MZe786 Rescues Cardiac Mitochondrial Activity in High sFlt-1 and Low HO-1 Environment
Abstract
1. Introduction
2. Materials and Methods
2.1. Adenovirus Preparation
2.2. Animal Studies
2.3. Drug Preparation
2.4. Animal Experimental Protocol
2.5. Isolation of Mitochondria
2.6. Mitochondrial Respiration Assays
2.7. Quantitative Real-Time PCR
2.8. Statistical Analysis
3. Results
3.1. Loss of HO-1 Disturb the Cardiac Mitochondrial Respiration
3.2. MZe786 Improves Cardiac Mitochondrial Biogenesis Signal and Stimulates Antioxidant Gene Transcription in Hmox1 Knockout Mice
3.3. MZe786 Rescues the sFlt-1-Induced Inhibition of the Cardiac Mitochondrial Activity in Hmox1+/− Mice
3.4. MZe786 Stimulates the Cardiac Mitochondrial Biogenesis and Antioxidant Defence in Hmox1+/− Mice Exposed to High sFlt-1 Environment
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Schindler, A.E. New data about preeclampsia: Some possibilities of prevention. Gynecol. Endocrinol. 2018, 34, 636–637. [Google Scholar] [CrossRef] [PubMed]
- Kuklina, E.V.; Ayala, C.; Callaghan, W.M. Hypertensive disorders and severe obstetric morbidity in the United States. Obstet. Gynecol. 2009, 113, 1299–1306. [Google Scholar] [CrossRef]
- Wilson, M.L.; Goodwin, T.M.; Pan, V.L.; Ingles, S.A. Molecular epidemiology of preeclampsia. Obstet. Gynecol. Surv. 2003, 58, 39–66. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Tsigas, E.Z.; Callaghan, W.M. Health and economic burden of preeclampsia: No time for complacency. Am. J. Obstet. Gynecol. 2017, 217, 235–236. [Google Scholar] [CrossRef] [PubMed]
- Shih, T.; Peneva, D.; Xu, X.; Sutton, A.; Triche, E.; Ehrenkranz, R.A.; Paidas, M.; Stevens, W. The Rising Burden of Preeclampsia in the United States Impacts Both Maternal and Child Health. Am. J. Perinatol. 2016, 33, 329–338. [Google Scholar] [PubMed]
- Kelly, B.B.; Narula, J.; Fuster, V. Recognizing global burden of cardiovascular disease and related chronic diseases. Mt. Sinai J. Med. 2012, 79, 632–640. [Google Scholar] [CrossRef]
- Trogdon, J.G.; Finkelstein, E.A.; Nwaise, I.A.; Tangka, F.K.; Orenstein, D. The economic burden of chronic cardiovascular disease for major insurers. Health Promot. Pract. 2007, 8, 234–242. [Google Scholar] [CrossRef]
- Finegold, J.A.; Asaria, P.; Francis, D.P. Mortality from ischaemic heart disease by country, region, and age: Statistics from World Health Organisation and United Nations. Int. J. Cardiol. 2013, 168, 934–945. [Google Scholar] [CrossRef]
- Bellamy, L.; Casas, J.P.; Hingorani, A.D.; Williams, D.J. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: Systematic review and meta-analysis. BMJ 2007, 335, 974. [Google Scholar] [CrossRef]
- Honigberg, M.C.; Zekavat, S.M.; Aragam, K.; Klarin, D.; Bhatt, D.L.; Scott, N.S.; Peloso, G.M.; Natarajan, P. Long-Term Cardiovascular Risk in Women with Hypertension During Pregnancy. J. Am. Coll. Cardiol. 2019, 74, 2743–2754. [Google Scholar] [CrossRef]
