The Effects of Different Garlic-Derived Allyl Sulfides on Anaerobic Sulfur Metabolism in the Mouse Kidney
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals
2.2. Animals and Treatment
2.3. Preparation of Tissue Homogenate
2.4. Methods
2.4.1. Total Sulfane Sulfur
2.4.2. Bound Sulfane Sulfur
2.4.3. H2S Level
2.4.4. γ-Cystathionase (CSE) Activity
2.4.5. Rhodanese (TST) Activity
2.4.6. Aldehyde Dehydrogenase (ALDH) Activity
2.4.7. Protein Content
2.5. Statistical Analysis
3. Results
3.1. The Effect of Garlic-Derived Allyl Sulfides on Kidney Weight
3.2. The Effect of Garlic-Derived Allyl Sulfides (DAS, DADS and DATS) on the Level of Various Reactive Sulfur Species in the Mouse Kidney
3.3. The Effect of Garlic-Derived Allyl Sulfides (DAS, DADS and DATS) on the Activities of Sulfurtransferases (CSE and TST) in the Mouse Kidney
3.4. The Effect of Garlic-Derived Allyl Sulfides (DAS, DADS and DATS) on ALDH Activity
4. Discussion
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Amagase, H. Clarifying the real bioactive constituents of garlic. J. Nutr. 2006, 136, 716S–725S. [Google Scholar] [PubMed]
- Mikaili, P.; Maadirad, S.; Moloudizargari, M.; Aghajanshakeri, S.; Sarahroodi, S. Therapeutic uses and pharmacological properties of garlic, shallot, and their biologically active compounds. Iran. J. Basic Med. Sci. 2013, 16, 1031–1048. [Google Scholar] [PubMed]
- Rana, S.V.; Pal, R.; Vaiphei, K.; Sharma, S.K.; Ola, R.P. Garlic in health and disease. Nutr. Res. Rev. 2011, 24, 60–71. [Google Scholar] [CrossRef] [PubMed]
- Iciek, M.; Kwiecień, I.; Włodek, L. Biological properties of garlic and garlic-derived organosulfur compounds. Environ. Mol. Mutagen. 2009, 50, 247–265. [Google Scholar] [CrossRef] [PubMed]
- Capasso, A. Antioxidant action and therapeutic efficacy of Allium sativum L. Molecules 2013, 18, 690–700. [Google Scholar] [CrossRef] [PubMed]
- Toohey, J.I. Sulphane sulphur in biological systems: A possible regulatory role. Biochem. J. 1989, 264, 625–632. [Google Scholar] [CrossRef] [PubMed]
- Iciek, M.; Wlodek, L. Biosynthesis and biological properties of compounds containing highly reactive, reduced sulfane sulfur. Pol. J. Pharmacol. 2001, 53, 215–225. [Google Scholar] [PubMed]
- Wood, J.L. Sulfane sulfur. Methods Enzymol. 1987, 143, 25–29. [Google Scholar] [PubMed]
- Ogasawara, Y.; Isoda, S.; Tanabe, S. Tissue and subcellular distribution of bound and acid-labile sulfur, and the enzymic capacity for sulfide production in the rat. Biol. Pharm. Bull. 1994, 17, 1535–1542. [Google Scholar] [CrossRef] [PubMed]
- Abe, K.; Kimura, H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 1996, 16, 1066–1071. [Google Scholar] [PubMed]
- Paul, B.D.; Snyder, S.H. H2S: A novel gasotransmitter that signals by sulfhydration. Trends Biochem. Sci. 2015, 40, 687–699. [Google Scholar] [CrossRef] [PubMed]
- Iciek, M.; Kowalczyk-Pachel, D.; Bilska-Wilkosz, A.; Kwiecień, I.; Górny, M.; Włodek, L. S-sulfhydration as a cellular redox regulation. Biosci. Rep. 2016, 36, e00304. [Google Scholar] [CrossRef] [PubMed]
- Mustafa, A.K.; Gadalla, M.M.; Sen, N.; Kim, S.; Mu, W.; Gazi, S.K.; Barrow, R.K.; Yang, G.; Wang, R.; Snyder, S.H. H2S signals through protein S-sulfhydration. Sci. Signal. 2009, 2, ra72. [Google Scholar] [CrossRef] [PubMed]
- Stipanuk, M.H.; Londono, M.; Lee, J.I.; Hu, M.; Yu, A.F. Enzymes and metabolites of cysteine metabolism in nonhepatic tissues of rats show little response to changes in dietary protein or sulfur amino acid levels. J. Nutr. 2002, 132, 3369–3378. [Google Scholar] [PubMed]
- Ubuka, T. Assay methods and biological roles of labile sulfur in animal tissues. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2002, 781, 227–249. [Google Scholar] [CrossRef]
