Antigenotoxicity and tumor growing inhibition by leafy Brassica carinata and sinigrin

Molecules

Volumn 20, Issue 9, 2015, Pages 15748-15765

  Lozano Baena, María Dolores ^a   Tasset, Inmaculada ^b   Obregón Cano, Sara ^a   De Haro Bailon, Antonio ^a   Muñoz Serrano, Andrés ^c   Alonso Moraga, Ángeles ^c  

^a INSTITUTO DE AGRICULTURA SOSTENIBLE   (Spain)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Antigenotoxicity; Bioactive compound; Brassica; Cytotoxicity; Drosophila melanogaster; HL60; Sinigrin

Indexed keywords

ANTINEOPLASTIC AGENT; GLUCOSINOLATE; HYDROGEN PEROXIDE; SINIGRIN;

ANIMAL; APOPTOSIS; BRASSICA; CELL PROLIFERATION; CHEMISTRY; DROSOPHILA MELANOGASTER; DRUG EFFECTS; HL 60 CELL LINE; HUMAN; PLANT LEAF;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BRASSICA; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; GLUCOSINOLATES; HL-60 CELLS; HUMANS; HYDROGEN PEROXIDE; PLANT LEAVES;

EID: 84947997216     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules200915748     Document Type: Article

References (57)

