164
Views
7
CrossRef citations to date
0
Altmetric
Review

Hydrogen Sulfide, Adipose Tissue and Diabetes Mellitus

, , , &
Pages 1873-1886 | Published online: 03 Jun 2020

References

  • Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16(3):1066. doi:10.1523/JNEUROSCI.16-03-01066.1996
  • Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol. 2020.
  • 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(11):1333–1337. doi:10.1089/ars.2009.2956
  • Yusuf M, Kwong Huat BT, Hsu A, Whiteman M, Bhatia M, Moore PK. Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulfide biosynthesis. Biochem Biophys Res Commun. 2005;333(4):1146–1152. doi:10.1016/j.bbrc.2005.06.021
  • Wu L, Yang W, Jia X, et al. Pancreatic islet overproduction of H2S and suppressed insulin release in Zucker diabetic rats. Lab Invest. 2009;89(1):59–67. doi:10.1038/labinvest.2008.109
  • Gheibi S, Samsonov AP, Gheibi S, Vazquez AB, Kashfi K. Regulation of carbohydrate metabolism by nitric oxide and hydrogen sulfide: implications in diabetes. Biochem Pharmacol. 2020;113819.
  • Zhang Y, Yang J, Wang T, et al. Decreased endogenous hydrogen sulfide generation in penile tissues of diabetic rats with erectile dysfunction. J Sex Med. 2016;13(3):350–360. doi:10.1016/j.jsxm.2016.01.002
  • Kimura H. Signalling by hydrogen sulfide and polysulfides via protein S-sulfuration. Br J Pharmacol. 2020;177:720–733. doi:10.1111/bph.14579
  • Shibuya N, Koike S, Tanaka M, et al. A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat Commun. 2013;4(1):1366. doi:10.1038/ncomms2371
  • Kabil O, Banerjee R. Enzymology of H2S biogenesis, decay and signaling. Antioxid Redox Signal. 2014;20(5):770–782. doi:10.1089/ars.2013.5339
  • Huang CW, Moore PK. H2S synthesizing enzymes: biochemistry and molecular aspects. Handb Exp Pharmacol. 2015;230:3–25.
  • Ahmad FU, Sattar MA, Rathore HA, et al. Exogenous Hydrogen Sulfide (H2S) reduces blood pressure and prevents the progression of diabetic nephropathy in spontaneously hypertensive rats. Ren Fail. 2012;34(2):203–210. doi:10.3109/0886022X.2011.643365
  • Suzuki K, Sagara M, Aoki C, Tanaka S, Aso Y. Clinical implication of plasma hydrogen sulfide levels in Japanese patients with Type 2 diabetes. Inter Med. 2017;56(1):17–21. doi:10.2169/internalmedicine.56.7403
  • Ali MY, Whiteman M, Low CM, Moore PK. Hydrogen sulphide reduces insulin secretion from HIT-T15 cells by a KATP channel-dependent pathway. J Endocrinol. 2007;195(1):105–112. doi:10.1677/JOE-07-0184
  • Yang G, Yang W, Wu L, Wang R. H2S, endoplasmic reticulum stress, and apoptosis of insulin-secreting beta cells. J Biol Chem. 2007;282(22):16567–16576. doi:10.1074/jbc.M700605200
  • Yang G, Tang G, Zhang L, Wu L, Wang R. The pathogenic role of cystathionine gamma-lyase/hydrogen sulfide in streptozotocin-induced diabetes in mice. Am J Pathol. 2011;179(2):869–879. doi:10.1016/j.ajpath.2011.04.028
  • Brancaleone V, Roviezzo F, Vellecco V, De Gruttola L, Bucci M, Cirino G. Biosynthesis of H2S is impaired in non-obese diabetic (NOD) mice. Br J Pharmacol. 2008;155:673–680. doi:10.1038/bjp.2008.296
  • Coppack SW. Adipose tissue changes in obesity. Biochem Soc Trans. 2005;33(5):1049. doi:10.1042/BST0331049
  • Hajer GR, van Haeften TW, Visseren FLJ. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J. 2008;29(24):2959–2971. doi:10.1093/eurheartj/ehn387
  • Unamuno X, Gómez-Ambrosi J. Adipokine dysregulation and adipose tissue inflammation in human obesity. 2018;48:e12997.