- Włodek, P.J.; Iciek, M.B.; Miłkowski, A.; Smoleński, O.B. Various forms of plasma cysteine and its metabolites in patients undergoing hemodialysis. Clin. Chim. Acta 2001, 304, 9–18. [Google Scholar] [CrossRef]
- Bergström, J.; Alvestrand, A.; Fürst, P.; Lindholm, B. Sulphur amino acids in plasma and muscle in patients with chronic renal failure: Evidence for taurine depletion. J. Intern. Med. 1989, 226, 189–194. [Google Scholar] [CrossRef] [PubMed]
- Ogasawara, Y.; Ishii, K.; Togawa, T.; Tanabe, S. Determination of bound sulfur in serum by gas dialysis/high-performance liquid chromatography. Anal. Biochem. 1993, 215, 73–81. [Google Scholar] [CrossRef] [PubMed]
- Kowalczyk-Pachel, D.; Iciek, M.; Wydra, K.; Nowak, E.; Gorny, M.; Filip, M.; Wlodek, L.; Lorenc-Koci, E. Cysteine metabolism and oxidative processes in the rat liver and kidney after acute and repeated cocaine treatment. PLoS ONE 2016, 11, e0147238. [Google Scholar] [CrossRef] [PubMed]
- Shen, X.; Pattillo, C.B.; Pardue, S.; Bir, S.C.; Wang, R.; Kevil, C.G. Measurement of plasma hydrogen sulfide in vivo and in vitro. Free Radic. Biol. Med. 2011, 50, 1021–1031. [Google Scholar] [CrossRef] [PubMed]
- Matsuo, Y.; Greenberg, D.M. A crystalline enzyme that cleaves homoserine and cystathionine. Mechanism of action, reversibility and substrate specify. J. Biol. Chem. 1959, 234, 516–519. [Google Scholar] [PubMed]
- Sörbo, B. Rhodanese. Methods Enzymol. 1955, 2, 334–337. [Google Scholar]
- Tottmar, S.O.; Pettersson, H.; Kiessling, K.H. The subcellular distribution and properties of aldehyde dehydrogenases in rat liver. Biochem. J. 1975, 135, 577–586. [Google Scholar] [CrossRef]
- Lowry, O.H.; Rosenbrough, N.J.; Farr, A.L.; Randall, R.I. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193, 265–275. [Google Scholar] [PubMed]
- Szczepkowski, T.W.; Wood, J.L. The cystathionase-rhodanese system. Biochim. Biophys. Acta 1967, 139, 469–478. [Google Scholar] [CrossRef]
- Porter, D.W.; Nealley, E.W.; Baskin, S.I. In vivo detoxification of cyanide by cystathionase γ-lyase. Biochem. Pharmacol. 1996, 52, 941–944. [Google Scholar] [CrossRef]
- Iciek, M.B.; Kowalczyk-Pachel, D.; Kwiecień, I.; Dudek, M.B. Effects of different garlic-derived allyl sulfides on peroxidative processes and anaerobic sulfur metabolism in mouse liver. Phytother. Res. 2012, 26, 425–431. [Google Scholar] [CrossRef] [PubMed]
- Iciek, M.; Bilska, A.; Książek, L.; Srebro, Z.; Włodek, L. Allyl disulfide as donor and cyanide as acceptor of sulfane sulfur in the mouse tissues. Pharmacol. Rep. 2005, 57, 212–218. [Google Scholar] [PubMed]
- Srebro, Z.; Iciek, M.; Sura, P.; Góralska, M. The glial Gomori-positive material is sulfane sulfur. Folia Histochem. Cytobiol. 2008, 46, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Jackson, M.R.; Melideo, S.L.; Jorns, M.S. Human sulfide: Quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 2012, 51, 6804–6815. [Google Scholar] [CrossRef] [PubMed]
- Hildebrandt, T.M.; Grieshaber, M.K. Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J. 2008, 275, 3352–3361. [Google Scholar] [CrossRef] [PubMed]
- Stipanuk, M.H.; Beck, P.W. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem. J. 1982, 206, 267–277. [Google Scholar] [CrossRef] [PubMed]
- Wang, P.; Isaak, C.K.; Siow, Y.L.; Karmin, O. Downregulation of cystathionine β-synthase and cystathionine γ-lyase expression stimulates inflammation in kidney ischemia–reperfusion injury. Physiol. Rep. 2014, 12, e12251. [Google Scholar] [CrossRef] [PubMed]
- Bełtowski, J. Hypoxia in the renal medulla: Implications for hydrogen sulfide signaling. J. Pharmacol. Exp. Ther. 2010, 334, 358–363. [Google Scholar] [CrossRef] [PubMed]
