Allyl isothiocyanate as a cancer chemopreventive phytochemical

Molecular Nutrition and Food Research

Volumn 54, Issue 1, 2010, Pages 127-135

  Zhang, Yuesheng ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Allyl isothiocyanate; Chemoprevention; Cruciferous vegetable; Sinigrin

Indexed keywords

ALLYL ISOTHIOCYANATE; ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT; ISOTHIOCYANIC ACID DERIVATIVE; PROTECTIVE AGENT;

ANIMAL; BIOAVAILABILITY; DRUG EFFECT; FEMALE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; MALE; METABOLISM; PENICILLIUM CHRYSOGENUM; PHYTOTHERAPY; REVIEW;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTICARCINOGENIC AGENTS; BIOLOGICAL AVAILABILITY; FEMALE; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; ISOTHIOCYANATES; MALE; PENICILLIUM CHRYSOGENUM; PHYTOTHERAPY; PROTECTIVE AGENTS;

ANIMALIA; RATTUS;

EID: 74349084800     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200900323     Document Type: Review

References (79)

1. Kushad, M. M., Brown, A. F., Kurilich, A. C., Juvik, J. A. et al., Variation of glucosinolates in vegetable crops of Brassica oleracea. J. Agric. Food Chem. 1999, 47, 1541-1548.
2. Fahey, J. W., Zalcmann, A. T., Talalay, P., The chemical diversity and distribution of glucosinolates and isothiocya- nates among plants. Phytochemistry 2001, 56, 5-51.
3. IARC Hand books of Cancer Prevention, Cruciferous Vege- tables, Isothiocyanates and Indoles, 9 IARC Press, Lyon 2004.
4. Zhang, Y., Tang, L., Discovery and development of sulfor- aphane as a cancer chemopreventive phytochemical. Acta Pharmacol. Sin. 2007, 28, 1343-1354.
5. 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.
6. Getahun, S. M., Chung, F. L., Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. Cancer Epidemiol. Biomarkers Prev. 1999, 8, 447-451.
7. Kensler, T. W., Chen, J. G., Egner, P. A., Fahey, J. W. et al., Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China. Cancer Epidemiol. Biomarkers Prev. 2005, 14, 2605-2613.
8. Rungapamestry, V., Duncan, A. J., Fuller, Z., Ratcliffe, B., Changes in glucosinolate concentrations, myrosinase activity, and production of metabolites of glucosinolates in cabbage (Brassica oleracea Var. capitata) cooked for different durations. J. Agric. Food Chem. 2006, 54, 7628-7634.
9. Uematsu, Y., Hirata, K., Suzuki, K., Iida, K. et al., Determi- nation of isothiocyanates and related compounds in mustard extract and horseradish extract used as natural food additives. Shokuhin Eiseigaku Zasshi 2002, 43, 10-17.
10. Sultana, T., Savage, G. P., McNeil, D. L., Porter, N. G. et al., Effects of fertilisation on the allyl isothiocyanate profile of above-ground tissue of New Zealand-grown wasabi. J. Sci. Food Agric. 2002, 82, 1477-1482.
11. Krul, C., Humblot, C., Philippe, C., Vermeulen, M. et al., Metabolism of sinigrin (2-propenyl glucosinolate) by the human colonic microflora in a dynamic in vitro large- intestinal model. Carcinogenesis 2002, 23, 1009-1016.
12. Elfoul, L., Rabot, S., Khelifa, N., Quinsac, A. et al., Formation of allyl isothiocyanate from sinigrin in the digestive tract of rats monoassociated with a human colonic strain of Bacteroides thetaiotaomicron. FEMS Microbiol. Lett. 2001, 197,99-103.
13. Kelleher, M. O., McMahon, M., Eggleston, I. M., Dixon, M. J. et al., 1-Cyano-2,3-epithiopropane is a novel plant-derived chemopreventive agent which induces cytoprotective genes that afford resistance against the genotoxic, a, b-unsaturated aldehyde acrolein. Carcinogenesis 2009, 30,1754-1762.
14. Eid, S. R., Crown, E. D., Moore, E. L., Liang, H. A. et al., HC- 030031, a TRPA1 selective antagonist, attenuates inflam- matory- and neuropathy-induced mechanical hypersensi- tivity. Mol. Pain 2008, 4, 48.
15. Cavanaugh, E. J., Simkin, D., Kim, D., Activation of transient receptor potential A1 channels by mustard oil, tetra- hydrocannabinol and Ca21 reveals different functional channel states. Neuroscience 2008, 154, 1467-1476.
16. Ioannou, Y. M., Burka, L. T., Matthews, H. B., Allyl isothio- cyanate: comparative disposition in rats and mice. Toxicol. Appl. Pharmacol. 1984, 75, 173-181.
