OP2113, a new drug for chronic hypoxia-induced pulmonary hypertension treatment in rat.
oxidative stress
pulmonary circulation
pulmonary hypertension
right ventricle
Journal
British journal of pharmacology
ISSN: 1476-5381
Titre abrégé: Br J Pharmacol
Pays: England
ID NLM: 7502536
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
02
06
2023
received:
15
11
2022
accepted:
13
06
2023
medline:
23
10
2023
pubmed:
23
6
2023
entrez:
23
6
2023
Statut:
ppublish
Résumé
Pulmonary hypertension (PH) is a cardiovascular disease characterised by an increase in pulmonary arterial (PA) resistance leading to right ventricular (RV) failure. Reactive oxygen species (ROS) play a major role in PH. OP2113 is a drug with beneficial effects on cardiac injuries that targets mitochondrial ROS. The aim of the study was to address the in vivo therapeutic effect of OP2113 in PH. PH was induced by 3 weeks of chronic hypoxia (CH-PH) in rats treated with OP2113 or its vehicle via subcutaneous osmotic mini-pumps. Haemodynamic parameters and both PA and heart remodelling were assessed. Reactivity was quantified in PA rings and in RV or left ventricular (LV) cardiomyocytes. Oxidative stress was detected by electron paramagnetic resonance and western blotting. Mitochondrial mass and respiration were measured by western blotting and oxygraphy, respectively. In CH-PH rats, OP2113 reduced the mean PA pressure, PA remodelling, PA hyperreactivity in response to 5-HT, the contraction slowdown in RV and LV and increased the mitochondrial mass in RV. Interestingly, OP2113 had no effect on haemodynamic parameters, both PA and RV wall thickness and PA reactivity, in control rats. Whereas oxidative stress was evidenced by an increase in protein carbonylation in CH-PH, this was not affected by OP2113. Our study provides evidence for a selective protective effect of OP2113 in vivo on alterations in both PA and RV from CH-PH rats without side effects in control rats.
Sections du résumé
BACKGROUND AND PURPOSE
Pulmonary hypertension (PH) is a cardiovascular disease characterised by an increase in pulmonary arterial (PA) resistance leading to right ventricular (RV) failure. Reactive oxygen species (ROS) play a major role in PH. OP2113 is a drug with beneficial effects on cardiac injuries that targets mitochondrial ROS. The aim of the study was to address the in vivo therapeutic effect of OP2113 in PH.
EXPERIMENTAL APPROACH
PH was induced by 3 weeks of chronic hypoxia (CH-PH) in rats treated with OP2113 or its vehicle via subcutaneous osmotic mini-pumps. Haemodynamic parameters and both PA and heart remodelling were assessed. Reactivity was quantified in PA rings and in RV or left ventricular (LV) cardiomyocytes. Oxidative stress was detected by electron paramagnetic resonance and western blotting. Mitochondrial mass and respiration were measured by western blotting and oxygraphy, respectively.
KEY RESULTS
In CH-PH rats, OP2113 reduced the mean PA pressure, PA remodelling, PA hyperreactivity in response to 5-HT, the contraction slowdown in RV and LV and increased the mitochondrial mass in RV. Interestingly, OP2113 had no effect on haemodynamic parameters, both PA and RV wall thickness and PA reactivity, in control rats. Whereas oxidative stress was evidenced by an increase in protein carbonylation in CH-PH, this was not affected by OP2113.
CONCLUSION AND IMPLICATIONS
Our study provides evidence for a selective protective effect of OP2113 in vivo on alterations in both PA and RV from CH-PH rats without side effects in control rats.
Substances chimiques
Reactive Oxygen Species
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2802-2821Informations de copyright
© 2023 The Authors. British Journal of Pharmacology published by John Wiley & Sons Ltd on behalf of British Pharmacological Society.
