords

Apoptosis; Cell death; Cytoskeleton; Lung cancer; Phenethyl isothiocyanate; Tubulin

Indexed keywords

ALPHA TUBULIN; DNA; F ACTIN; LIPOCORTIN 5; PHENETHYL ISOTHIOCYANATE; PROTEIN P53;

ACTIN FILAMENT; ANALYTICAL EQUIPMENT; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE G1 PHASE; CELL DEATH; CELL SPECIFICITY; CELL STRAIN A549; CELL STRAIN H1299; CELL STRUCTURE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; DNA CONTENT; DRUG CYTOTOXICITY; DRUG POTENCY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; G2 PHASE CELL CYCLE CHECKPOINT; GROWTH INHIBITION; HUMAN; HUMAN CELL; INCUBATION TIME; LUNG NON SMALL CELL CANCER; MITOSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRESS FIBER; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE;

ACTINS; ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; CYTOSKELETON; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; ISOTHIOCYANATES; LUNG NEOPLASMS; TIME FACTORS; TUBULIN;

EID: 84865483549     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.07.043     Document Type: Article

References (82)

1. Adam-Rodwell G., Morse M.A., Stoner G.D. The effects of phenethyl isothiocyanate on benzo[a]pyrene-induced tumors and DNA adducts in A/J mouse lung. Cancer Lett. 1993, 71:35-42.
2. Agudo A., Esteve M.G., Pallarés C., Martínez-Ballarín I., Fabregat X., Malats N., Machengs I., Badia A., González C.A. Vegetable and fruit intake and the risk of lung cancer in women in Barcelona, Spain. Eur. J. Cancer 1997, 33:1256-1261.
3. Balansky R., Ganchev G., Iltcheva M., Steele V.E., De Flora S. Prevention of cigarette smoke-induced lung tumors in mice by budesonide, phenethyl isothiocyanate, and N-acetylcysteine. Int. J. Cancer 2010, 126:1047-1054.
4. Bogaards J.J., Verhagen H., Willems M.I., van Poppel G., van Bladeren P.J. Consumption of Brussels sprouts results in elevated alpha-class glutathione S-transferase levels in human blood plasma. Carcinogenesis 1994, 15:1073-1075.
5. Bond G.G., Thompson F.E., Cook R.R. Dietary vitamin A and lung cancer: results of a case-control study among chemical workers. Nutr. Cancer 1987, 9:109-121.
6. Caelles C., Helmberg A., Karin M. P53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 1994, 370:220-223.
7. Carpenter C.L., Yu M.C., London S.J. Dietary isothiocyanates, glutathione S-transferase M1 (GSTM1), and lung cancer risk in African Americans and Caucasians from Los Angeles County, California. Nutr. Cancer 2009, 61:492-499.
8. Castedo M., Perfettini J.L., Roumier T., Andreau K., Medema R., Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 2004, 23:2825-2837.
9. Chow W.H., Schuman L.M., McLaughlin J.K., Bjelke E., Gridley G., Wacholder S., Chien H.T., Blot W.J. A cohort study of tobacco use, diet, occupation, and lung cancer mortality. Cancer Causes Control 1992, 3:247-254.
10. Chung F.L., Jiao D., Getahun S.M., Yu M.C. A urinary biomarker for uptake of dietary isothiocyanates in humans. Cancer Epidemiol. Biomarkers Prev. 1998, 7:103-108.
11. Chung F.L., Kelloff G., Steele V., Pittman B., Zang E., Jiao D., Rigotty J., Choi C.I., Rivenson A. Chemopreventive efficacy of arylalkyl isothiocyanates and N-acetylcysteine for lung tumorigenesis in Fischer rats. Cancer Res. 1996, 56:772-778.
12. Conaway C.C., Krzeminski J., Amin S., Chung F.L. Decomposition rates of isothiocyanate conjugates determine their activity as inhibitors of cytochrome p450 enzymes. Chem. Res. Toxicol. 2001, 14:1170-1176.
13. Croce M.V., Colussi A.G., Price M.R., Segal-Eiras A. Identification and characterization of different subpopulations in a human lung adenocarcinoma cell line (A549). Pathol. Oncol. Res. 1999, 5:197-204.
