Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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Mitochondria-mediated Apoptosis in Human Lung Cancer A549 Cells by 4-Methylsulfinyl-3-butenyl Isothiocyanate from Radish Seeds

  • Wang, Nan (College of Biology and Environmental Engineering, Zhejiang Shuren University) ;
  • Wang, Wei (Institute of Quality and Standard for Agriculture Products, Zhejiang Academy of Agricultural Science) ;
  • Huo, Po (College of Biology and Environmental Engineering, Zhejiang Shuren University) ;
  • Liu, Cai-Qin (College of Biology and Environmental Engineering, Zhejiang Shuren University) ;
  • Jin, Jian-Chang (College of Biology and Environmental Engineering, Zhejiang Shuren University) ;
  • Shen, Lian-Qing (College of Food Science and Biotechnology Engineering, Zhejiang Gongshang University)
  • Published : 2014.03.01
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Abstract

4-Methylsulfinyl-3-butenyl isothiocyanate (MTBITC) found in the radish (Raphanus sativus L.), is a wellknown anticancer agent. In this study, the mechanisms of the MTBITC induction of cell apoptosis in human A549 lung cancer cells were investigated. Our PI staining results showed that MTBITC treatment significantly increased the apoptotic sub-G1 fraction in a dose-dependent manner. The mechanism of apoptosis induced by MTBITC was investigated by testing the change of mitochondrial membrane potential (${\Delta}{\Psi}m$), the expression of mRNAs of apoptosis-related genes by RT-PCR, and the activities of caspase-3 and -9 by caspase colorimetric assay. MTBITC treatment decreased mitochondrial membrane potential by down-regulating the rate of Bcl-2/Bax and Bcl-xL/Bax, and activation of caspase-3 and -9. Therefore, mitochondrial pathway and Bcl-2 gene family could be involved in the mechanisms of A549 cell apoptosis induced by MTBITC.