Références
Agrawal, V., Lahm, T., Hansmann, G., & Hemnes, A. R. (2020). Molecular mechanisms of right ventricular dysfunction in pulmonary arterial hypertension: Focus on the coronary vasculature, sex hormones, and glucose/lipid metabolism. Cardiovascular Diagnosis and Therapy, 10(5), 1522-1540. https://doi.org/10.21037/cdt-20-404
Alexander, S. P., Christopoulos, A., Davenport, A. P., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Abbracchio, M. P., & CGTP Collaborators. (2021). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: G protein-coupled receptors. British Journal of Pharmacology, 178(S1), S27-S156. https://doi.org/10.1111/bph.15538
Alexander, S. P., Fabbro, D., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Annett, S., Boison, D., Burns, K. E., Dessauer, C., Gertsch, J., Helsby, N. A., Izzo, A. A., … Wong, S. S. (2021). The Concise Guide to PHARMACOLOGY 2021/22: Enzymes. British Journal of Pharmacology, 178(Suppl 1), S313-S411. https://doi.org/10.1111/bph.15542
Alexander, S. P., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Buneman, O. P., Cidlowski, J. A., Christopoulos, A., Davenport, A. P., Fabbro, D., Spedding, M., Striessnig, J., Davies, J. A., Ahlers-Dannen, K. E., … Zolghadri, Y. (2021). The Concise Guide to PHARMACOLOGY 2021/22: Introduction and other protein targets. British Journal of Pharmacology, 178(Suppl 1), S1-S26. https://doi.org/10.1111/bph.15537
Alexander, S. P., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Amarosi, L., Anderson, C. M. H., Beart, P. M., Broer, S., Dawson, P. A., Hagenbuch, B., Hammond, J. R., Inui, K.-i., … Verri, T. (2021). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: Transporters. British Journal of Pharmacology, 178(S1), S412-S513. https://doi.org/10.1111/bph.15543
Alexander, S. P., Mathie, A., Peters, J. A., Veale, E. L., Striessnig, J., Kelly, E., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Aldrich, R. W., Attali, B., Baggetta, A. M., Becirovic, E., Biel, M., Bill, R. M., Catterall, W. A., … Zhu, M. (2021). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: Ion channels. British Journal of Pharmacology, 178(S1), S157-S245. https://doi.org/10.1111/bph.15539
Alexander, S. P. H., Roberts, R. E., Broughton, B. R. S., Sobey, C. G., George, C. H., Stanford, S. C., Cirino, G., Docherty, J. R., Giembycz, M. A., Hoyer, D., Insel, P. A., Izzo, A. A., Ji, Y., MacEwan, D. J., Mangum, J., Wonnacott, S., & Ahluwalia, A. (2018). Goals and practicalities of immunoblotting and immunohistochemistry: A guide for submission to the British Journal of Pharmacology. British Journal of Pharmacology, 175(3), 407-411. https://doi.org/10.1111/bph.14112
Bernal-Ramirez, J., Silva-Platas, C., Jerjes-Sanchez, C., Ramos-Gonzalez, M. R., Vazquez-Garza, E., Chapoy-Villanueva, H., Ramirez-Rivera, A., Zarain-Herzberg, A., Garcia, N., & Garcia-Rivas, G. (2021). Resveratrol prevents right ventricle dysfunction, calcium mishandling, and energetic failure via SIRT3 stimulation in pulmonary arterial hypertension. Oxidative Medicine and Cellular Longevity, 2021, 9912434. https://doi.org/10.1155/2021/9912434
Billaud, M., Dahan, D., Marthan, R., Savineau, J. P., & Guibert, C. (2011). Role of the gap junctions in the contractile response to agonists in pulmonary artery from two rat models of pulmonary hypertension. Respiratory Research, 12, 30. https://doi.org/10.1186/1465-9921-12-30
Billaud, M., Marthan, R., Savineau, J. P., & Guibert, C. (2009). Vascular smooth muscle modulates endothelial control of vasoreactivity via reactive oxygen species production through myoendothelial communications. PLoS ONE, 4(7), e6432. https://doi.org/10.1371/journal.pone.0006432
Bonnet, S., & Boucherat, O. (2018). The ROS controversy in hypoxic pulmonary hypertension revisited. European Respiratory Journal, 51, 1800276. https://doi.org/10.1183/13993003.00276-2018