14. Edelman M.J., Quam H., Mullins B. Interactions of gemcitabine, carboplatin and paclitaxel in molecularly defined non-small-cell lung cancer cell lines. Cancer Chemother. Pharmacol. 2001, 48:141-144.
15. Eklind K.I., Morse M.A., Chung F.L. Distribution and metabolism of the natural anticarcinogen phenethyl isothiocyanate in A/J mice. Carcinogenesis 1990, 11:2033-2036.
16. Fei P., El-Deiry W.S. P53 and radiation responses. Oncogene 2003, 22:5774-5783.
17. Feskanich D., Ziegler R.G., Michaud D.S., Giovannucci E.L., Speizer F.E., Willett W.C., Colditz G.A. Prospective study of fruit and vegetable consumption and risk of lung cancer among men and women. J. Natl. Cancer Inst. 2000, 92:1812-1823.
18. Fimognari C., Nüsse M., Berti F., Iori R., Cantelli-Forti G., Hrelia P. Cyclin D3 and p53 mediate sulforaphane-induced cell cycle delay and apoptosis in non-transformed human T lymphocytes. Cell Mol. Life Sci. 2002, 59:2004-2012.
19. Foster K.A., Oster C.G., Mayer M.M., Avery M.L., Audus K.L. Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism. Exp. Cell Res. 1998, 243:359-366.
20. Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., Gottlieb E., Green D.R., Hengartner M.O., Kepp O., Knight R.A., Kumar S., Lipton S.A., Lu X., Madeo F., Malorni W., Mehlen P., Nuñez G., Peter M.E., Piacentini M., Rubinsztein D.C., Shi Y., Simon H.U., Vandenabeele P., White E., Yuan J., Zhivotovsky B., Melino G., Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012, 19:107-120.
21. Giard D.J., Aaronson S.A., Todaro G.J., Arnstein P., Kersey J.H., Dosik H., Parks W.P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J. Natl. Cancer Inst. 1973, 51:1417-1423.
22. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
23. Grzanka D., Stepien A., Grzanka A., Gackowska L., Helmin-Basa A., Szczepanski M.A. Hyperthermia-induced reorganization of microtubules and microfilaments and cell killing in CHO AA8 cell line. Neoplasma 2008, 55:409-415.
24. Hecht S.S., Carmella S.G., Kenney P.M., Low S.H., Arakawa K., Yu M.C. Effects of cruciferous vegetable consumption on urinary metabolites of the tobacco-specific lung carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in Singapore chinese. Cancer Epidemiol. Biomarkers Prev. 2004, 13:997-1004.
25. Hecht S.S., Carmella S.G., Murphy S.E. Effects of watercress consumption on urinary metabolites of nicotine in smokers. Cancer Epidemiol. Biomarkers Prev. 1999, 8:907-913.
26. Hecht S.S., Kenney P.M., Wang M., Trushin N., Upadhyaya P. Effects of phenethyl isothiocyanate and benzyl isothiocyanate, individually and in combination, on lung tumorigenesis induced in A/J mice by benzo[a]pyrene and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Cancer Lett. 2000, 150:49-56.
27. Hecht S.S., Trushin N., Rigotty J., Carmella S.G., Borukhova A., Akerkar S., Rivenson A. Complete inhibition of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced rat lung tumorigenesis and favorable modification of biomarkers by phenethyl isothiocyanate. Cancer Epidemiol. Biomarkers Prev. 1996, 5:645-652.
28. Hoffman P.C., Mauer A.M., Vokes E.E. Lung cancer. Lancet 2000, 355:479-485.
29. Hu J., Mao Y., Dryer D., White K. Risk factors for lung cancer among Canadian women who have never smoked. Cancer Detect. Prev. 2002, 26:129-138. Canadian Cancer Registries Epidemiology Research Group.
30. Hu R., Kim B.R., Chen C., Hebbar V., Kong A.N. The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 2003, 24:1361-1367.
31. Huang C., Ma W.Y., Li J., Hecht S.S., Dong Z. Essential role of p53 in phenethyl isothiocyanate-induced apoptosis. Cancer Res. 1998, 58:4102-4106.
