Natural thioallyl compounds increase oxidative stress resistance and lifespan in Caenorhabditis elegans by modulating SKN-1/Nrf

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ogawa, Takahiro ^a,b   Kodera, Yukihiro ^b   Hirata, Dai ^a   Blackwell, T Keith ^c   Mizunuma, Masaki ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b WAKUNAGA PHARMACEUTICAL CO LTD   (Japan)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CYSTEINE; DAF-16 PROTEIN, C ELEGANS; DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; REACTIVE OXYGEN METABOLITE; S-ALLYLCYSTEINE; S-ALLYLMERCAPTOCYSTEINE; SKN-1 PROTEIN, C ELEGANS; TRANSCRIPTION FACTOR;

AGING; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CAENORHABDITIS ELEGANS; CHEMISTRY; DRUG EFFECTS; GARLIC; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LONGEVITY; METABOLISM; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CYSTEINE; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GARLIC; GENE EXPRESSION REGULATION; LONGEVITY; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84959018133     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21611     Document Type: Article

References (54)

1. Fridovich, I. Fundamental aspects of reactive oxygen species, or what's the matter with oxygen? Ann. N. Y. Acad. Sci. 893, 13-18 (1999).
2. Leung, H. W., Vang, M. J. & Mavis, R. D. The cooperative interaction between vitamin E and vitamin C in suppression of peroxidation of membrane phospholipids. Biochim. Biophys. Acta. 664, 266-272 (1981).
3. Guerrero-Beltrán, C. E., Calderón-Oliver, M., Pedraza-Chaverri, J. & Chirino, Y. I. Protective effect of sulforaphane against oxidative stress: recent advances. Exp. Toxicol. Pathol. 64, 503-508 (2012).
4. Sumiyoshi, H. & Wargovich, M. J. Garlic (Allium sativum): a review of its relationship to cancer. Asia Pacific J. Pharmacol. 4, 133-140 (1989).
5. Makheja, A. N., Vanderhoek, J. Y. & Bailey, J. M. Inhibition of platelet aggregation and thromboxane synthesis by onion and garlic. Lancet 1, 781 (1979).
6. Kamanna, V. S. & Chandrasekhara, N. Effect of garlic (Allium sativum linn) on serum lipoproteins and lipoprotein cholesterol levels in albino rats rendered hypercholesteremic by feeding cholesterol. Lipids 17, 483-488 (1982).
7. Hikino, H. et al. Antihepatotoxic actions of Allium sativum bulbs. Planta Med. 52, 163-168 (1986).
8. Sumiyoshi, H. & Wargovich, M. J. Chemoprevention of 1,2-dimethyl hydrazine-induced colon cancer in mice by naturally occurring organo-sulfur compounds. Cancer Res. 50, 5084-5087 (1990).
9. Chuah, S. C., Moore, P. K. & Zhu, Y. Z. S-allylcysteine mediates cardioprotection in an acute myocardial infarction rat model via a hydrogen sulfide-mediated pathway. Am. J. Physiol. Heart Circ. Physiol. 293, H2693-H2701 (2007).
10. Moriguchi, T. et al. Neurotrophic activity of organosulfur compounds having a thioallyl group on cultured rat hippocampal neurons. Neurochem. Res. 22, 1449-1452 (1997).
11. Hsu, C. C., Lin, C. C., Liao, T. S. & Yin, M. C. Protective effect of s-allyl cysteine and s-propyl cysteine on acetaminophen-induced hepatotoxicity in mice. Food Chem. Toxicol. 44, 393-397 (2006).
12. Shirin, H. et al. Antiproliferative effects of S-allylmercaptocysteine on colon cancer cells when tested alone or in combination with sulindac sulfide. Cancer Res. 61, 725-731 (2001).
13. Sumioka, I., Matsura, T., Kasuga, S., Itakura, Y. & Yamada, K. Mechanisms of protection by S-allylmercaptocysteine against acetaminophen-induced liver injury in mice. Jpn. J. Pharmacol. 78, 199-207 (1998).
14. Thomson, M. & Ali, M. Garlic [Allium sativum]: A review of its potential use as an anti-cancer agent. Curr. Cancer Drug Targets 3, 67-81 (2003).
15. Li, G. et al. Antiproliferative effects of garlic constituents in cultured human breast-cancer cells. Oncol. Rep. 2, 787-791 (1995).
16. Hatono, S., Jimenez, A. & Wargovich, M. J. Chemopreventive effect of S-allylcysteine and its relationship to the detoxification enzyme glutathione S-transferase. Carcinogenesis 17, 1041-1044 (1996).
17. McMahon, M. et al. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res. 61, 3299-3307 (2001).
18. Shi, H. et al. S-allyl cysteine activates the Nrf2-dependent antioxidant response and protects neurons against ischemic injury in vitro and in vivo. J. Neurochem. 133, 298-308 (2014).
19. Kenyon, C., Chang, J., Gensch, E., Rudner, A. & Tabtiang, R. A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464 (1993).
20. Ewald, C. Y., Landis, J. N., Porter Abate, J., Murphy, C. T. & Blackwell, T. K. Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity. Nature 519, 97-101 (2015).
21. Sykiotis, G. P. & Bohmann, D. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3, re3 (2010).
22. Murphy, C. T. et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283 (2003).