- Leon, L.J.; McCarthy, F.P.; Direk, K.; Gonzalez-Izquierdo, A.; Prieto-Merino, D.; Casas, J.P.; Chappell, L. Preeclampsia and Cardiovascular Disease in a Large UK Pregnancy Cohort of Linked Electronic Health Records: A CALIBER Study. Circulation 2019, 140, 1050–1060. [Google Scholar] [CrossRef] [PubMed]
- Craici, I.; Wagner, S.; Garovic, V.D. Preeclampsia and future cardiovascular risk: Formal risk factor or failed stress test? Ther. Adv. Cardiovasc. Dis. 2008, 2, 249–259. [Google Scholar] [CrossRef] [PubMed]
- Irgens, H.U.; Reisaeter, L.; Irgens, L.M.; Lie, R.T. Long term mortality of mothers and fathers after pre-eclampsia: Population based cohort study. BMJ 2001, 323, 1213–1217. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, A. Heparin-binding angiogenic growth factors in pregnancy: A review. Placenta 1997, 18, 215–258. [Google Scholar] [CrossRef]
- Levine, R.J.; Maynard, S.E.; Qian, C.; Lim, K.H.; England, L.J.; Yu, K.F.; Schisterman, E.F.; Thadhani, R.; Sachs, D.P.; Epstein, F.H.; et al. Circulating angiogenic factors and the risk of preeclampsia. N. Engl. J. Med. 2004, 350, 672–683. [Google Scholar] [CrossRef]
- Maynard, S.E.; Venkatesha, S.; Thadhani, R.; Karumanchi, S.A. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res. 2005, 57 Pt 2, 1R–7R. [Google Scholar] [CrossRef]
- Cindrova-Davies, T.; Sanders, D.A.; Burton, G.J.; Charnock-Jones, D.S. Soluble FLT1 sensitizes endothelial cells to inflammatory cytokines by antagonizing VEGF receptor-mediated signalling. Cardiovasc. Res. 2011, 89, 671–679. [Google Scholar] [CrossRef]
- Lou, W.Z.; Jiang, F.; Hu, J.; Chen, X.X.; Song, Y.N.; Zhou, X.Y.; Liu, J.; Bian, X.; Gao, J. Maternal Serum Angiogenic Factor sFlt-1 to PlGF Ratio in Preeclampsia: A Useful Marker for Differential Diagnosis and Prognosis Evaluation in Chinese Women. Dis. Markers 2019, 2019, 6270187. [Google Scholar] [CrossRef]
- Lehnen, H.; Mosblech, N.; Reineke, T.; Puchooa, A.; Menke-Mollers, I.; Zechner, U.; Gembruch, U. Prenatal Clinical Assessment of sFlt-1 (Soluble fms-like Tyrosine Kinase-1)/PlGF (Placental Growth Factor) Ratio as a Diagnostic Tool for Preeclampsia, Pregnancy-induced Hypertension, and Proteinuria. Geburtshilfe Frauenheilkd. 2013, 73, 440–445. [Google Scholar] [CrossRef]
- Palmer, K.R.; Kaitu’u-Lino, T.J.; Hastie, R.; Hannan, N.J.; Ye, L.; Binder, N.; Cannon, P.; Tuohey, L.; Johns, T.G.; Shub, A.; et al. Placental-Specific sFLT-1 e15a Protein Is Increased in Preeclampsia, Antagonizes Vascular Endothelial Growth Factor Signaling, and Has Antiangiogenic Activity. Hypertension 2015, 66, 1251–1259. [Google Scholar] [CrossRef]
- Cudmore, M.; Ahmad, S.; Al-Ani, B.; Fujisawa, T.; Coxall, H.; Chudasama, K.; Devey, L.R.; Wigmore, S.J.; Abbas, A.; Hewett, P.W.; et al. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 2007, 115, 1789–1797. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, A.; Rezai, H.; Broadway-Stringer, S. Evidence-Based Revised View of the Pathophysiology of Preeclampsia. Adv. Exp. Med. Biol. 2017, 956, 355–374. [Google Scholar] [PubMed]