32. International Agency for Research on Cancer, 2004. Cruciferous Vegetables, Isothiocyanates and Indoles. IARC Handbooks of Cancer, Prevention, vol. 9.
33. Ji Y., Morris M.E. Determination of phenethyl isothiocyanate in human plasma and urine by ammonia derivatization and liquid chromatography-tandem mass spectrometry. Anal. Biochem. 2003, 323:39-47.
34. Ji Y., Morris M.E. Transport of dietary phenethyl isothiocyanate is mediated by multidrug resistance protein 2 but not P-glycoprotein. Biochem. Pharmacol. 2005, 70:640-647.
35. INK4a gene expression radiosensitizes non-small cell lung cancer cells in a p53-dependent manner. Oncogene 2000, 19:5359-5366.
36. Kawakami M., Harada N., Hiratsuka M., Kawai K., Nakamura Y. Dietary isothiocyanates modify mitochondrial functions through their electrophilic reaction. Biosci. Biotechnol. Biochem. 2005, 69:2439-2444.
37. Kuang Y.F., Chen Y.H. Induction of apoptosis in a non-small cell human lung cancer cell line by isothiocyanates is associated with P53 and P21. Food Chem. Toxicol. 2004, 42:1711-1718.
38. Kulms D., Düssmann H., Pöppelmann B., Ständer S., Schwarz A., Schwarz T. Apoptosis induced by disruption of the actin cytoskeleton is mediated via activation of CD95 (Fas/APO-1). Cell Death Differ. 2002, 9:598-608.
39. Le Marchand L., Yoshizawa C.N., Kolonel L.N., Hankin J.H., Goodman M.T. Vegetable consumption and lung cancer risk: a population-based case-control study in Hawaii. J. Natl. Cancer Inst. 1989, 81:1158-1164.
40. Liang H., Lai B., Yuan Q. Sulforaphane induces cell-cycle arrest and apoptosis in cultured human lung adenocarcinoma LTEP-A2 cells and retards growth of LTEP-A2 xenografts in vivo. J. Nat. Prod. 2008, 71:1911-1914.
41. Lieber M., Smith B., Szakal A., Nelson-Rees W., Todaro G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int. J. Cancer 1976, 17:62-70.
42. Liebes L., Conaway C.C., Hochster H., Mendoza S., Hecht S.S., Crowell J., Chung F.L. High-performance liquid chromatography-based determination of total isothiocyanate levels in human plasma: application to studies with 2-phenethyl isothiocyanate. Anal. Biochem. 2001, 291:279-289.
43. Lin H.P., Kuo L.K., Chuu C.P. Combined treatment of curcumin and small molecule inhibitors suppresses proliferation of A549 and H1299 human non-small-cell lung cancer cells. Phytother. Res. 2012, 26:122-126.
44. Lindström M.S., Wiman K.G. Myc and E2F1 induce p53 through p14ARF-independent mechanisms in human fibroblasts. Oncogene 2003, 22:4993-5005.
45. London S.J., Yuan J.M., Chung F.L., Gao Y.T., Coetzee G.A., Ross R.K., Yu M.C. Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: a prospective study of men in Shanghai, China. Lancet 2000, 356:724-729.
46. Mi L., Gan N., Cheema A., Dakshanamurthy S., Wang X., Yang D.C., Chung F.L. Cancer preventive isothiocyanates induce selective degradation of cellular alpha- and beta-tubulins by proteasomes. J. Biol. Chem. 2009, 284:17039-17051.
47. Mi L., Hood B.L., Stewart N.A., Xiao Z., Govind S., Wang X., Conrads T.P., Veenstra T.D., Chung F.L. Identification of potential protein targets of isothiocyanates by proteomics. Chem. Res. Toxicol. 2011, 24:1735-1743.
48. Mi L., Wang X., Govind S., Hood B.L., Veenstra T.D., Conrads T.P., Saha D.T., Goldman R., Chung F.L. The role of protein binding in induction of apoptosis by phenethyl isothiocyanate and sulforaphane in human non-small lung cancer cells. Cancer Res. 2007, 67:6409-6416.