1. Herr, I.; Buchler, M.W. Dietary constituents of broccoli and other cruciferous vegetables: Implications for prevention and therapy of cancer. Cancer Treat. Rev. 2010, 36, 377-383.
2. Manchali, S.; Murthy, K.N.C.; Patil, B.S. Crucial facts about health benefits of popular cruciferous vegetables. J. Funct. Foods 2012, 4, 94-106.
3. Jahgangir, M.J.; Kim, H.K.; Choi, Y.H.; Verpoorte, R. Health-affecting compounds in Brassicaceae. Compr. Rev. Food Sci. Food Saf. 2009, 8, 31-34.
4. Redovniković, I.R.; Glivetić, T.; Delonga, K.; Vorkapic-Furač, J. Glucosinolates and their potential role in plant. Period. Biol. 2008, 110, 297-309.
5. Antonious, G.F.; Bomford, M.; Vincelli, P. Screening Brassica species for glucosinolate content. J. Environ. Sci. Health Part B 2009, 44, 311-316.
6. Latté, K.P.; Appel, K.E.; Lampen, A. Health benefits and possible risks of broccoli-A review. Food Chem. Toxicol. 2011, 49, 3287-3309.
7. Zukalová, H.; Va͉ák, J. The role and effect of glucosinolates of Brassica species-A review. Rostl. Vyroba 2002, 48, 175-180.
8. Schippers, R.R. African Indigenous Vegetables: An Overview of the Cultivated Species; University of Greenwich, Natural Resources Institute: London, UK, 2000.
9. Tadelle, D.; Alemu, Y.; Moges, H.M.; Fasil, K. Effect of Level of Rapeseed (Brassica carinata) Cake in Rations on Broiler Performance. Livest. Res. Rural Dev. 2003, 15; Available online: http://www.lrrd.org/lrrd15/4/tade154.htm (accessed on 25 June 2015)
10. Taylor, D.C.; Falk, K.C.; Palmer, C.D.; Hammerlindl, J.; Babic, V.; Mietkiewska, E.; Jadhav, A.; Marillia, E.F.; Francis, T.; Hoffman, T.; et al. Brassica carinata-A new molecular farming platform for delivering bio-industrial oil feedstocks: Case studies of genetic modifications to improve very long-chain fatty acid and oil content in seeds. Biofuels Bioprod. Biorefin. 2010, 4, 538-561.
11. De Haro, A.; Domínguez, J.; García, R.; Muñoz, J.; Fernández-Martínez, J.M. Registration of six Ethiopian mustard germplasm lines. Crop Sci. 1998, 38, 558-559.
12. Warwick, S.I.; Gugel, R.K.; McDonald, T.; Falk, K.C. Genetic variation of Ethiopian mustard (Brassica carinata A. Braun) germplasm in western Canada. Genet. Resour. Crop Evol. 2006, 53, 297-312.
13. Bellostas, N.; Sørensen, J.C.; Sørensen, H. Profiling glucosinolates in vegetative and reproductive tissues of four Brassica species of the U-triangle for their biofumigation potential. J. Sci. Food Agric. 2007, 87, 1586-1594.
14. Donkin, S.G.; Eiteman, M.A.; Williams, P.L. Toxicity of glucosinolates and their enzymatic decomposition products to Caenorhabditis elegans. J. Nematol. 1995, 27, 258-262.
15. Martínez-Ballesta, M.C.; Muries, B.; Moreno, D.A.; Dominguez-Perles, R.; García-Viguera, C.; Carvajal, M. Involvement of a glucosinolate (sinigrin) in the regulation of water transport in Brassica oleracea grown under salt stress. Physiol. Plant 2014, 150, 145-160.
16. Hwang, E.S.; Lee, H.J. Induction of quinone reductase by allylisothiocyanate (AITC) and the N-acetylcysteine conjugate of AITC in Hepa1c1c7 mouse hepatoma cells. BioFactors 2006, 26, 7-15.
17. Zhang, Y. Allyl isothiocyanates as a cancer chemopreventive phytochemical. Mol. Nutr. Food Res. 2010, 54, 127-135.
18. Zhang, Y.; Talalay, P. Anticarcinogenic activities of organic isothiocyanates: Chemistry and mechanisms. Cancer Res. 1994, 54, 1976s-1981s.
19. Lamy, E.; Schmitz, S.; Krumbein, A.; Mersch-Sundermann, V. Isothiocyanate-containing mustard protects human cells against genotoxins in vitro and in vivo. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2011, 726, 146-150.
20. Keck, A.S.; Finley, J.W. Cruciferous Vegetables: Cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr. Cancer Ther. 2004, 3, 5-12.
21. USDA. Vegetables. Available online: http://www.choosemyplate.gov/food-groups/vegetables.html (accessed on 25 June 2015).