17. Bollard, M., Stribbling, S., Mitchell, S., Caldwell, J., The disposition of allyl isothiocyanate in the rat and mouse. Food Chem. Toxicol. 1997, 35, 933-943.
18. Munday, R., Zhang, Y., Fahey, J. W., Jobson, H. E. et al., Evaluation of isothiocyanates as potent inducers of carci- nogen-detoxifying enzymes in the urinary bladder: critical nature of in vivo bioassay. Nutr. Cancer 2006, 54, 223-231.
19. Jiao, D., Ho, C. T., Foiles, P., Chung, F. L., Identification and quantification of the N-acetylcysteine conjugate of allyl isothiocyanate in human urine after ingestion of mustard. Cancer Epidemiol. Biomarkers Prev. 1994, 3, 487-492.
20. Nakamura, T., Kawai, Y., Kitamoto, N., Osawa, T., Kato, Y., Covalent modification of lysine residues by allyl isothio- cyanate in physiological conditions: pausible transforma- tion of isothiocyanate from thiol to amine. Chem. Res. Toxicol. 2009, 22, 536-542.
21. Zhang, Y., Talalay, P., Mechanism of differential potencies of isothiocyanates as inducers of anticarcinogenic Phase 2 enzymes. Cancer Res. 1998, 58, 4632-4639.
22. Zhang, Y., Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 2000, 21,1175-1182.
23. Tang, L., Li, G., Song, L., Zhang, Y., The principal urinary metabolites of dietary isothiocyanates, N-acetylcysteine conjugates, elicit the same anti-proliferative response as their parent compounds in human bladder cancer cells. Anticancer Drugs 2006, 17, 297-305.
24. Zhang, Y., Molecular mechanism of rapid cellular accumu- lation of anticarcinogenic isothiocyanates. Carcinogenesis 2001,22,425-431.
25. Bruggeman, I. M., Temmink, J. H., van Bladeren, P. J., Glutathione- and cysteine-mediated cytotoxicity of allyl and benzyl isothiocyanate. Toxicol. Appl. Pharmacol. 1986, 83, 349-359.
26. Zhang, Y., Callaway, E. C., High cellular accumulation of sulphoraphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conju- gate. Biochem. J. 2002, 364, 301-307.
27. Callaway, E. C., Zhang, Y., Chew, W., Chow, H. H., Cellular accumulation of dietary anticarcinogenic isothiocyanates is followed by transporter-mediated export as dithiocarba- mates. Cancer Lett. 2004, 204, 23-31.
28. Ye, L., Zhang, Y., Total intracellular accumulation levels of dietary isothiocyanates determine their activity in elevation of cellular glutathione and induction of Phase 2 detoxifica- tion enzymes. Carcinogenesis 2001, 22, 1987-1992.
29. Munday, R., Mhawech-Fauceglia, P., Munday, C. M., Paonessa, J. D. et al., Inhibition of urinary bladder carcino- genesis by broccoli sprouts. Cancer Res. 2008, 68, 1593-1600.
30. Conaway, C. C., Krzeminski, J., Amin, S., Chung, F. L., Decomposition rates of isothiocyanate conjugates deter- mine their activity as inhibitors of cytochrome p450 enzymes. Chem. Res. Toxicol. 2001, 14, 1170-1176.
31. Shin, I. S., Masuda, H., Naohide, K., Bactericidal activity of wasabi (Wasabia japonica) against Helicobacter pylori. Int. J. Food Microbiol. 2004, 94, 255-261.
32. Luciano, F. B., Holley, R. A., Enzymatic inhibition by allyl isothiocyanate and factors affecting its antimicrobial action against Escherichia coli O157:H7. Int. J. Food Microbiol. 2009,131,240-245.
33. Tunc, S., Chollet, E., Chalier, P., Preziosi-Belloy, L., Gontard, N., Combined effect of volatile antimicrobial agents on the growth of Penicillium notatum. Int. J. Food Microbiol. 2007, 113, 263-270.
34. Nielsen, P. V., Rios, R., Inhibition of fungal growth on bread by volatile components from spices and herbs, and the possible application in active packaging, with special emphasis on mustard essential oil. Int. J. Food Microbiol. 2000,60,219-229.
35. Suhr, K. I., Nielsen, P. V., Antifungal activity of essential oils evaluated by two different application techniques against rye bread spoilage fungi. J. Appl. Microbiol. 2003, 94, 665-674.
36. Lin, C. M., Preston, J. F., 3rd, Wei, C. I., Antibacterial mechanism of allyl isothiocyanate. J. Food Prot. 2000, 63, 727-734.
37. Kassie, F., Knasmuller, S., Genotoxic effects of allyl isothiocyanate (AITC) and phenethyl isothiocyanate (PEITC). Chem. Biol. Interact. 2000, 127, 163-180.