49. Mi L., Xiao Z., Hood B.L., Dakshanamurthy S., Wang X., Govind S., Conrads T.P., Veenstra T.D., Chung F.L. Covalent binding to tubulin by isothiocyanates. A mechanism of cell growth arrest and apoptosis. J. Biol. Chem. 2008, 283:22136-22146.
50. Mithen R., Faulkner K., Magrath R., Rose P., Williamson G., Marquez J. Development of isothiocyanate-enriched broccoli, and its enhanced ability to induce phase 2 detoxification enzymes in mammalian cells. Theor. Appl. Genet. 2003, 106:727-734.
51. Miyoshi N., Uchida K., Osawa T., Nakamura Y. A link between benzyl isothiocyanate-induced cell cycle arrest and apoptosis: involvement of mitogen-activated protein kinases in the Bcl-2 phosphorylation. Cancer Res. 2004, 64:2134-2142.
52. Miyoshi N., Uchida K., Osawa T., Nakamura Y. Benzyl isothiocyanate modifies expression of the G2/M arrest-related genes. BioFactors 2004, 21:23-26.
53. Miyoshi N., Uchida K., Osawa T., Nakamura Y. Selective cytotoxicity of benzyl isothiocyanate in the proliferating fibroblastoid cells. Int. J. Cancer 2007, 120:484-492.
54. Miyoshi N., Watanabe E., Osawa T., Okuhira M., Murata Y., Ohshima H., Nakamura Y. ATP depletion alters the mode of cell death induced by benzyl isothiocyanate. Biochim. Biophys. Acta 2008, 1782:566-573.
55. Mummenbrauer T., Janus F., Müller B., Wiesmüller L., Deppert W., Grosse F. P53 protein exhibits 3'-to-5' exonuclease activity. Cell 1996, 85:1089-1099.
56. Nakamura Y., Kawakami M., Yoshihiro A., Miyoshi N., Ohigashi H., Kawai K., Osawa T., Uchida K. Involvement of the mitochondrial death pathway in chemopreventive benzyl isothiocyanate-induced apoptosis. J. Biol. Chem. 2002, 277:8492-8499.
57. Nishikawa A., Furukawa F., Uneyama C., Ikezaki S., Tanakamaru Z., Chung F.L., Takahashi M., Hayashi Y. Chemopreventive effects of phenethyl isothiocyanate on lung and pancreatic tumorigenesis in N-nitrosobis(2-oxopropyl)amine-treated hamsters. Carcinogenesis 1996, 17:1381-1384.
58. Okamoto A., Hussain S.P., Hagiwara K., Spillare E.A., Rusin M.R., Demetrick D.J., Serrano M., Hannon G.J., Shiseki C.C., Zariwala M., Xiong Y., Beach D.H., Yokota J., Harris C.C. Mutations in the p16INK4/MTS1/CDKN2, p15INK4B/MTS2, and p18 genes in primary and metastatic lung cancer. Cancer Res. 1995, 55:1448-1451.
59. Pollard T.D. The cytoskeleton, cellular motility and the reductionist agenda. Nature 2003, 422:741-745.
60. Powolny A., Takahashi K., Hopkins R.G., Loo G. Induction of GADD gene expression by phenethylisothiocyanate in human colon adenocarcinoma cells. J. Cell. Biochem. 2003, 90:1128-1139.
61. Rello-Varona S., Kepp O., Vitale I., Michaud M., Senovilla L., Jemaà M., Joza N., Galluzzi L., Castedo M., Kroemer G. An automated fluorescence videomicroscopy assay for the detection of mitotic catastrophe. Cell Death Dis. 2010, 1:e25.
62. Rose P., Faulkner K., Williamson G., Mithen R. 7-Methylsulfinylheptyl and 8-methylsulfinyloctyl isothiocyanates from watercress are potent inducers of phase II enzymes. Carcinogenesis 2000, 21:1983-1988.
63. Safiejko-Mroczka B., Bell P.B. Distribution of cytoskeletal proteins in neomycin-induced protrusions of human fibroblasts. Exp. Cell Res. 1998, 242:495-514.