- Wikstrom, A.K.; Larsson, A.; Eriksson, U.J.; Nash, P.; Olovsson, M. Early postpartum changes in circulating pro- and anti-angiogenic factors in early-onset and late-onset pre-eclampsia. Acta Obstet. Gynecol. Scand. 2008, 87, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Saleh, L.; Samantar, R.; Garrelds, I.M.; van den Meiracker, A.H.; Visser, W.; Danser, A.H.J. Low Soluble Fms-Like Tyrosine Kinase-1, Endoglin, and Endothelin-1 Levels in Women with Confirmed or Suspected Preeclampsia Using Proton Pump Inhibitors. Hypertension 2017, 70, 594–600. [Google Scholar] [CrossRef] [PubMed]
- Akhter, T.; Wikstrom, A.K.; Larsson, M.; Larsson, A.; Wikstrom, G.; Naessen, T. Association between angiogenic factors and signs of arterial aging in women with pre-eclampsia. Ultrasound Obstet. Gynecol. 2017, 50, 93–99. [Google Scholar] [CrossRef]
- Yet, S.F.; Layne, M.D.; Liu, X.; Chen, Y.H.; Ith, B.; Sibinga, N.E.; Perrella, M.A. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003, 17, 1759–1761. [Google Scholar] [CrossRef]
- Liu, X.; Wei, J.; Peng, D.H.; Layne, M.D.; Yet, S.F. Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 2005, 54, 778–784. [Google Scholar] [CrossRef]
- Yet, S.F.; Tian, R.; Layne, M.D.; Wang, Z.Y.; Maemura, K.; Solovyeva, M.; Ith, B.; Melo, L.G.; Zhang, L.; Ingwall, J.S.; et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ. Res. 2001, 89, 168–173. [Google Scholar] [CrossRef]
- Hull, T.D.; Boddu, R.; Guo, L.; Tisher, C.C.; Traylor, A.M.; Patel, B.; Joseph, R.; Prabhu, S.D.; Suliman, H.D.; Piantadosi, C.A.; et al. Heme oxygenase-1 regulates mitochondrial quality control in the heart. JCI Insight 2016, 1, e85817. [Google Scholar] [CrossRef]
- Huang, C.W.; Moore, P.K. H2S Synthesizing Enzymes: Biochemistry and Molecular Aspects. Handb. Exp. Pharmacol. 2015, 230, 3–25. [Google Scholar]
- Suzuki, K.; Olah, G.; Modis, K.; Coletta, C.; Kulp, G.; Gero, D.; Szoleczky, P.; Chang, T.; Zhou, Z.; Wu, L.; et al. Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc. Natl. Acad. Sci. USA 2011, 108, 13829–13834. [Google Scholar] [CrossRef] [PubMed]
- Yong, Q.C.; Choo, C.H.; Tan, B.H.; Low, C.M.; Bian, J.S. Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem. Int. 2010, 56, 508–515. [Google Scholar] [CrossRef] [PubMed]
- Cheung, S.H.; Lau, J.Y.W. Hydrogen sulfide mediates athero-protection against oxidative stress via S-sulfhydration. PLoS ONE 2018, 13, e0194176. [Google Scholar] [CrossRef] [PubMed]
- Shao, M.; Zhuo, C.; Jiang, R.; Chen, G.; Shan, J.; Ping, J.; Tian, H.; Wang, L.; Lin, C.; Hu, L. Protective effect of hydrogen sulphide against myocardial hypertrophy in mice. Oncotarget 2017, 8, 22344–22352. [Google Scholar] [CrossRef]