38. Luciano, F. B., Hosseinian, F. S., Beta, T., Holley, R. A., Effect of free-SH containing compounds on allyl isothiocyanate antimicrobial activity against Escherichia coli O157:H7. J. Food Sci. 2008, 73, M214-M220.
39. Zhang, Y., Tang, L., Gonzalez, V., Selected isothiocyanates rapidly induce growth inhibition of cancer cells. Mol. Cancer Ther. 2003, 2, 1045-1052.
40. Xiao, D., Srivastava, S. K., Lew, K. L., Zeng, Y. et al., Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits proliferation of human prostate cancer cells by causing G2/M arrest and inducing apoptosis. Carcinogen- esis 2003, 24, 891-897.
41. Musk, S. R., Johnson, I. T., Allyl isothiocyanate is selectively toxic to transformed cells of the human colorectal tumour line HT29. Carcinogenesis 1993, 14, 2079-2083.
42. Tang, L., Zhang, Y., Dietary isothiocyanates inhibit the growth of human bladder carcinoma cells. J. Nutr. 2004, 134,2004-2010.
43. 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.
44. Hasegawa, T., Nishino, H., Iwashima, A., Isothiocyanates inhibit cell cycle progression of HeLa cells at G2/M phase. Anticancer Drugs 1993, 4, 273-279.
45. Smith, T. K., Lund, E. K., Parker, M. L., Clarke, R. G., John- son, I. T., Allyl-isothiocyanate causes mitotic block, loss of cell adhesion and disrupted cytoskeletal structure in HT29 cells. Carcinogenesis 2004, 25, 1409-1415.
46. 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.
47. Xu, C., Shen, G., Yuan, X., Kim, J. H. et al., ERK and JNK signaling pathways are involved in the regulation of acti- vator protein 1 and cell death elicited by three isothiocya- nates in human prostate cancer PC-3 cells. Carcinogenesis 2006,27,437-445.
48. Jeong, W. S., Kim, I. W., Hu, R., Kong, A. N., Modulation of AP-1 by natural chemopreventive compounds in human colon HT-29 cancer cell line. Pharm. Res. 2004, 21, 649-660.
49. Li, J., Yao, S., Zhang, Y., The role of c-Jun in the AP-1 activation induced by naturally occurring isothiocyanates. Food Chem. Toxicol. 2005, 43, 1373-1380.
50. Hwang, E. S., Lee, H. J., Allyl isothiocyanate and its N-acetylcysteine conjugate suppress metastasis via inhibi- tion of invasion, migration, and matrix metalloproteinase- 2/ 9 activities in SK-Hep 1 human hepatoma cells. Exp. Biol. Med. 2006, 231, 421-430.
51. Zucker, S., Vacirca, J., Role of matrix metalloproteinases (MMPs) in colorectal cancer. Cancer Metastasis Rev. 2004, 23,101-117.
52. Vincenti, M. P., The matrix metalloproteinase (MMP) and tissue inhibitor of metalloproteinase (TIMP) genes. Tran- scriptional and posttranscriptional regulation, signal trans- duction and cell-type-specific expression. Methods Mol. Biol. 2001, 151, 121-148.
53. Mahlknecht, U., Hoelzer, D., Histone acetylation modifiers in the pathogenesis of malignant disease. Mol. Med. 2000, 6, 623-644.
54. Marks, P. A., Richon, V. M., Rifkind, R. A., Histone deace- tylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst. 2000, 92, 1210-1216.
55. Lea, M. A., Randolph, V. M., Lee, J. E., desBordes, C., Induction of histone acetylation in mouse erythroleukemia cells by some organosulfur compounds including allyl isothiocyanate. Int. J. Cancer 2001, 92, 784-789.
56. Myzak, M. C., Hardin, K., Wang, R., Dashwood, R. H., Ho, E., Sulforaphane inhibits histone deacetylase activity in BPH-1, LnCaP and PC-3 prostate epithelial cells. Carcinogenesis 2006,27,811-819.
57. Ippoushi, K., Itou, H., Azuma, K., Higashio, H., Effect of naturally occurring organosulfur compounds on nitric oxide production in lipopolysaccharide-activated macrophages. Life Sci. 2002, 71, 411-419.
58. Jeong, W. S., Kim, I. W., Hu, R., Kong, A. N., Modulatory properties of various natural chemopreventive agents on the activation of NF-kB signaling pathway. Pharm. Res. 2004,21,661-670.
59. Srivastava, S. K., Xiao, D., Lew, K. L., Hershberger, P. et al., Allyl isothiocyanate, a constituent of cruciferous vege- tables, inhibits growth of PC-3 human prostate cancer xenografts in vivo. Carcinogenesis 2003, 24, 1665-1670.