22. Agudo, A.; Ibanez, R.; Amiano, P.; Ardanaz, E.; Barricarte, A.; Berenguer, A.; Dolores, C.M.; Dorronsoro, M.; Jakszyn, P.; Larranaga, N.; et al. Consumption of cruciferous vegetables and glucosinolates in a Spanish adult population. Eur. J. Clin. Nutr. 2008, 62, 324-331.
23. Spherix. Generally Recognized as Safe (GRAS) Notification for the Use of Aqueous Broccoli Seed Extract Powder in Food. Available online: http://www.fda.gov/ucm/groups/fdagov-public/@fdagov-foods-gen/documents/document/ucm388588.pdf (accessed on 25 June 2015).
24. Sang, J.H.; King, R.C. Nutritional requirements of axenically cultured Drosophila melanogaster adults. J. Exp. Biol. 1961, 38, 793-809.
25. Miller, R.S.; Thomas, J.L. The effects of larval crowding and body size on the longevity of adult Drosophila melanogaster. Ecology 1958, 39, 118-125.
26. Borek, V.; Elberson, L.R.; McCaffrey, J.P.; Morra, M.J. Toxicity of aliphatic and aromatic isothiocyanates to eggs of the black vine weevil (Coleoptera: Curculionidae). J. Econ. Entomol. 1995, 88, 1192-1196.
27. Verhoeven, D.T.H.; Verhagen, H.; Goldbohm, R.A.; van den Brant, P.A.; van Poppel, G. A review of mechanisms underlying anticarcinogenicity by Brassica vegetables. Chem. -Biol. Interact. 1997, 103, 79-129.
28. Pedroche, J.; Just, M.M.; Lqari, H.; Megias, C.; Giron-Calle, J.; Alaiz, M. Obtaining of Brassica carinata protein hydrolysates enriched in bioactive peptides using immobilized digestive proteases. Food Res. Int. 2007, 40, 931-938.
29. Cabello-Hurtado, F.; Gicquel, M.; Esnault, M.A. Evaluation of the antioxidant potential of cauliflower (Brassica oleracea) from a glucosinolate content perspective. Food Chem. 2012, 132, 1003-1009.
30. Romero-Jimenez, M.; Campos-Sanchez, J.; Analla, M.; Munoz-Serrano, A.; Alonso-Moraga, A. Genotoxicity and anti-genotoxicity of some traditional medicinal herbs. Mutat. Res. 2005, 585, 147-155.
31. Tasset-Cuevas, I.; Fernández-Bedmar, Z.; Lozano-Baena, M.D.; Campos-Sánchez, J.; de Haro-Bailón, A.; Muñoz-Serrano, A.; Alonso-Moraga, A. Protective effect of borage seed oil and gamma linolenic acid on DNA: In vivo and in vitro studies. PLoS ONE 2013, 8, e56986.
32. Lobo, V.; Patil, A.; Phatak, A.; Chandra, N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn. Rev. 2010, 4, 118-126.
33. Frei, H.; Würgler, F.E. Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result. Mutat. Res. Environ. Mutagen. Relat. Subj. 1988, 203, 297-308.
34. Frei, H.; Würgler, F.E. Optimal experimental design and sample size for the statistical evaluation of data from somatic mutation and recombination tests (SMART) in Drosophila. Mutat. Res. Environ. Mutagen. Relat. Subj. 1995, 334, 247-258.
35. Baasanjav-Gerber, C.; Hollnagel, H.M.; Brauchmann, J.; Iori, R.; Glatt, H. Detection of genotoxicants in Brassicales using endogenous DNA as a surrogate target and adducts determined by 32P-postlabelling as an experimental end point. Mutagenesis 2011, 26, 407-413.
36. Hansen, M.; Møller, P.; Sørensen, H. Glucosinolates in broccoli stored under controlled atmosphere. J. Am. Soc. Hortic. Sci. 1995, 120, 1069-1074.
37. Heres-Pulido, M.E.; Duenas-Garcia, I.; Castaneda-Partida, L.; Santos-Cruz, L.F.; Vega-Contreras, V.; Rebollar-Vega, R.; Gomez-Luna, J.C.; Duran-Diaz, A. Genotoxicity studies of organically grown broccoli (Brassica oleracea var. italica) and its interactions with urethane, methyl methanesulfonate and 4-nitroquinoline-1-oxide genotoxicity in the wing spot test of Drosophila melanogaster. Food Chem. Toxicol. 2010, 48, 120-128.
38. Musk, S.R.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. Lett. 1995, 348, 19-23.
39. Gonçales, A.L.M.; Lemos, M.; Niero, R.; de Andrade, S.F.; Maistro, E.L. Evaluation of the genotoxic and antigenotoxic potential of Brassica oleracea L. var. acephala DC in different cells of mice. J. Ethnopharmacol. 2012, 143, 740-745.