- Hui, Y.; Du, J.; Tang, C.; Bin, G.; Jiang, H. Changes in arterial hydrogen sulfide (H2S) content during septic shock and endotoxin shock in rats. J. Infect. 2003, 47, 155–160. [Google Scholar] [CrossRef]
- Kamoun, P. Mental retardation in Down syndrome: A hydrogen sulfide hypothesis. Med. Hypotheses 2001, 57, 389–392. [Google Scholar] [CrossRef] [PubMed]
- Iciek, M.; Marcinek, J.; Mleczko, U.; Włodek, L. Selective effects of diallyl disulfide, a sulfane sulfur precursor, in the liver and Ehrlich ascites tumor cells. Eur. J. Pharmacol. 2007, 569, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Benavides, G.A.; Squadrito, G.L.; Mills, R.W.; Patel, H.D.; Isbell, T.S.; Patel, R.P.; Darley-Usmar, V.M.; Doeller, J.E.; Kraus, D.W. Hydrogen sulfide mediates the vasoactivity of garlic. Proc. Natl. Acad. Sci. USA 2007, 104, 17977–17982. [Google Scholar] [CrossRef] [PubMed]
- Paulsen, C.E.; Carroll, K.S. Cysteine-mediated redox signaling: Chemistry, biology, and tools for discovery. Chem. Rev. 2013, 113, 4633–4679. [Google Scholar] [CrossRef] [PubMed]
- DeLeon, E.R.; Gao, Y.; Huang, E.; Olson, K.R. Garlic oil polysulfides: H2S- and O2-independent prooxidants in buffer and antioxidants in cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2016, 310, R1212–R1225. [Google Scholar] [CrossRef] [PubMed]
- Toohey, J.I. Sulfur signaling: Is the agent sulfide or sulfane? Anal. Biochem. 2011, 413, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Vasiliou, V.; Pappa, A.; Petersen, D.R. Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem. Biol. Interact. 2000, 129, 1–19. [Google Scholar] [CrossRef]
- Esterbauer, H.; Schaur, R.J.; Zollner, H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11, 81–128. [Google Scholar] [CrossRef]
- Kim, S.H.; Kaschula, C.H.; Priedigkeit, N.; Lee, A.V.; Singh, S.V. Forkhead Box Q1 Is a Novel Target of Breast Cancer Stem Cell Inhibition by Diallyl Trisulfide. J. Biol. Chem. 2016, 291, 13495–13508. [Google Scholar] [CrossRef] [PubMed]
- Kishimoto, R.; Ueda, M.; Yoshinag, H.; Goda, K.; Park, S.S. Combined effects of ethanol and garlic on hepatic ethanol metabolism in mice. J. Nutr. Sci. Vitaminol. 1999, 45, 275–286. [Google Scholar] [CrossRef] [PubMed]
- Bagheri, F.; Gol, A.; Dabiri, S.; Javadi, A. Preventive effect of garlic juice on renal reperfusion injury. Iran. J. Kidney Dis. 2011, 5, 194–200. [Google Scholar] [PubMed]
Group | Kidney Weight (Mean ± SD) (g) |
---|---|
Control | 0.277 ± 0.028 |
DAS | 0.307 ± 0.061 |
DADS | 0.308 ± 0.032 |
DATS | 0.289 ± 0.028 |
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Iciek, M.; Bilska-Wilkosz, A.; Górny, M.; Sokołowska-Jeżewicz, M.; Kowalczyk-Pachel, D. The Effects of Different Garlic-Derived Allyl Sulfides on Anaerobic Sulfur Metabolism in the Mouse Kidney. Antioxidants 2016, 5, 46. https://doi.org/10.3390/antiox5040046
Iciek M, Bilska-Wilkosz A, Górny M, Sokołowska-Jeżewicz M, Kowalczyk-Pachel D. The Effects of Different Garlic-Derived Allyl Sulfides on Anaerobic Sulfur Metabolism in the Mouse Kidney. Antioxidants. 2016; 5(4):46. https://doi.org/10.3390/antiox5040046
Chicago/Turabian StyleIciek, Małgorzata, Anna Bilska-Wilkosz, Magdalena Górny, Maria Sokołowska-Jeżewicz, and Danuta Kowalczyk-Pachel. 2016. "The Effects of Different Garlic-Derived Allyl Sulfides on Anaerobic Sulfur Metabolism in the Mouse Kidney" Antioxidants 5, no. 4: 46. https://doi.org/10.3390/antiox5040046
APA StyleIciek, M., Bilska-Wilkosz, A., Górny, M., Sokołowska-Jeżewicz, M., & Kowalczyk-Pachel, D. (2016). The Effects of Different Garlic-Derived Allyl Sulfides on Anaerobic Sulfur Metabolism in the Mouse Kidney. Antioxidants, 5(4), 46. https://doi.org/10.3390/antiox5040046