  • Feng X, Chen Y, Zhao J, Tang C, Jiang Z, Geng B. Hydrogen sulfide from adipose tissue is a novel insulin resistance regulator. Biochem Biophys Res Commun. 2009;380(1):153–159. doi:10.1016/j.bbrc.2009.01.059
  • Fang L, Zhao J, Chen Y, et al. Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J Hypertens. 2009;27(11):2174–2185. doi:10.1097/HJH.0b013e328330a900
  • Bełtowski J, Jamroz-Wiśniewska A. Hydrogen sulfide in the adipose tissue-physiology, pathology and a target for pharmacotherapy. Molecules (Basel, Switzerland). 2016;22.
  • Akash MS, Rehman K, Chen S. Role of inflammatory mechanisms in pathogenesis of type 2 diabetes mellitus. J Cell Biochem. 2013;114(3):525–531. doi:10.1002/jcb.24402
  • Richardson VR, Smith KA, Carter AM. Adipose tissue inflammation: feeding the development of type 2 diabetes mellitus. Immunobiology. 2013;218(12):1497–1504. doi:10.1016/j.imbio.2013.05.002
  • Deng J, Wang M, Guo Y, et al. Activation of α7nAChR via vagus nerve prevents obesity-induced insulin resistance via suppressing endoplasmic reticulum stress-induced inflammation in Kupffer cells. Med Hypotheses. 2020;140:109671. doi:10.1016/j.mehy.2020.109671
  • Crujeiras AB, Cordero P. Molecular basis of the inflammation related to obesity. Oxid Med Cell Longevity. 2019;2019:5250816.
  • Reilly SM, Saltiel AR. Adapting to obesity with adipose tissue inflammation. Nat Rev Endocrinol. 2017;13(11):633–643. doi:10.1038/nrendo.2017.90
  • Petrus P, Lecoutre S, Dollet L, et al. Glutamine links obesity to inflammation in human white adipose tissue. Cell Metab. 2020;31(2):375–90.e11. doi:10.1016/j.cmet.2019.11.019
  • Saxton SN, Clark BJ, Withers SB, Eringa EC, Heagerty AM. Mechanistic links between obesity, diabetes, and blood pressure: role of perivascular adipose tissue. Physiol Rev. 2019;99(4):1701–1763. doi:10.1152/physrev.00034.2018
  • Zhu Q, Scherer PE. Immunologic and endocrine functions of adipose tissue: implications for kidney disease. Nat Rev Nephrol. 2018;14(2):105–120. doi:10.1038/nrneph.2017.157
  • Comas F, Latorre J, Cussó O, et al. Hydrogen sulfide impacts on inflammation-induced adipocyte dysfunction. Food Chem Toxicol. 2019;131:110543.