64. Satyan K.S., Swamy N., Dizon D.S., Singh R., Granai C.O., Brard L. Phenethyl isothiocyanate (PEITC) inhibits growth of ovarian cancer cells by inducing apoptosis: role of caspase and MAPK activation. Gynecol. Oncol. 2006, 103:261-270.
65. Shapiro T.A., Fahey J.W., Wade K.L., Stephenson K.K., Talalay P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol. Biomarkers Prev. 1998, 7:1091-1100.
66. Spitz M.R., Duphorne C.M., Detry M.A., Pillow P.C., Amos C.I., Lei L., de Andrade M., Gu X., Hong W.K., Wu X. Dietary intake of isothiocyanates: evidence of a joint effect with glutathione S-transferase polymorphisms in lung cancer risk. Cancer Epidemiol. Biomarkers Prev. 2000, 9:1017-1020.
67. Stoner G.D., Morse M.A. Isothiocyanates and plant polyphenols as inhibitors of lung and esophageal cancer. Cancer Lett. 1997, 114:113-119.
68. Trachootham D., Zhang H., Zhang W., Feng L., Du M., Zhou Y., Chen Z., Pelicano H., Plunkett W., Wierda W.G., Keating M.J., Huang P. Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 2008, 112:1912-1922.
69. Trachootham D., Zhou Y., Zhang H., Demizu Y., Chen Z., Pelicano H., Chiao P.J., Achanta G., Arlinghaus R.B., Liu J., Huang P. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell. 2006, 10:241-252.
70. Voorrips L.E., Goldbohm R.A., Verhoeven D.T., van Poppel G.A., Sturmans F., Hermus R.J., van den Brandt P.A. Vegetable and fruit consumption and lung cancer risk in the Netherlands Cohort Study on diet and cancer. Cancer Causes Control 2000, 11:101-115.
71. Wu X., Kassie F., Mersch-Sundermann V. Induction of apoptosis in tumor cells by naturally occurring sulfur-containing compounds. Mutat. Res. 2005, 589:81-102.
72. Wu X., Zhou Q., Xu K. Are isothiocyanates potential anti-cancer drugs?. Acta Pharmacol. Sin. 2009, 30:501-512.
73. Xiao D., Singh S.V. Phenethyl isothiocyanate-induced apoptosis in p53-deficient PC-3 human prostate cancer cell line is mediated by extracellular signal-regulated kinases. Cancer Res. 2002, 62:3615-3619.
74. Xu K., Thornalley P.J. Studies on the mechanism of the inhibition of human leukaemia cell growth by dietary isothiocyanates and their cysteine adducts in vitro. Biochem. Pharmacol. 2000, 60:221-231.
75. Xu K., Thornalley P.J. Involvement of glutathione metabolism in the cytotoxicity of the phenethyl isothiocyanate and its cysteine conjugate to human leukaemia cells in vitro. Biochem. Pharmacol. 2001, 61:165-177.
76. Xu K., Thornalley P.J. Signal transduction activated by the cancer chemopreventive isothiocyanates: cleavage of BID protein, tyrosine phosphorylation and activation of JNK. Br. J. Cancer 2001, 84:670-673.
77. Yin P., Kawamura T., He M., Vanaja D.K., Young C.Y. Phenethyl isothiocyanate induces cell cycle arrest and reduction of α- and β-tubulin isotypes in human prostate cancer cells. Cell Biol. Int. 2009, 33:57-64.
78. Yu R., Mandlekar S., Harvey K.J., Ucker D.S., Kong A.N. Chemopreventive isothiocyanates induce apoptosis and caspase-3-like protease activity. Cancer Res. 1998, 58:402-408.
79. Zhang Y. Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000, 21:1175-1182.
80. Zhang Y. Molecular mechanism of rapid cellular accumulation of anticarcinogenic isothiocyanates. Carcinogenesis 2001, 22:425-431.
81. Zhang Y., Callaway E.C. High cellular accumulation of sulphoraphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conjugate. Biochem. J. 2002, 364:301-307.
82. Zhang Y., Tang L., Gonzalez V. Selected isothiocyanates rapidly induce growth inhibition of cancer cells. Mol. Cancer Ther. 2003, 2:1045-1052.