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References

  1. Abdull Razis AF, Noor NM (2013). Cruciferous vegetables: dietary phytochemicals for cancer prevention. Asian Pacific J Cancer Prev, 14, 1565-70. https://doi.org/10.7314/APJCP.2013.14.3.1565
  2. Abdull Razis AF, Noor NM (2013). Sulforaphane is superior to glucoraphanin in modulating carcinogen-metabolising enzymes in Hep G2 Cells. Asian Pac J Cancer Prev, 14, 4235-8. https://doi.org/10.7314/APJCP.2013.14.7.4235
  3. Antonsson B, Montessuit S, Sanchez B, et al (2001). Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem, 276, 11615-23. https://doi.org/10.1074/jbc.M010810200
  4. Ashkenazi A, Dixit VM (1998). Death receptors: signaling and modulation. Science, 281, 1305-8. https://doi.org/10.1126/science.281.5381.1305
  5. Basanez G, Sharpe JC, Galanis J, et al (2002). Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem, 277, 49360-5. https://doi.org/10.1074/jbc.M206069200
  6. Brinker AM, Gayland FS (1993). Herbicidal activity of sulforaphene from stock (Matthiola incana). J Chem Ecol, 19, 2279-84. https://doi.org/10.1007/BF00979663
  7. Chen CY, Hsu YL, Tsai YC, et al (2008). Kotomolide A arrests cell cycle progression and induces apoptosis through the induction of ATM/p53 and the initiation of mitochondrial system in human non-small cell lung cancer A549 cells. Food Chem Toxicol, 46, 2476-84. https://doi.org/10.1016/j.fct.2008.04.016
  8. Chen CY, Liu TZ, Liu YW, et al (2007). 6-Shogaol (alkanone from Ginger) induces apoptotic cell death of human hepatoma p53 mutant Mahlavu subline via an oxidative stress-mediated caspase-dependent mechanism. J Agri Food Chem, 55, 948-54. https://doi.org/10.1021/jf0624594
  9. Chiao JW. Chung FL, Kancherla R, et al (2002). Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells. Int J Oncol, 20, 631-6.
  10. Conaway CC, Yang YM, Chung FL (2002). Isothiocyanates as cancer chemopreventive agents: their biological activities and metabolism in rodents and humans. Curr Drug Metab, 3, 233-255. https://doi.org/10.2174/1389200023337496
  11. Devi JR, Thangam EB (2012). Mechanisms of anticancer activity of sulforaphane from Brassica oleracea in HEP-2 human epithelial carcinoma cell line. Asian Pacific J Cancer Prev, 13, 2095-2100. https://doi.org/10.7314/APJCP.2012.13.5.2095
  12. Dewson G, Kluck RM (2010). Bcl-2 family-regulated apoptosis in health and disease. Cell Health and Cytoskeleton, 2, 9-22.
  13. Dias N, Bailly C (2005). Drugs targeting mitochondrial functions to control tumor cell growth. Biochem Pharmacol, 70 (1):1-12. https://doi.org/10.1016/j.bcp.2005.03.021
  14. Eskes R, Antonsson B, Osen-Sand A, et al (1998). Bax-induced cytochrome c release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2+ ions. J Cell Biol, 143, 217-24. https://doi.org/10.1083/jcb.143.1.217
  15. Fisher DE (1994). Apoptosis in cancer therapy: crossing the threshold. Cell, 78, 539-42. https://doi.org/10.1016/0092-8674(94)90518-5
  16. Fisher M, Golden NH, Katzman DK, et al. (1995). Eating disorders in adolescents: a background paper. J Adolesc Health, 16, 420-37. https://doi.org/10.1016/1054-139X(95)00069-5
  17. Frankfurt OS, Krishan A (2003). Apoptosis-based drug screening and detection of selective toxicity to cancer cells. Anticancer Drugs, 14, 555-61. https://doi.org/10.1097/00001813-200308000-00008
  18. Green DR, Reed JC (1998). Mitochondria and apoptosis. Science, 281, 1309-12. https://doi.org/10.1126/science.281.5381.1309
  19. Hanlon PR, Webber DM, Barnes DM (2007). Aqueous extract from Spanish black radish (Raphanus sativus L. Var. niger) induces detoxification enzymes in the HepG2 human hepatoma cell line. J Agric Food Chem, 55, 6439-46. https://doi.org/10.1021/jf070530f
  20. Hengartner MO (2000). The biochemistry of apoptosis. Nature, 407, 770-6. https://doi.org/10.1038/35037710
  21. Hecht SS (2000). Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev, 32, 395-411. https://doi.org/10.1081/DMR-100102342
  22. Hsu W, Lee B, Pan T (2010). Redmold dioscorea-induced G2/M arrest and apoptosis in human oral cancer cells. J Sci Food Agric, 90, 2709-15. https://doi.org/10.1002/jsfa.4144
  23. Ishii G, Saijo R, Mizutani J (1989). A quantitative of 4-methylthio-3-butenyl glucosinolate in Daikon (Raphanus sativus L.) roots by gas liquid chromatography. J Japan Soc Hort Sci, 58, 339-44. https://doi.org/10.2503/jjshs.58.339
  24. Karen-Ng LP, Marhazlinda J, Abdul Rahman ZA, et al (2011). Effects of isothiocyanate intake, glutathione s-transferase polymorphisms and risk habits for age of oral squamous cell carcinoma development, Asian Pacific J Cancer Prev, 12, 1161-6.
  25. Kluck RM, Bossy-Wetzel E, Green DR, et al (1997). The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science, 275, 1132-6. https://doi.org/10.1126/science.275.5303.1132
  26. Kore AM, Spencer GF, Wallig MA (1993). Purification of the $\omega$- (Methylsulfiny1)alkyl Glucosinolate Hydrolysis Products: 1-Isothiocyanato-3-(methylsulfinyl) propane, 1-Isothiocyanato-4-(methylsulfinyl) butane, 4- (Methylsulfinyl) butanenitrile, and 5- (Methylsulfinyl) pentanenitrile from Broccoli and Lesquerella fendleri. J Agric Food Chem, 41, 89-95. https://doi.org/10.1021/jf00025a019