  • Chi Q, Chi X, Hu X, Wang S, Zhang H, Li S. The effects of atmospheric hydrogen sulfide on peripheral blood lymphocytes of chickens: perspectives on inflammation, oxidative stress and energy metabolism. Environ Res. 2018;167:1–6. doi:10.1016/j.envres.2018.06.051
  • Barton M, Meyer MR. HuR-ry up: how hydrogen sulfide protects against atherosclerosis. Circulation. 2019;139(1):115–118. doi:10.1161/CIRCULATIONAHA.118.036854
  • 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(10):3171–3184. doi:10.2337/db16-0020
  • Luo ZL, Ren JD, Huang Z, et al. The role of exogenous hydrogen sulfide in free fatty acids induced inflammation in macrophages. Cell Physiol Biochem. 2017;42:1635–1644. doi:10.1159/000479405
  • Suzuki K, Olah G, Modis K, et al. Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci U S A. 2011;108(33):13829–13834. doi:10.1073/pnas.1105121108
  • Cheng Z, Shen X, Jiang X, et al. Hyperhomocysteinemia potentiates diabetes-impaired EDHF-induced vascular relaxation: role of insufficient hydrogen sulfide. Redox Biol. 2018;16:215–225. doi:10.1016/j.redox.2018.02.006
  • Cheng Z, Garikipati VN, Nickoloff E, et al. Restoration of hydrogen sulfide production in diabetic mice improves reparative function of bone marrow cells. Circulation. 2016;134(19):1467–1483. doi:10.1161/CIRCULATIONAHA.116.022967
  • 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(8):1722–1726. doi:10.1007/s00125-010-1761-5
  • Pan Z, Wang H, Liu Y, et al. Involvement of CSE/H2S in high glucose induced aberrant secretion of adipokines in 3T3-L1 adipocytes. Lipids Health Dis. 2014;13(1):155. doi:10.1186/1476-511X-13-155
  • Velmurugan GV, Huang H, Sun H, et al. Depletion of H2S during obesity enhances store-operated Ca2+entry in adipose tissue macrophages to increase cytokine production. Sci Signal. 2015;8(407):ra128. doi:10.1126/scisignal.aac7135
  • Zhou X, Yang W, Li J. Ca2+- and protein kinase C-dependent signaling pathway for nuclear Factor-κB activation, inducible nitric-oxide synthase expression, and tumor necrosis factor-α production in lipopolysaccharide-stimulated rat peritoneal macrophages. J Biol Chem. 2006;281(42):31337–31347. doi:10.1074/jbc.M602739200
  • Kim Y, Moon JS, Lee KS, et al. Ca2+/calmodulin-dependent protein phosphatase calcineurin mediates the expression of iNOS through IKK and NF-kappaB activity in LPS-stimulated mouse peritoneal macrophages and RAW 264.7 cells. Biochem Biophys Res Commun. 2004;314(3):695–703. doi:10.1016/j.bbrc.2003.12.153
  • Barazzoni R, Gortan Cappellari G, Ragni M, Nisoli E. Insulin resistance in obesity: an overview of fundamental alterations. Eating Weight Disord. 2018;23(2):149–157. doi:10.1007/s40519-018-0481-6
  • Feller DD, Feist E. Conversion of methionine and threonine to fatty acids by adipose tissue. Can J Biochem Physiol. 1963;41(1):269–273. doi:10.1139/y63-034
  • Heeren J, Scheja L. Brown adipose tissue and lipid metabolism. Curr Opin Lipidol. 2018;29(3):180–185. doi:10.1097/MOL.0000000000000504
  • Antonopoulos AS, Tousoulis D. The molecular mechanisms of obesity paradox. Cardiovasc Res. 2017;113(9):1074–1086. doi:10.1093/cvr/cvx106
  • Kim WJ, Lee W, Jung Y, Jang HJ, Kim YK, Kim SN. PPARβ/δ agonist GW501516 inhibits TNFα-induced repression of adiponectin and insulin receptor in 3T3-L1 adipocytes. Biochem Biophys Res Commun. 2019;510(4):621–628. doi:10.1016/j.bbrc.2019.02.013
  • Palit SP, Patel R, Jadeja SD, Rathwa N, Mahajan A, Ramachandran AV. A genetic analysis identifies a haplotype at adiponectin locus: association with obesity and type 2 diabetes. Sci Rep. 2020;10:2904.
