578
Views
52
CrossRef citations to date
0
Altmetric
Original Article

Hydrogen sulfide increases glutathione biosynthesis, and glucose uptake and utilisation in C2C12 mouse myotubes

ORCID Icon &
Pages 288-303 | Received 26 Sep 2017, Accepted 19 Jan 2018, Published online: 12 Mar 2018

References

  • Jain SK. L-cysteine supplementation as an adjuvant therapy for type-2 diabetes. Can J Physiol Pharmacol. 2012;90:1061–1064.
  • Jain SK, Bull R, Rains JL, et al. Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocin-treated rats causes vascular inflammation? Antioxid Redox Signal. 2010;12:1333–1337.
  • Jain SK, Huning L, Micinski D. Hydrogen sulfide upregulates glutamate-cysteine ligase catalytic subunit, glutamate-cysteine ligase modifier subunit, and glutathione and inhibits interleukin-1beta secretion in monocytes exposed to high glucose levels. Metab Syndr Relat Disord. 2014;12:299–302.
  • Jain SK, Kahlon G, Bass P, et al. Can L-cysteine and vitamin D rescue vitamin D and vitamin D binding protein levels in blood plasma of African American Type 2 diabetic patients? Antioxid Redox Signal. 2015;23:688–693.
  • Jain SK, Kahlon G, Morehead L, et al. The effect of sleep apnea and insomnia on blood levels of leptin, insulin resistance, IP-10, and hydrogen sulfide in type 2 diabetic patients. Metab Syndr Relat Disord. 2012;10:331–336.
  • Jain SK, Kanikarla-Marie P, Warden C, et al. L-cysteine supplementation upregulates glutathione (GSH) and vitamin D binding protein (VDBP) in hepatocytes cultured in high glucose and in vivo in liver, and increases blood levels of GSH, VDBP, and 25-hydroxy-vitamin D in Zucker diabetic fatty rats. Mol Nutr Food Res. 2016;60:1090–1098.
  • Jain SK, Micinski D. Vitamin D upregulates glutamate cysteine ligase and glutathione reductase, and GSH formation, and decreases ROS and MCP-1 and IL-8 secretion in high-glucose exposed U937 monocytes. Biochem Biophys Res Commun. 2013;437:7–11.
  • Jain SK, Micinski D, Lieblong BJ, et al. Relationship between hydrogen sulfide levels and HDL-cholesterol, adiponectin, and potassium levels in the blood of healthy subjects. Atherosclerosis. 2012;225:242–245.
  • Manna P, Gungor N, McVie R, et al. Decreased cystathionine-gamma-lyase (CSE) activity in livers of type 1 diabetic rats and peripheral blood mononuclear cells (PBMC) of type 1 diabetic patients. J Biol Chem. 2014;289:11767–11778.
  • Manna P, Jain SK. Vitamin D up-regulates glucose transporter 4 (GLUT4) translocation and glucose utilization mediated by cystathionine-gamma-lyase (CSE) activation and H2S formation in 3T3L1 adipocytes. J Biol Chem. 2012;287:42324–42332.
  • Manna P, Jain SK. PIP3 but not PIP2 increases GLUT4 surface expression and glucose metabolism mediated by AKT/PKCζ/λ phosphorylation in 3T3L1 adipocytes. Mol Cell Biochem. 2013;381:291–299.
  • Manna P, Jain SK. L-cysteine and hydrogen sulfide increase PIP3 and AMPK/PPARgamma expression and decrease ROS and vascular inflammation markers in high glucose treated human U937 monocytes. J Cell Biochem. 2013;114:2334–2345.
  • Sekhar RV, McKay SV, Patel SG, et al. Glutathione synthesis is diminished in patients with uncontrolled diabetes and restored by dietary supplementation with cysteine and glycine. Diabetes Care. 2011;34:162–167.
  • Rey FE, Gonzalez MD, Cheng J, et al. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci USA. 2013;110:13582–13587.