  27. Korsmeyer SJ (1999). Bcl-2 gene family and the regulation of programmed cell death. Cancer Res, 59, 1693s-1700s.
  28. Kothakota S, Azuma T, Reinhard C, et al (1997). Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science, 278, 294-8. https://doi.org/10.1126/science.278.5336.294
  29. Kohler C, Orrenius S, Zhivotovsky B (2002). Evaluation of caspase activity in apoptotic cells. J Immunol Methods, 265, 97-110. https://doi.org/10.1016/S0022-1759(02)00073-X
  30. Kjaer A, Ohashi M, Wilson JM, et al (1963). Mass spectra of isothiocyanates. Acta Chemica Scandinavica, 17, 2143-54. https://doi.org/10.3891/acta.chem.scand.17-2143
  31. Li C, Wu H, Huang Y, et al (2008). 6-O-Angeloylenolin induces apoptosis through a mitochondrial/caspase and NF-kB pathway in human leukemia HL60 cells. Biomed Pharmacother, 62, 401-9. https://doi.org/10.1016/j.biopha.2007.10.010
  32. Liu MJ, Yue PY, Wang Z, et al (2005). Methyl protodioscin induces G2/M arrest and apoptosis in K562 cells with the hyperpolarization of mitochondria. Cancer Lett, 224, 229-41. https://doi.org/10.1016/j.canlet.2004.11.051
  33. Milojkovic A, Hemmati PG, Muer A, et al (2013). p14ARF induces apoptosis via an entirely caspase-3-dependent mitochondrial amplification loop. Int J Cancer, 133, 2551-62.
  34. Narita M, Shimizu S, Ito T, et al (1998). Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc Nati Acad Sci USA, 95, 14681-6. https://doi.org/10.1073/pnas.95.25.14681
  35. Okada H, Mak TW (2004). Pathways of apoptotic and nonapoptotic death in tumour cells. Nat Rev Cancer, 4, 592-603. https://doi.org/10.1038/nrc1412
  36. Papi A, Orlandi M, Bartolini G, et al (2008). Cytotoxic and Antioxidant Activity of 4-Methylthio-3-butenyl isothiocyanate from Raphanus sativus L. (Kaiware Daikon) Sprouts. J Agric Food Chem, 56, 875-83. https://doi.org/10.1021/jf073123c
  37. Pereira NA, Song Z (2008). Some commonly used caspase substrates and inhibitors lack the specificity required to monitor individual caspase activity. Biochem Biophys Res Commun, 377, 873-7. https://doi.org/10.1016/j.bbrc.2008.10.101
  38. Philchenkov A (2004). Caspases: potential targets for regulating cell death. J Cell Mol Med, 8, 432-44. https://doi.org/10.1111/j.1582-4934.2004.tb00468.x
  39. Rahmani M, Aust MM, Attkisson E, et al (2013). Dual inhibition of Bcl-2 and Bcl-xL strikingly enhances PI3K inhibitioninduced apoptosis in human myeloid leukemia cells through a GSK3- and Bim-dependent mechanisms. Cancer Res, 73, 1340. https://doi.org/10.1158/0008-5472.CAN-12-1365
  40. Sambaziotis D, Kapranos N, Kontogeorgos G (2003). Correlation of bcl-2 and bax with apoptosis in human pituitary adenomas. Pituitary, 6, 127-33. https://doi.org/10.1023/B:PITU.0000011173.04191.37
  41. Song L, Iori R, Thornalley PJ (2006). Purification of major glucosinolates from Brassicaceae seeds and preparation of isothiocyanate and amine metabolites. J Sci Food Agr, 86, 1271-80. https://doi.org/10.1002/jsfa.2488
  42. Sharifia A M, Eslami H, Larijani B, et al (2009). Involvement of caspase-8, -9, and -3 in high glucose-induced apoptosis in PC12 cells. Neuroscience Lett, 459, 47-51. https://doi.org/10.1016/j.neulet.2009.03.100
  43. Troncoso R, Espinoza C, Sanchez-Estrada A, et al (2005). Analysis of the isothiocyanates present in cabbage leaves extract and their potential application to control Alternaria rot in bell peppers. Food Res Int, 38, 701-8. https://doi.org/10.1016/j.foodres.2005.02.004
  44. Vaughn SF, Berhow MA (2005). Glucosinolate hydrolysis products from various plant sources: pH effects, isolation, and purification. Ind Crops Prod, 21, 193-202. https://doi.org/10.1016/j.indcrop.2004.03.004
  45. Wang N, Qu T, Shen L, et al (2010). In-silico study of 4-methylsulfinyl-3-butenyl isothiocyanate binding to tubulin induces A549 cells apoptosis. Acta Pharmaceutica Sinica, 45, 934-9.
  46. Wang N, Shen LQ, Qiu SX, et al (2010). Analysis of the isothiocyanates present in three Chinese Brassica vegetable seeds and their potential anticancer bioactivities. Eur Food Res Technol, 231, 951-8. https://doi.org/10.1007/s00217-010-1348-x
  47. Xia D, Fangshi Z, Yun Yang, et al (2013). Purification, antitumor activity in vitro of steroidal glycoalkaloids from black nightshade (Solanum nigrum L.). Food Chem, 141, 1181-6. https://doi.org/10.1016/j.foodchem.2013.03.062
  48. Xi Z, Shen L L, Zhou J Y, et al (2012). Beta-asarone induces lovo colon cancer cell apoptosis by up-regulation of caspases through a mitochondrial pathway in vitro and in vivo. Asian Pacific J Cancer Prev, 13, 5291-8. https://doi.org/10.7314/APJCP.2012.13.10.5291
  49. Zhu Y, Zhuang J X, Wang Q, et al (2013). Inhibitory effect of benzyl isothiocyanate on proliferation in vitro of human glioma cells. Asian Pacific J Cancer Prev, 14, 2607-10. https://doi.org/10.7314/APJCP.2013.14.4.2607

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