  • Bermúdez VJ, Rojas E, Toledo A, et al. Single-nucleotide polymorphisms in adiponectin, AdipoR1, and AdipoR2 genes: insulin resistance and type 2 diabetes mellitus candidate genes. Am J Ther. 2013;20(4):414–421. doi:10.1097/MJT.0b013e318235f206
  • Huang CY, Yao WF, Wu WG, Lu YL, Wan H, Wang W. Endogenous CSE/H2 S system mediates TNF-alpha-induced insulin resistance in 3T3-L1 adipocytes. Cell Biochem Funct. 2013;31:468–475. doi:10.1002/cbf.2920
  • 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. doi:10.1074/jbc.M112.407833
  • Manna P, Jain SK. Hydrogen sulfide and L-cysteine increase phosphatidylinositol 3,4,5-trisphosphate (PIP3) and glucose utilization by inhibiting phosphatase and tensin homolog (PTEN) protein and activating phosphoinositide 3-kinase (PI3K)/serine/threonine protein kinase (AKT)/protein kinase Czeta/lambda (PKCzeta/lambda) in 3T3l1 adipocytes. J Biol Chem. 2011;286:39848–39859.
  • Manna P, Jain SK. Hydrogen sulfide and L-cysteine increase phosphatidylinositol 3,4,5-trisphosphate (PIP3) and glucose utilization by inhibiting phosphatase and tensin homolog (PTEN) protein and activating phosphoinositide 3-kinase (PI3K)/serine/threonine protein kinase (AKT)/protein kinase Cζ/λ (PKCζ/λ) in 3T3l1 adipocytes. J Biol Chem. 2011;286(46):39848–39859.
  • Xue R, Hao DD, Sun JP, et al. Hydrogen sulfide treatment promotes glucose uptake by increasing insulin receptor sensitivity and ameliorates kidney lesions in type 2 diabetes. Antioxid Redox Signal. 2013;19:5–23. doi:10.1089/ars.2012.5024
  • 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(9):e73892. doi:10.1371/journal.pone.0073892
  • Geng B. [Adipocytic endogenous hydrogen sulfide-function,regulation and diseases]. Sheng li Ke Xue Jin Zhan [Progress in Physiology]. 2017;48(1):37–41. Chinese.
  • Lee WH, Rho JG, Han HS, et al. Self-assembled hyaluronic acid nanoparticle suppresses fat accumulation via CD44 in diet-induced obese mice. Carbohydr Polym. 2020;237:116161. doi:10.1016/j.carbpol.2020.116161
  • Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS. Regulation of lipolysis in adipocytes. Annu Rev Nutr. 2007;27(1):79–101. doi:10.1146/annurev.nutr.27.061406.093734
  • Abranches MV, Oliveira FC, Conceicao LL, Peluzio MD. Obesity and diabetes: the link between adipose tissue dysfunction and glucose homeostasis. Nutr Res Rev. 2015;28:121–132. doi:10.1017/S0954422415000098
  • Tsai CY, Peh MT, Feng W, Dymock BW, Moore PK. Hydrogen sulfide promotes adipogenesis in 3T3L1 cells. PLoS One. 2015;10:e0119511. doi:10.1371/journal.pone.0119511
  • Haj-Yasein NN, Berg O, Jerneren F, Refsum H, Nebb HI, Dalen KT. Cysteine deprivation prevents induction of peroxisome proliferator-activated receptor gamma-2 and adipose differentiation of 3T3-L1 cells. Biochim Biophys Acta. 2017;1862:623–635.
  • Cai J, Shi X, Wang H, et al. Cystathionine gamma lyase-hydrogen sulfide increases peroxisome proliferator-activated receptor gamma activity by sulfhydration at C139 site thereby promoting glucose uptake and lipid storage in adipocytes. Biochim Biophys Acta. 2016;1861:419–429. doi:10.1016/j.bbalip.2016.03.001
  • Haj-Yasein NN, Berg O, Jernerén F, Refsum H, Nebb HI, Dalen KT. Cysteine deprivation prevents induction of peroxisome proliferator-activated receptor gamma-2 and adipose differentiation of 3T3-L1 cells. Biochimica Et Biophysica Acta Molecular and Cell Biology of Lipids. 2017;1862(6):623–635.