  • Bianchini F, Vainio H. Allium vegetables and organosulfur compounds: do they help prevent cancer? Environ Health Perspect. 2001;109:893–902.
  • Szabó C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6:917–935.
  • Li L, Rose P, Moore PK. Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol. 2011;51:169–187.
  • Liu YH, Lu M, Hu LF, et al. Hydrogen sulfide in the mammalian cardiovascular system. Antioxid Redox Signal. 2012;17:141–185.
  • Predmore BL, Lefer DJ, Gojon G. Hydrogen sulfide in biochemistry and medicine. Antioxid Redox Signal. 2012;17:119–140.
  • Tsai CY, Peh MT, Feng W, et al. Hydrogen sulfide promotes adipogenesis in 3T3L1 cells. PLoS ONE. 2015;10:e0119511.
  • Achari AE, Jain SK. L-cysteine supplementation increases adiponectin synthesis and secretion, and GLUT4 and glucose utilization by upregulating disulfide bond A-like protein expression mediated by MCP-1 inhibition in 3T3-L1 adipocytes exposed to high glucose. Mol Cell Biochem. 2016;414:105–113.
  • Kanikarla-Marie P, Jain SK. L-cysteine supplementation reduces high-glucose and ketone-induced adhesion of monocytes to endothelial cells by inhibiting ROS. Mol Cell Biochem. 2014;391:251–256.
  • Whiteman M, Gooding KM, Whatmore JL, et al. Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia. 2010;53:1722–1726.
  • Geng B, Cai B, Liao F, et al. Increase or decrease hydrogen sulfide exert opposite lipolysis, but reduce global insulin resistance in high fatty diet induced obese mice. PLoS ONE. 2013;8:e73892.
  • Padiya R, Khatua TN, Bagul PK, et al. Garlic improves insulin sensitivity and associated metabolic syndromes in fructose fed rats. Nutr Metab. 2011;8:53.
  • Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066–1071.
  • Nagai Y, Tsugane M, Oka J, et al. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J. 2004;18:557–559.
  • Nedachi T, Kanzaki M. Regulation of glucose transporters by insulin and extracellular glucose in C2C12 myotubes. Am J Physiol Endocrinol Metab. 2006;291:E817–E828.
  • Candiloros H, Muller S, Zeghari N, et al. Decreased erythrocyte membrane fluidity in poorly controlled IDDM. Influence of ketone bodies. Diabetes Care. 1995;18:549–551.
  • Jin S, Pu SX, Hou CL, et al. Cardiac H2S generation is reduced in ageing diabetic mice. Oxid Med Cell Longev. 2015;2015:758358.
  • Lin VS, Lippert AR, Chang CJ. Cell-trappable fluorescent probes for endogenous hydrogen sulfide signaling and imaging H2O2-dependent H2S production. Proc Natl Acad Sci USA. 2013;110:7131–7135.
  • Rubinstein R, Genaro AM, Motta A, et al. Impaired immune responses in streptozotocin-induced type I diabetes in mice. Involvement of high glucose. Clin Exp Immunol. 2008;154:235–246.
  • Barja G. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr. 1999;31:347–366.
  • Borrás C, Gambini J, Gómez-Cabrera MC, et al. 17beta-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFkappaB cascade. Aging Cell. 2005;4:113–118.
  • Jung DW, Ha HH, Zheng X, et al. Novel use of fluorescent glucose analogues to identify a new class of triazine-based insulin mimetics possessing useful secondary effects. Mol Biosyst. 2011;7:346–358.
  • Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101–1108.
  • Pfeiffer CM, Huff DL, Gunter EW. Rapid and accurate HPLC assay for plasma total homocysteine and cysteine in a clinical laboratory setting. Clin Chem. 1999;45:290–292.
  • Ilgü H, Jeckelmann JM, Gapsys V, et al. Insights into the molecular basis for substrate binding and specificity of the wild-type L-arginine/agmatine antiporter AdiC. Proc Natl Acad Sci USA. 2016;113:10358–10363.