- Zhao, W.; Zhang, J.; Lu, Y.; Wang, R. The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J. 2001, 20, 6008–6016. [Google Scholar] [CrossRef]
- Zanardo, R.C.; Brancaleone, V.; Distrutti, E.; Fiorucci, S.; Cirino, G.; Wallace, J.L. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006, 20, 2118–2120. [Google Scholar] [CrossRef]
- Elrod, J.W.; Calvert, J.W.; Morrison, J.; Doeller, J.E.; Kraus, D.W.; Tao, L.; Jiao, X.; Scalia, R.; Kiss, L.; Szabo, C.; et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc. Natl. Acad. Sci. USA 2007, 104, 15560–15565. [Google Scholar] [CrossRef]
- Papapetropoulos, A.; Pyriochou, A.; Altaany, Z.; Yang, G.; Marazioti, A.; Zhou, Z.; Jeschke, M.G.; Branski, L.K.; Herndon, D.N.; Wang, R.; et al. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106, 21972–21977. [Google Scholar] [CrossRef]
- Giuffre, A.; Vicente, J.B. Hydrogen Sulfide Biochemistry and Interplay with Other Gaseous Mediators in Mammalian Physiology. Oxid. Med. Cell Longev. 2018, 2018, 6290931. [Google Scholar] [CrossRef]
- D’Araio, E.; Shaw, N.; Millward, A.; Demaine, A.; Whiteman, M.; Hodgkinson, A. Hydrogen sulfide induces heme oxygenase-1 in human kidney cells. Acta Diabetol. 2014, 51, 155–157. [Google Scholar] [CrossRef] [PubMed]
- Zhang, C.Y.; Li, X.H.; Zhang, T.; Fu, J.; Cui, X.D. Hydrogen sulfide upregulates heme oxygenase-1 expression in rats with volume overload-induced heart failure. Biomed. Rep. 2013, 1, 454–458. [Google Scholar] [CrossRef] [PubMed]
- Sparatore, A.; Perrino, E.; Tazzari, V.; Giustarini, D.; Rossi, R.; Rossoni, G.; Erdmann, K.; Schröder, H.; Del Soldato, P. Pharmacological profile of a novel H(2)S-releasing aspirin. Free Radic. Biol. Med. 2009, 46, 586–592. [Google Scholar] [CrossRef] [PubMed]
- Rossoni, G.; Manfredi, B.; Tazzari, V.; Sparatore, A.; Trivulzio, S.; Del Soldato, P.; Berti, F. Activity of a new hydrogen sulfide-releasing aspirin (ACS14) on pathological cardiovascular alterations induced by glutathione depletion in rats. Eur. J. Pharmacol. 2010, 648, 139–145. [Google Scholar] [CrossRef] [PubMed]
- Giustarini, D.; Del Soldato, P.; Sparatore, A.; Rossi, R. Modulation of thiol homeostasis induced by H2S-releasing aspirin. Free Radic. Biol. Med. 2010, 48, 1263–1272. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Aranguren, L.C.; Espinosa-Gonzalez, C.T.; Gonzalez-Ortiz, L.M.; Sanabria-Barrera, S.M.; Riano-Medina, C.E.; Nunez, A.F.; Ahmed, A.; Vasquez-Vivar, J.; López, M. Soluble Fms-Like Tyrosine Kinase-1 Alters Cellular Metabolism and Mitochondrial Bioenergetics in Preeclampsia. Front. Physiol. 2018, 9, 83. [Google Scholar] [CrossRef]
- Ky, B.; French, B.; Ruparel, K.; Sweitzer, N.K.; Fang, J.C.; Levy, W.C.; Sawyer, D.B.; Cappola, T.P. The vascular marker soluble fms-like tyrosine kinase 1 is associated with disease severity and adverse outcomes in chronic heart failure. J. Am. Coll. Cardiol. 2011, 58, 386–394. [Google Scholar] [CrossRef]