  • Soltis EE, Cassis LA. Influence of perivascular adipose tissue on rat aortic smooth muscle responsiveness. Clin Exp Hypertension Part A. 1991;13(2):277–296. doi:10.3109/10641969109042063
  • Kassam SI, Lu C, Buckley N, Gao YJ, Lee RM. Modulation of thiopental-induced vascular relaxation and contraction by perivascular adipose tissue and endothelium. Br J Anaesth. 2012;109(2):177–184. doi:10.1093/bja/aes127
  • Oriowo MA. Perivascular adipose tissue, vascular reactivity and hypertension. Med Principl Pract. 2015;24(Suppl 1):29–37. doi:10.1159/000356380
  • Szasz T, Webb RC. Perivascular adipose tissue: more than just structural support. Clin sci. 2012;122(1):1–12. doi:10.1042/CS20110151
  • Gollasch M. Vasodilator signals from perivascular adipose tissue. Br J Pharmacol. 2012;165(3):633–642. doi:10.1111/j.1476-5381.2011.01430.x
  • Stasko A, Brezova V, Zalibera M, Biskupic S, Ondrias K. Electron transfer: a primary step in the reactions of sodium hydrosulphide, an H2S/HS−donor. Free Radic Res. 2009;43(6):581–593. doi:10.1080/10715760902977416
  • Gamper N, Zaika O, Li Y, et al. Oxidative modification of M-type K+ channels as a mechanism of cytoprotective neuronal silencing. EMBO J. 2006;25(20):4996–5004. doi:10.1038/sj.emboj.7601374
  • Schleifenbaum J, Kohn C, Voblova N, et al. Systemic peripheral artery relaxation by KCNQ channel openers and hydrogen sulfide. J Hypertens. 2010;28(9):1875–1882. doi:10.1097/HJH.0b013e32833c20d5
  • Kohn C, Schleifenbaum J, Szijarto IA, et al. Differential effects of cystathionine-gamma-lyase-dependent vasodilatory H2S in periadventitial vasoregulation of rat and mouse aortas. PLoS One. 2012;7(8):e41951.
  • Emilova R, Dimitrova D, Mladenov M, Daneva T, Schubert R, Gagov H. Cystathionine gamma-lyase of perivascular adipose tissue with reversed regulatory effect in diabetic rat artery. Biotechnol Biotechnol Equip. 2015;29(1):147–151. doi:10.1080/13102818.2014.991565
  • Queiroz M, Sena CM. Perivascular adipose tissue in age-related vascular disease. Ageing Res Rev. 2020;59:101040. doi:10.1016/j.arr.2020.101040
  • Köhn C, Schleifenbaum J, Szijártó IA, et al. Differential effects of cystathionine-γ-lyase-dependent vasodilatory H2S in periadventitial vasoregulation of rat and mouse aortas. PLoS One. 2012;7(8):e41951.
  • Orlov SN, Gusakova SV, Smaglii LV, Koltsova SV, Sidorenko SV. Vasoconstriction triggered by hydrogen sulfide: evidence for Na(+),K(+),2Cl(-)cotransport and L-type Ca(2+) channel-mediated pathway. Biochem Biophys Rep. 2017;12:220–227. doi:10.1016/j.bbrep.2017.09.010
  • Yamauchi T, Kamon J, Waki H, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7(8):941–946. doi:10.1038/90984
  • Ran J, Hirano T, Fukui T, et al. Angiotensin II infusion decreases plasma adiponectin level via its type 1 receptor in rats: an implication for hypertension-related insulin resistance. Metabolism. 2006;55(4):478–488. doi:10.1016/j.metabol.2005.10.009
  • Chu NF, Spiegelman D, Hotamisligil GS, Rifai N, Stampfer M, Rimm EB. Plasma insulin, leptin, and soluble TNF receptors levels in relation to obesity-related atherogenic and thrombogenic cardiovascular disease risk factors among men. Atherosclerosis. 2001;157(2):495–503. doi:10.1016/S0021-9150(00)00755-3
  • Fruhbeck G, Catalan V, Gomez-Ambrosi J, Rodriguez A. Aquaporin-7 and glycerol permeability as novel obesity drug-target pathways. Trends Pharmacol Sci. 2006;27(7):345–347. doi:10.1016/j.tips.2006.05.002
  • Gomez-Ambrosi J, Catalan V, Ramirez B, et al. Plasma osteopontin levels and expression in adipose tissue are increased in obesity. J Clin Endocrinol Metab. 2007;92(9):3719–3727. doi:10.1210/jc.2007-0349
  • Furuhashi M, Fucho R, Gorgun CZ, Tuncman G, Cao H, Hotamisligil GS. Adipocyte/macrophage fatty acid-binding proteins contribute to metabolic deterioration through actions in both macrophages and adipocytes in mice. J Clin Invest. 2008;118:2640–2650. doi:10.1172/JCI34750
  • Matsuzawa Y. Therapy Insight: adipocytokines in metabolic syndrome and related cardiovascular disease. Nat Clin Pract Cardiovasc Med. 2006;3(1):35–42. doi:10.1038/ncpcardio0380
  • Fruhbeck G. The Sir David Cuthbertson Medal Lecture. Hunting for new pieces to the complex puzzle of obesity. Proc Nutr Soc. 2006;65:329–347.