60. Smith, T., Musk, S. R. R., Johnson, I. T., Allyl isothiocyanate seletively kills undifferentiated HT29 cells in vitro and suppresses aberrant crypt foci in the colonic mucosa of rats. Biochem. Soc. Trans. 1996, 24, 381S.
61. Tanaka, T., Mori, Y., Morishita, Y., Hara, A. et al., Inhibitory effect of sinigrin and indole-3-carbinol on diethylni- trosamine-induced hepatocarcinogenesis in male ACI/N rats. Carcinogenesis 1990, 11, 1403-1406.
62. Jiao, D., Eklind, K. I., Choi, C. I., Desai, D. H. et al., Structure- activity relationships of isothiocyanates as mechanism- based inhibitors of 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanone-induced lung tumorigenesis in A/J mice. Cancer Res. 1994, 54, 4327-4333.
63. Jeong, W. S., Keum, Y. S., Chen, C., Jain, M. R. et al., Differential expression and stability of endogenous nuclear factor E2-related factor 2 (Nrf2) by natural chemopreventive compounds in HepG2 human hepatoma cells. J. Biochem. Mol. Biol. 2005, 38, 167-176.
64. Bogaards, J. J., van Ommen, B., Falke, H. E., Willems, M. I., van Bladeren, P. J., Glutathione S-transferase subunit induction patterns of Brussels sprouts, allyl isothiocyanate and goitrin in rat liver and small intestinal mucosa: a new approach for the identification of inducing xenobiotics. Food Chem. Toxicol. 1990, 28, 81-88.
65. McWalter, G. K., Higgins, L. G., McLellan, L. I., Henderson, C. J. et al., Transcription factor Nrf2 is essential for induc- tion of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J. Nutr. 2004, 134, 3499S-3506S.
66. Kwak, M. K., Wakabayashi, N., Itoh, K., Motohashi, H. et al., Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identifi- cation of novel gene clusters for cell survival. J. Biol. Chem. 2003,278,8135-8145.
67. Matsuda, H., Ochi, M., Nagatomo, A., Yoshikawa, M., Effects of allyl isothiocyanate from horseradish on several experimental gastric lesions in rats. Eur. J. Pharmacol. 2007,561,172-181.
68. Uhl, M., Laky, B., Lhoste, E., Kassie, F. et al., Effects of mustard sprouts and allylisothiocyanate on benzo(a)pyr- ene-induced DNA damage in human-derived cells: a model study with the single cell gel electrophoresis/Hep G2 assay. Teratog., Carcinog. Mutagen. 2003, 1, 273-282.
69. Murata, M., Yamashita, N., Inoue, S., Kawanishi, S., Mechanism of oxidative DNA damage induced by carcino- genic allyl isothiocyanate. Free Radic. Biol. Med. 2000, 28, 797-805.
70. Yonezawa, Y., Nishikawa, K., Nishioka, H., DNA damage and intracellular generation of reactive oxygen species by allyl isothiocyanate in Escherichia coli. J. Environ. Med. 1999,1,27-31.
71. Schiffmann, D., Eder, E., Neudecker, T., Henschler, D., Induction of unscheduled DNA synthesis in HeLa cells by allylic compounds. Cancer Lett. 1983, 20, 263-269.
72. Musk, S. R., Johnson, I. T., The clastogenic effects of isothiocyanates. Mutat. Res. 1993, 300, 111-117.
73. Musk, S. R., Smith, T. K., Johnson, I. T., On the cytotoxicity and genotoxicity of allyl and phenethyl isothiocyanates and their parent glucosinolates sinigrin and gluconasturtiin. Mutat. Res. 1995, 348, 19-23.
74. Bechtel, D., Henderson, L., Proudlock, R., Lack of UDS activity in the livers of rats exposed to allylisothiocyanate. Teratog., Carcinog. Mutagen. 1998, 18, 209-217.
75. Langer, P., Stolc, V., Goitrogenic activity of allylisothiocya- nate--a widespread natural mustard oil. Endocrinology 1965,76,151-155.
76. Lewerenz, H. J., Plass, R., Bleyl, D. W., Macholz, R., Short- term toxicity study of allyl isothiocyanate in rats. Nahrung 1988,32,723-728.
77. NTP Technical Report of the Carcinogenesis Bioassay of Allye Isothiocyanate (CAS No 57-06-07), NTP-81-36, NIH publication No. 83-1790, National Toxicology Program Technical Report Series, Washington D.C. 1982.
78. NAS/NRC, National Academy of Sciences and the National Research Council, Washington, D.C. 1982.
79. Masutomi, N., Toyoda, K., Shibutani, M., Niho, N. et al., Toxic effects of benzyl and allyl isothiocyanates and benzyl- isoform specific metabolites in the urinary bladder after a single intravesical application to rats. Toxicol. Pathol. 2001, 29,617-622.