- Gruson, D.; Hermans, M.P.; Ferracin, B.; Ahn, S.A.; Rousseau, M.F. Sflt-1 in heart failure: Relation with disease severity and biomarkers. Scand. J. Clin. Lab. Investig. 2016, 76, 411–416. [Google Scholar] [CrossRef] [PubMed]
- Sakamuri, S.; Sperling, J.A.; Sure, V.N.; Dholakia, M.H.; Peterson, N.R.; Rutkai, I.; Mahalingam, P.S.; Satou, R.; Katakam, P.V.G. Measurement of respiratory function in isolated cardiac mitochondria using Seahorse XFe24 Analyzer: Applications for aging research. Geroscience 2018, 40, 347–356. [Google Scholar] [CrossRef]
- Boutagy, N.E.; Rogers, G.W.; Pyne, E.S.; Ali, M.M.; Hulver, M.W.; Frisard, M.I. Using Isolated Mitochondria from Minimal Quantities of Mouse Skeletal Muscle for High throughput Microplate Respiratory Measurements. J. Vis. Exp. 2015, 104, e53216. [Google Scholar] [CrossRef]
- Brand, M.D.; Nicholls, D.G. Assessing mitochondrial dysfunction in cells. Biochem. J. 2011, 435, 297–312. [Google Scholar] [CrossRef]
- Quiros, P.M.; Goyal, A.; Jha, P.; Auwerx, J. Analysis of mtDNA/nDNA Ratio in Mice. Curr. Protoc. Mouse Biol. 2017, 7, 47–54. [Google Scholar] [CrossRef] [PubMed]
- Siasos, G.; Tsigkou, V.; Kosmopoulos, M.; Theodosiadis, D.; Simantiris, S.; Tagkou, N.M.; Tsimpiktsioglou, A.; Stampouloglou, P.K.; Oikonomou, E.; Mourouzis, K.; et al. Mitochondria and cardiovascular diseases-from pathophysiology to treatment. Ann. Transl. Med. 2018, 6, 256. [Google Scholar]
- Arany, Z.; He, H.; Lin, J.; Hoyer, K.; Handschin, C.; Toka, O.; Ahmad, F.; Matsui, T.; Chin, S.; Wu, H.; et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005, 1, 259–271. [Google Scholar] [CrossRef] [PubMed]
- Riehle, C.; Abel, E.D. PGC-1 proteins and heart failure. Trends Cardiovasc. Med. 2012, 22, 98–105. [Google Scholar] [CrossRef]
- Lu, Z.; Xu, X.; Hu, X.; Fassett, J.; Zhu, G.; Tao, Y.; Li, J.; Huang, Y.; Zhang, P.; Zhao, B.; et al. PGC-1 alpha regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid. Redox Signal. 2010, 13, 1011–1022. [Google Scholar] [CrossRef] [PubMed]
- Zhao, H.; Azuma, J.; Kalish, F.; Wong, R.J.; Stevenson, D.K. Maternal heme oxygenase 1 regulates placental vasculature development via angiogenic factors in mice. Biol. Reprod. 2011, 85, 1005–1012. [Google Scholar] [CrossRef] [PubMed]
- Bushnell, C.; McCullough, L.D.; Awad, I.A.; Chireau, M.V.; Fedder, W.N.; Furie, K.L.; Howard, V.J.; Lichtman, J.H.; Lisabeth, L.D.; Piña, I.L.; et al. Guidelines for the prevention of stroke in women: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2014, 45, 1545–1588. [Google Scholar] [CrossRef]
- Brown, M.C.; Best, K.E.; Pearce, M.S.; Waugh, J.; Robson, S.C.; Bell, R. Cardiovascular disease risk in women with pre-eclampsia: Systematic review and meta-analysis. Eur. J. Epidemiol. 2013, 28, 1–19. [Google Scholar] [CrossRef]
- Lykke, J.A.; Langhoff-Roos, J.; Sibai, B.M.; Funai, E.F.; Triche, E.W.; Paidas, M.J. Hypertensive pregnancy disorders and subsequent cardiovascular morbidity and type 2 diabetes mellitus in the mother. Hypertension 2009, 53, 944–951. [Google Scholar] [CrossRef]