23. Lee, S. S., Kennedy, S., Tolonen, A. C. & Ruvkun, G. DAF-16 target genes that control C. elegans life-span and metabolism. Science 300, 644-647 (2003).
24. Tullet, J. M. A. et al. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025-1038 (2008).
25. Bowerman, B., Eaton, B. A. & Priess, J. R. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68, 1061-1075 (1992).
26. An, J. H. & Blackwell, T. K. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes dev. 17, 1882-1893 (2003).
27. Oliveira, R. P. et al. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8, 524-541 (2009).
28. Robida-Stubbs, S. et al. TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15, 713-724 (2012).
29. Mizunuma, M., Neumann-Haefelin, E., Moroz, N., Li, Y. & Blackwell, T. K. mTORC2-SGK-1 acts in two environmentally responsive pathways with opposing effects on longevity. Aging Cell 13, 869-878 (2014).
30. Inoue, H. et al. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes dev. 19, 2278-2283 (2005).
31. Wang, J. et al. RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition. PLoS Genet. 6, e1001048 (2010).
32. Li, X. et al. Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet. 7, e1002119 (2011).
33. Glover-Cutter, K. M., Lin, S. & Blackwell, T. K. Integration of the unfolded protein and oxidative stress responses through SKN-1/ Nrf. PLoS Genet. 9, e1003701 (2013).
34. Lithgow, G. J., White, T. M., Melov, S. & Johnson, T. E. Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc. Natl. Acad. Sci. USA. 92, 7540-7544 (1995).
35. Muñoz, M. J. & Riddle, D. L. Positive selection of Caenorhabditis elegans mutants with increased stress resistance and longevity. Genetics 163, 171-180 (2003).
36. Kahn, N. W., Rea, S. L., Moyle, S., Kell, A. & Johnson, T. E. Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans. Biochem. J. 409, 205-213 (2008).
37. Choe, K. P., Przybysz, A. J. & Strange, K. The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol. Cell Biol. 29, 2704-2715 (2009).
38. Alavez, S., Vantipalli, M. C., Zucker, D. J., Klang, I. M. & Lithgow, G. J. Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472, 226-229 (2011).
39. Bishop, N. A. & Guarente, L. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447, 545-549 (2007).
40. Uruno, A. & Motohashi, H. The Keap1-Nrf2 system as an in vivo sensor for electrophiles. Nitric Oxide 25, 153-160 (2011).
41. Choe, K. P., Leung, C. K. & Miyamoto, M. M. Unique structure and regulation of the nematode detoxification gene regulator, SKN- 1:implications to understanding and controlling drug resistance. Drug Metab. Rev. 44, 209-223 (2012).
42. Walker, G., Houthoofd, K., Vanfleteren, J. R. & Gems, D. Dietary restriction in C. elegans: From rate-of-living effects to nutrient sensing pathways. Mech. Ageing Dev. 126, 929-937 (2005).
43. Jiang, J., Jaruga, E., Repnevskaya, M. & Jazwinski, S. An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J. 14, 2135-2137 (2000).
44. Weindruch, R., Walford, R., Fligiel, S. & Guthrie, D. The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J. Nutr. 116, 641-654 (1986).
45. Partridge, L., Green, A. & Fowler, K. Effects of egg-production and of exposure to males on female survival in Drosophila melanogaster. J. Insect Physiol. 33, 745-749 (1987).
46. Liu, L. & Yeh, Y. Y. Inhibition of cholesterol biosynthesis by organosulfur compounds derived from garlic. Lipids 35, 197-203 (2000).
47. Argüello-García, R., Medina-Campos, O. N., Pérez-Hernández, N., Pedraza-Chaverrí, J. & Ortega-Pierres, G. Hypochlorous acid scavenging activities of thioallyl compounds from garlic. J. Agric. Food Chem. 58, 11226-11233 (2010).
48. Liu, L. & Yeh, Y. Y. Water-soluble organosulfur compounds of garlic inhibit fatty acid and triglyceride syntheses in cultured rat hepatocytes. Lipids 36, 395-400 (2001).
49. Powolny, A. A., Singh, S. V., Melov, S., Hubbard, A. & Fisher, A. L. The garlic constituent diallyl trisulfide increases the lifespan of C. elegans via skn-1 activation. Exp. Gerontol. 46, 441-452 (2011).
50. Hatono, S. & Wargovich, M. J. Role of garlic in disease prevention - preclinical models, in Nutraceuticals: Designer food III Garlic, Soy and Licorice; Lachance P. A., Ed.; Food and Nutrition Press: Trumbull, CT, 139-151 (1997).
51. Nagae, S. et al. Pharmacokinetics of the garlic compound S-allylcysteine. Planta Med. 60, 214-217 (1994).
52. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
53. Solis, G. M. & Petrascheck, M. Measuring Caenorhabditis elegans life span in 96 well microtiter plates. J. Vis. Exp. 49, pii: 2496. doi:10.3791/2496 (2011).
54. Smith, E. D. et al. Age- and calorie-independent life span extension from dietary restriction by bacterial deprivation in Caenorhabditis elegans. BMC Dev. Biol. 8, doi:10.1186/1471-213X-8-49 (2008).