  • Zhang Y, Zitsman JL, Hou J, et al. Fat cell size and adipokine expression in relation to gender, depot, and metabolic risk factors in morbidly obese adolescents. Obesity (Silver Spring, Md). 2014;22(3):691–697. doi:10.1002/oby.20528
  • Mihu D, Ciortea R, Mihu CM. Abdominal adiposity through adipocyte secretion products, a risk factor for endometrial cancer. Gynecol Endocrinol. 2013;29(5):448–451. doi:10.3109/09513590.2012.752452
  • Fischer-Posovszky P, Hebestreit H, Hofmann AK, et al. Role of CD95-mediated adipocyte loss in autoimmune lipodystrophy. J Clin Endocrinol Metab. 2006;91(3):1129–1135. doi:10.1210/jc.2005-0737
  • Prins JB, Walker NI, Winterford CM, Cameron DP. Human adipocyte apoptosis occurs in malignancy. Biochem Biophys Res Commun. 1994;205(1):625–630. doi:10.1006/bbrc.1994.2711
  • Domingo P, Matias-Guiu X, Pujol RM, et al. Subcutaneous adipocyte apoptosis in HIV-1 protease inhibitor-associated lipodystrophy. AIDS (London, England). 1999;13(16):2261–2267. doi:10.1097/00002030-199911120-00008
  • Ortiz VE, Vidal-Melo MF, Walsh JL. Strategies for managing oxygenation in obese patients undergoing laparoscopic surgery. Surg Obesity Related Dis. 2015;11(3):721–728. doi:10.1016/j.soard.2014.11.021
  • Gong L, Zou Z, Huang L, Guo S, Xing D. Photobiomodulation therapy decreases free fatty acid generation and release in adipocytes to ameliorate insulin resistance in type 2 diabetes. Cell Signal. 2020;67:109491. doi:10.1016/j.cellsig.2019.109491
  • Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes. 2007;56(4):901–911. doi:10.2337/db06-0911
  • Prins JB, Walker NI, Winterford CM, Cameron DP. Apoptosis of human adipocytes in vitro. Biochem Biophys Res Commun. 1994;201(2):500–507. doi:10.1006/bbrc.1994.1730
  • Papineau D, Gagnon A, Sorisky A. Apoptosis of human abdominal preadipocytes before and after differentiation into adipocytes in culture. Metabolism. 2003;52(8):987–992. doi:10.1016/S0026-0495(03)00165-3
  • Chaiittianan R, Sutthanut K, Rattanathongkom A. Purple corn silk: a potential anti-obesity agent with inhibition on adipogenesis and induction on lipolysis and apoptosis in adipocytes. J Ethnopharmacol. 2017;201:9–16. doi:10.1016/j.jep.2017.02.044
  • Hamrick MW, Della Fera MA, Choi YH, Hartzell D, Pennington C, Baile CA. Injections of leptin into rat ventromedial hypothalamus increase adipocyte apoptosis in peripheral fat and in bone marrow. Cell Tissue Res. 2007;327(1):133–141. doi:10.1007/s00441-006-0312-3
  • Jung TW, Kim ST, Lee JH, et al. Phosphatidylcholine causes lipolysis and apoptosis in adipocytes through the tumor necrosis factor alpha-dependent pathway. Pharmacology. 2018;101(3–4):111–119. doi:10.1159/000481571