- Wu, P.; Haththotuwa, R.; Kwok, C.S.; Babu, A.; Kotronias, R.A.; Rushton, C. Preeclampsia and Future Cardiovascular Health: A Systematic Review and Meta-Analysis. Circ. Cardiovasc. Qual. Outcomes 2017, 10, e003497. [Google Scholar] [CrossRef]
- McDonald, S.D.; Malinowski, A.; Zhou, Q.; Yusuf, S.; Devereaux, P.J. Cardiovascular sequelae of preeclampsia/eclampsia: A systematic review and meta-analyses. Am. Heart, J. 2008, 156, 918–930. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, A.; Rahman, M.; Zhang, X.; Acevedo, C.H.; Nijjar, S.; Rushton, I.; Bussolati, B.; St. John, J. Induction of placental heme oxygenase-1 is protective against TNFalpha-induced cytotoxicity and promotes vessel relaxation. Mol. Med. 2000, 6, 391–409. [Google Scholar] [CrossRef] [PubMed]
- Zenclussen, M.L.; Linzke, N.; Schumacher, A.; Fest, S.; Meyer, N.; Casalis, P.A. Heme oxygenase-1 is critically involved in placentation, spiral artery remodeling, and blood pressure regulation during murine pregnancy. Front. Pharmacol. 2014, 5, 291. [Google Scholar] [CrossRef] [PubMed]
- Kaartokallio, T.; Utge, S.; Klemetti, M.M.; Paananen, J.; Pulkki, K.; Romppanen, J. Fetal Microsatellite in the Heme Oxygenase 1 Promoter Is Associated With Severe and Early-Onset Preeclampsia. Hypertension 2018, 71, 95–102. [Google Scholar] [CrossRef]
- Lancel, S.; Hassoun, S.M.; Favory, R.; Decoster, B.; Motterlini, R.; Neviere, R. Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J. Pharmacol. Exp. Ther. 2009, 329, 641–648. [Google Scholar] [CrossRef]
- Stanley, W.C.; Recchia, F.A.; Lopaschuk, G.D. Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev. 2005, 85, 1093–1129. [Google Scholar] [CrossRef]
- Wisneski, J.A.; Gertz, E.W.; Neese, R.A.; Gruenke, L.D.; Morris, D.L.; Craig, J.C. Metabolic fate of extracted glucose in normal human myocardium. J. Clin. Investig. 1985, 76, 1819–1827. [Google Scholar] [CrossRef]
- McCommis, K.S.; Finck, B.N. Mitochondrial pyruvate transport: A historical perspective and future research directions. Biochem. J. 2015, 466, 443–454. [Google Scholar] [CrossRef]
- Fillmore, N.; Mori, J.; Lopaschuk, G.D. Mitochondrial fatty acid oxidation alterations in heart failure, ischaemic heart disease and diabetic cardiomyopathy. Br. J. Pharmacol. 2014, 171, 2080–2090. [Google Scholar] [CrossRef]
- Pfleger, J.; He, M.; Abdellatif, M. Mitochondrial complex II is a source of the reserve respiratory capacity that is regulated by metabolic sensors and promotes cell survival. Cell Death Dis. 2015, 6, e1835. [Google Scholar] [CrossRef]
- Maynard, S.E.; Min, J.Y.; Merchan, J.; Lim, K.H.; Li, J.; Mondal, S.; Libermann, T.A.; Morgan, J.P.; Sellke, F.W.; Stillman, I.E.; et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Investig. 2003, 111, 649–658. [Google Scholar] [CrossRef]