40. Cartea, M.E.; Velasco, P.; Obregón, S.; Padilla, G.; de Haro, A. Seasonal variation in glucosinolate content in Brassica oleracea crops grown in northwestern Spain. Phytochemistry 2008, 69, 403-410.
41. Akao, Y.; Maruyama, H.; Matsumoto, K.; Ohguchi, K.; Nishizawa, K.; Sakamoto, T.; Araki, Y.; Mishima, S.; Nozawa, Y. Cell growth inhibitory effect of cinnamic acid derivatives from propolis on human tumor cell lines. Biol. Pharm. Bull. 2003, 26, 1057-1059.
42. Jakubikova, J.; Bao, Y.; Sedlak, J. Isothiocyanates induce cell cycle arrest, apoptosis and mitochondrial potential depolarization in HL-60 and multidrug-resistant cell lines. Anticancer Res. 2005, 25, 3375-3386.
43. Ludikhuyze, L.; Rodrigo, L.; Hendrickx, M. The activity of myrosinase from broccoli (Brassica oleracea L. var. italica): Influence of intrinsic and extrinsic factors. J. Food Prot. 2000, 63, 400-403.
44. Jie, M.; Cheung, W.M.; Yu, V,; Zhou, Y.; Tong, P.H.; Ho, J.W. Anti-proliferative activities of sinigrin on carcinogen-induced hepatotoxicity in rats. PLoS ONE 2014, 9, e110145.
45. Øverby, A.; Bævre, M.S.; Thangstad, O.P.; Bones, A.M. Disintegration of microtubules in Arabidopsis thaliana and bladder cancer cells by isothiocyanates. Front. Plant Sci. 2015, 6, doi:10.3389/fpls.2015.00006.
46. Tanaka, T.; Mori, Y.; Morishita, Y.; Hara, A.; Ohno, T.; Kojima, T.; Mori, H. Inhibitory effect of sinigrin and indole-3-carbinol on diethylnitrosamine-induced hepatocarcinogenesis in male ACI/N rats. Carcinogenesis 1990, 11, 1403-1406.
47. Smith, T.K.; Lund, E.K.; Parker, M.L.; Clarke, R.; Johnson, I.T. Allyl-isothiocyanate causes mitotic block, loss of cell adhesion and disrupted cytoskeletal structure in HT29 cells. Carcinogenesis 2004, 25, 1409-1415.
48. Hwang, E.S.; Lee, H.J. Allyl isothiocyanate and its N-acetylcysteine conjugate suppress metastasis via inhibition of invasion, migration, and matrix metalloproteinase-2/-9 activities in SK-Hep 1 human hepatoma cells. Exp. Biol. Med. (Maywood) 2006, 231, 421-430.
49. Lancashire, P.D.; Bleiholder, H.P.; van den Boom, T.; Langeluddecke, P.; Stauss, R.; Weber, E.; Witzenberger, A. A uniform decimal code for growth stages of crops and weeds. Ann. Appl. Biol. 1991, 119, 561-601.
50. Font, R.M.; del Río-Celestino, M.; Cartea, M.E.; de Haro, A. Quantification of aliphatic and índole glucosinolates in leaves of leaf rape (Brassica napus var. pabularia) by near infrared spectroscopy. Phytochemistry 2005, 66, 175-185.
51. Wathelet, J.P.; Wagstaffe, P.; Boenke, A. The Certification of the Total Glucosinolate and Sulphur Contents of Three Rapeseeds (Colza), CRMs 190, 366 and 367; European Commission: Brussels, Belgium, 1991.
52. Graf, U.; Würgler, F.E.; Katz, A.J.; Frei, H.; Juon, H.; Hall, C.B.; Kale, P.G. Somatic mutation and recombination test in Drosophila melanogaster. Environ. Mutagen. 1984, 6, 153-188.
53. Rubin, G.M.; Yandell, M.D.; Wortman, J.R.; Gabor Miklos, G.L.; Nelson, C.R.; Harihanan, I.K.; Fortini, M.E.; Li, P.W.; Apweiler, R.; Fleischmann, W.; et al. Comparative genomics of the eukaryotes. Science 2000, 287, 2204-2215.
54. Graf, U.; Spano, M.A.; Rincon, J.G.; Abraham, S.K.; de Andrade, H.H. The wing somatic mutation and recombination test (SMART) in Drosophila melanogaster: An efficient tool for the detection of genotoxic activity of pure compounds or complex mixtures as well as for studies on antigenotoxicity. Afr. Newslett. Occup. Health Saf. 1996, 6, 9-13.
55. Lindsley, D.L.; Zimm, G.G. The Genome of Drosophila Melanogaster; Academic Press Inc.: San Diego, CA, USA, 1992.
56. Zhu, C.Y.; Loft, S. Effect of chemopreventive compounds from Brassica vegetables on NAD(P)H: Quinine reductase and induction of DNA strand breaks in murine hepa1c1c7 cells. Food Chem. Toxicol. 2003, 41, 455-462.
57. Abraham, S.K. Antigenotoxicity of coffee in the Drosophila assay for somatic mutation and recombination. Mutagenesis 1994, 9, 383-386.