  • Yang J-Y, Della-Fera MA, Rayalam S, Baile CA. Effect of xanthohumol and isoxanthohumol on 3T3-L1 cell apoptosis and adipogenesis. Apoptosis. 2007;12(11):1953–1963. doi:10.1007/s10495-007-0130-4
  • Yang JY, Della-Fera MA, Nelson-Dooley C, Baile CA. Molecular mechanisms of apoptosis induced by ajoene in 3T3-L1 adipocytes. Obesity (Silver Spring, Md). 2006;14(3):388–397. doi:10.1038/oby.2006.52
  • Rayalam S, Yang JY, Ambati S, Della-Fera MA, Baile CA. Resveratrol induces apoptosis and inhibits adipogenesis in 3T3-L1 adipocytes. Phytother Res. 2008;22:1367–1371. doi:10.1002/ptr.2503
  • Ambati S, Yang JY, Rayalam S, Park HJ, Della-Fera MA, Baile CA. Ajoene exerts potent effects in 3T3-L1 adipocytes by inhibiting adipogenesis and inducing apoptosis. Phytother Res. 2009;23(4):513–518. doi:10.1002/ptr.2663
  • Qi R, Huang J, Wang Q, et al. MicroRNA-224-5p regulates adipocyte apoptosis induced by TNFalpha via controlling NF-kappaB activation. J Cell Physiol. 2018;233:1236–1246. doi:10.1002/jcp.25992
  • Henderson PW, Singh SP, Weinstein AL, et al. Therapeutic metabolic inhibition: hydrogen sulfide significantly mitigates skeletal muscle ischemia reperfusion injury in vitro and in vivo. Plast Reconstr Surg. 2010;126(6):1890–1898. doi:10.1097/PRS.0b013e3181f446bc
  • Henderson PW, Singh SP, Belkin D, et al. Hydrogen sulfide protects against ischemia-reperfusion injury in an in vitro model of cutaneous tissue transplantation. J Surg Res. 2010;159(1):451–455. doi:10.1016/j.jss.2009.05.010
  • Aykan A, Ozturk S, Sahin I, Avcu F, Sagkan RI, Isik S. The effects of hydrogen sulfide on adipocyte viability in human adipocyte and adipocyte-derived mesenchymal stem cell cultures under ischemic conditions. Ann Plast Surg. 2015;75(6):657–665. doi:10.1097/SAP.0000000000000595
  • Powell CR, Dillon KM, Matson JB. A review of hydrogen sulfide (H(2)S) donors: chemistry and potential therapeutic applications. Biochem Pharmacol. 2018;149:110–123. doi:10.1016/j.bcp.2017.11.014
  • Zhao S, Song T, Gu Y, et al. Hydrogen sulfide alleviates liver injury via S-sulfhydrated-Keap1/Nrf2/LRP1 pathway. Hepatology (Baltimore, Md). 2020.
  • Nin DS, Idres SB, Song ZJ, Moore PK, Deng LW. Biological effects of morpholin-4-Ium 4 Methoxyphenyl (Morpholino) phosphinodithioate and other phosphorothioate-based hydrogen sulfide donors. Antioxid Redox Signal. 2020;32(2):145–158. doi:10.1089/ars.2019.7896
  • Bayan L, Koulivand PH, Gorji A. Garlic: a review of potential therapeutic effects. Avicenna J Phytomed. 2014;4(1):1–14.
  • Stein A, Bailey SM. Redox biology of hydrogen sulfide: implications for physiology, pathophysiology, and pharmacology. Redox Biol. 2013;1(1):32–39. doi:10.1016/j.redox.2012.11.006