- Jiang, Z.; Zou, Y.; Ge, Z.; Zuo, Q.; Huang, S.Y.; Sun, L. A Role of sFlt-1 in Oxidative Stress and Apoptosis in Human and Mouse Pre-Eclamptic Trophoblasts. Biol. Reprod. 2015, 93, 73. [Google Scholar] [CrossRef]
- Nandi, S.; Ravindran, S.; Kurian, G.A. Role of endogenous hydrogen sulfide in cardiac mitochondrial preservation during ischemia reperfusion injury. Biomed. Pharmacother. 2018, 97, 271–279. [Google Scholar] [CrossRef]
- Shimizu, Y.; Polavarapu, R.; Eskla, K.L.; Nicholson, C.K.; Koczor, C.A.; Wang, R.; Lewis, W.; Shiva, S.; Lefer, D.J.; Calvert, J.W. Hydrogen sulfide regulates cardiac mitochondrial biogenesis via the activation of AMPK. J. Mol. Cell Cardiol. 2018, 116, 29–40. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Shen, Z.; Luo, S.; Guo, W.; Zhu, Y.Z. The Cardioprotective Effects of Hydrogen Sulfide in Heart Diseases: From Molecular Mechanisms to Therapeutic Potential. Oxid. Med. Cell Longev. 2015, 2015, 925167. [Google Scholar] [CrossRef] [PubMed]
- Guo, W.; Kan, J.T.; Cheng, Z.Y.; Chen, J.F.; Shen, Y.Q.; Xu, J.; Wu, D.; Zhu, Y. Hydrogen sulfide as an endogenous modulator in mitochondria and mitochondria dysfunction. Oxid. Med. Cell Longev. 2012, 2012, 878052. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Xie, L.; Gu, Y.; Wen, M.; Zhao, S.; Wang, W.; Ma, Y.; Meng, G.; Han, Y.; Wang, Y.; Liu, G.; et al. Hydrogen Sulfide Induces Keap1 S-sulfhydration and Suppresses Diabetes-Accelerated Atherosclerosis via Nrf2 Activation. Diabetes 2016, 65, 3171–3184. [Google Scholar] [CrossRef]
- Shin, I.; Hong, J.; Jeon, C.M.; Shin, N.R.; Kwon, O.K.; Kim, H.S.; Kim, J.C.; Oh, S.R.; Ahn, K.S. Diallyl-disulfide, an organosulfur compound of garlic, attenuates airway inflammation via activation of the Nrf-2/HO-1 pathway and NF-kappaB suppression. Food Chem. Toxicol. 2013, 62, 506–513. [Google Scholar] [CrossRef]
- Wang, R.; Szabo, C.; Ichinose, F.; Ahmed, A.; Whiteman, M.; Papapetropoulos, A. The role of H2S bioavailability in endothelial dysfunction. Trends Pharmacol. Sci. 2015, 36, 568–578. [Google Scholar] [CrossRef]
- Wang, K.; Ahmad, S.; Cai, M.; Rennie, J.; Fujisawa, T.; Crispi, F.; Baily, J.; Miller, M.R.; Cudmore, M.; Hadoke, P.W.F.; et al. Dysregulation of hydrogen sulfide producing enzyme cystathionine gamma-lyase contributes to maternal hypertension and placental abnormalities in preeclampsia. Circulation 2013, 127, 2514–2522. [Google Scholar] [CrossRef]
- Lu, F.; Xing, J.; Zhang, X.; Dong, S.; Zhao, Y.; Wang, L.; Li, H.; Yang, F.; Xu, C.; Zhang, W. Exogenous hydrogen sulfide prevents cardiomyocyte apoptosis from cardiac hypertrophy induced by isoproterenol. Mol. Cell Biochem. 2013, 381, 41–50. [Google Scholar] [CrossRef] [PubMed]
- Karwi, Q.G.; Bornbaum, J.; Boengler, K.; Torregrossa, R.; Whiteman, M.; Wood, M.E.; Schulz, R.; Baxter, G.F. AP39, a mitochondria-targeting hydrogen sulfide (H2 S) donor, protects against myocardial reperfusion injury independently of salvage kinase signalling. Br. J. Pharmacol. 2017, 174, 287–301. [Google Scholar] [CrossRef] [PubMed]