  • Deng D, Sun P, Yan C, et al. Molecular basis of ligand recognition and transport by glucose transporters. Nature. 2015;526:391–396.
  • Hresko RC, Kraft TE, Quigley A, et al. Mammalian glucose transporter activity is dependent upon anionic and conical phospholipids. J Biol Chem. 2016;291:17271–17282.
  • Altschul SF, Madden TL, Schäffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402.
  • Remmert M, Biegert A, Hauser A, et al. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods. 2011;9:173–175.
  • Benkert P, Biasini M, Schwede T. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics. 2011;27:343–350.
  • Arnold K, Bordoli L, Kopp J, et al. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 2006;22:195–201.
  • Biasini M, Bienert S, Waterhouse A, et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014;42:W252–W258.
  • Lewerenz J, Hewett SJ, Huang Y, et al. The cystine/glutamate antiporter system x(c)(-) in health and disease: from molecular mechanisms to novel therapeutic opportunities. Antioxid Redox Signal. 2013;18:522–555.
  • Kabil O, Vitvitsky V, Xie P, et al. The quantitative significance of the transsulfuration enzymes for H2S production in murine tissues. Antioxid Redox Signal. 2011;15:363–372.
  • Rains JL, Jain SK. Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med. 2011;50:567–575.
  • Dalle-Donne I, Rossi R, Giustarini D, et al. S-glutathionylation in protein redox regulation. Free Radic Biol Med. 2007;43:883–898.
  • Niwa T. Protein glutathionylation and oxidative stress. J Chromatogr B Analyt Technol Biomed Life Sci. 2007;855:59–65.
  • Muñiz P, Valls V, Perez-Broseta C, et al. The role of 8-hydroxy-2′-deoxyguanosine in rifamycin-induced DNA damage. Free Radic Biol Med. 1995;18:747–755.
  • Chen Y, Johansson E, Fan Y, et al. Early onset senescence occurs when fibroblasts lack the glutamate-cysteine ligase modifier subunit. Free Radic Biol Med. 2009;47:410–418.
  • Ballatori N, Krance SM, Notenboom S, et al. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem. 2009;390:191–214.
  • Harvey CJ, Thimmulappa RK, Singh A, et al. Nrf2-regulated glutathione recycling independent of biosynthesis is critical for cell survival during oxidative stress. Free Radic Biol Med. 2009;46:443–453.
  • Xie L, Gu Y, Wen M, et al. Hydrogen sulfide induces Keap1 S-sulfhydration and suppresses diabetes-accelerated atherosclerosis via Nrf2 activation. Diabetes. 2016;65:3171–3184.
  • Yang G, Zhao K, Ju Y, et al. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal. 2013;18:1906–1919.
  • Itoh K, Mimura J, Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid Redox Signal. 2010;13:1665–1678.
  • Cramer SL, Saha A, Liu J, et al. Systemic depletion of L-cyst(e)ine with cyst(e)inase increases reactive oxygen species and suppresses tumor growth. Nat Med. 2017;23:120–127.
  • Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev. 2012;92:791–896.
  • Lushchak VI. Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids. 2012;2012:736837.
  • Nordberg J, Arnér ES. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med. 2001;31:1287–1312.
  • Lee ZW, Low YL, Huang S, et al. The cystathionine gamma-lyase/hydrogen sulfide system maintains cellular glutathione status. Biochem J. 2014;460:425–435.
  • Watson RT, Kanzaki M, Pessin JE. Regulated membrane trafficking of the insulin-responsive glucose transporter 4 in adipocytes. Endocr Rev. 2004;25:177–204.
  • Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab. 2007;5:237–252.
  • Yamamoto J, Sato W, Kosugi T, et al. Distribution of hydrogen sulfide (H(2)S)-producing enzymes and the roles of the H(2)S donor sodium hydrosulfide in diabetic nephropathy. Clin Exp Nephrol. 2013;17:32–40.
  • Yang G, Wu L, Jiang B, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008;322(5901):587–590.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.