- Holwerda, K.M.; Burke, S.D.; Faas, M.M.; Zsengeller, Z.; Stillman, I.E.; Kang, P.M.; van Goor, H.; McCurley, A.; Jaffe, I.Z.; Karumanchi, S.A.; et al. Hydrogen sulfide attenuates sFlt1-induced hypertension and renal damage by upregulating vascular endothelial growth factor. J. Am. Soc. Nephrol. 2014, 25, 717–725. [Google Scholar] [CrossRef] [PubMed]
- Bos, E.M.; van Goor, H.; Joles, J.A.; Whiteman, M.; Leuvenink, H.G. Hydrogen sulfide: Physiological properties and therapeutic potential in ischaemia. Br. J. Pharmacol. 2015, 172, 1479–1493. [Google Scholar] [CrossRef] [PubMed]
- Nicholson, C.K.; Lambert, J.P.; Molkentin, J.D.; Sadoshima, J.; Calvert, J.W. Thioredoxin 1 is essential for sodium sulfide-mediated cardioprotection in the setting of heart failure. Arterioscler Arterioscler. Thromb. Vasc. Biol. 2013, 33, 744–751. [Google Scholar] [CrossRef]
- Matsui, R.; Ferran, B.; Oh, A.; Croteau, D.; Shao, D.; Han, J.; Pimentel, D.R.; Bachschmid, M.M. Redox Regulation via Glutaredoxin-1 and Protein S-Glutathionylation. Antioxid Redox Signal. 2020, 32, 677–700. [Google Scholar] [CrossRef]
- Gallogly, M.M.; Shelton, M.D.; Qanungo, S.; Pai, H.V.; Starke, D.W.; Hoppel, C.L.; Lesnefsky, E.J.; Mieyal, J.J. Glutaredoxin regulates apoptosis in cardiomyocytes via NFkappaB targets Bcl-2 and Bcl-xL: Implications for cardiac aging. Antioxid Redox Signal. 2010, 12, 1339–1353. [Google Scholar] [CrossRef]
- Pai, H.V.; Starke, D.W.; Lesnefsky, E.J.; Hoppel, C.L.; Mieyal, J.J. What is the functional significance of the unique location of glutaredoxin 1 (GRx1) in the intermembrane space of mitochondria? Antioxid Redox Signal. 2007, 9, 2027–2033. [Google Scholar] [CrossRef]
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Sanchez-Aranguren, L.C.; Rezai, H.; Ahmad, S.; Alzahrani, F.A.; Sparatore, A.; Wang, K.; Ahmed, A. MZe786 Rescues Cardiac Mitochondrial Activity in High sFlt-1 and Low HO-1 Environment. Antioxidants 2020, 9, 598. https://doi.org/10.3390/antiox9070598
Sanchez-Aranguren LC, Rezai H, Ahmad S, Alzahrani FA, Sparatore A, Wang K, Ahmed A. MZe786 Rescues Cardiac Mitochondrial Activity in High sFlt-1 and Low HO-1 Environment. Antioxidants. 2020; 9(7):598. https://doi.org/10.3390/antiox9070598
Chicago/Turabian StyleSanchez-Aranguren, Lissette Carolina, Homira Rezai, Shakil Ahmad, Faisal A. Alzahrani, Anna Sparatore, Keqing Wang, and Asif Ahmed. 2020. "MZe786 Rescues Cardiac Mitochondrial Activity in High sFlt-1 and Low HO-1 Environment" Antioxidants 9, no. 7: 598. https://doi.org/10.3390/antiox9070598
APA StyleSanchez-Aranguren, L. C., Rezai, H., Ahmad, S., Alzahrani, F. A., Sparatore, A., Wang, K., & Ahmed, A. (2020). MZe786 Rescues Cardiac Mitochondrial Activity in High sFlt-1 and Low HO-1 Environment. Antioxidants, 9(7), 598. https://doi.org/10.3390/antiox9070598