Chunyu, Z., Junbao, D., Dingfang, B., Hui, Y., Xiuying, T., & Chaoshu, T. (2003). The regulatory effect of hydrogen sulfide on hypoxic pulmonary hypertension in rats. Biochemical and Biophysical Research Communications, 302(4), 810-816. https://doi.org/10.1016/s0006-291x(03)00256-0
Culley, M. K., & Chan, S. Y. (2018). Mitochondrial metabolism in pulmonary hypertension: Beyond mountains there are mountains. Journal of Clinical Investigation, 128(9), 3704-3715. https://doi.org/10.1172/JCI120847
Curtis, M. J., Alexander, S. P. H., Cirino, G., George, C. H., Kendall, D. A., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Patel, H. H., Sobey, C. G., Stanford, S. C., Stanley, P., Stefanska, B., Stephens, G. J., Teixeira, M. M., Vergnolle, N., & Ahluwalia, A. (2022). Planning experiments: Updated guidance on experimental design and analysis and their reporting III. British Journal of Pharmacology, 179(15), 3907-3913. https://doi.org/10.1111/bph.15868
Dai, W., Amoedo, N. D., Perry, J., Le Grand, B., Boucard, A., Carreno, J., Zhao, L., Brown, D. A., Rossignol, R., & Kloner, R. A. (2022). Effects of OP2113 on myocardial infarct size and no reflow in a rat myocardial ischemia/reperfusion model. Cardiovascular Drugs and Therapy, 36(2), 217-227. https://doi.org/10.1007/s10557-020-07113-7
Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., & Milzani, A. (2003). Protein carbonylation in human diseases. Trends in Molecular Medicine, 9(4), 169-176. https://doi.org/10.1016/s1471-4914(03)00031-5
de Jesus, D. S., DeVallance, E., Li, Y., Falabella, M., Guimaraes, D., Shiva, S., Kaufman, B. A., Gladwin, M. T., & Pagano, P. J. (2019). Nox1/Ref-1-mediated activation of CREB promotes Gremlin1-driven endothelial cell proliferation and migration. Redox Biology, 22, 101138. https://doi.org/10.1016/j.redox.2019.101138
Detaille, D., Pasdois, P., Semont, A., Dos Santos, P., & Diolez, P. (2019). An old medicine as a new drug to prevent mitochondrial complex I from producing oxygen radicals. PLoS ONE, 14(5), e0216385. https://doi.org/10.1371/journal.pone.0216385
Dias Amoedo, N., Dard, L., Sarlak, S., Mahfouf, W., Blanchard, W., Rousseau, B., Izotte, J., Claverol, S., Lacombe, D., Rezvani, H. R., Pierri, C. L., & Rossignol, R. (2020). Targeting human lung adenocarcinoma with a suppressor of mitochondrial superoxide production. Antioxidants & Redox Signaling, 33(13), 883-902. https://doi.org/10.1089/ars.2019.7892
Ducret, T., Guibert, C., Marthan, R., & Savineau, J. P. (2008). Serotonin-induced activation of TRPV4-like current in rat intrapulmonary arterial smooth muscle cells. Cell Calcium, 43(4), 315-323. https://doi.org/10.1016/j.ceca.2007.05.018
Egnatchik, R. A., Brittain, E. L., Shah, A. T., Fares, W. H., Ford, H. J., Monahan, K., Kang, C. J., Kocurek, E. G., Zhu, S., Luong, T., Nguyen, T. T., Hysinger, E., Austin, E. D., Skala, M. C., Young, J. D., Roberts, L. J. 2nd, Hemnes, A. R., West, J., & Fessel, J. P. (2017). Dysfunctional BMPR2 signaling drives an abnormal endothelial requirement for glutamine in pulmonary arterial hypertension. Pulmonary Circulation, 7(1), 186-199. https://doi.org/10.1086/690236
Fowler, E. D., Benoist, D., Drinkhill, M. J., Stones, R., Helmes, M., Wust, R. C., Stienen, G. J., Steele, D. S., & White, E. (2015). Decreased creatine kinase is linked to diastolic dysfunction in rats with right heart failure induced by pulmonary artery hypertension. Journal of Molecular and Cellular Cardiology, 86, 1-8. https://doi.org/10.1016/j.yjmcc.2015.06.016
Fowler, E. D., Drinkhill, M. J., Norman, R., Pervolaraki, E., Stones, R., Steer, E., Benoist, D., Steele, D. S., Calaghan, S. C., & White, E. (2018). Beta1-adrenoceptor antagonist, metoprolol attenuates cardiac myocyte Ca2+ handling dysfunction in rats with pulmonary artery hypertension. Journal of Molecular and Cellular Cardiology, 120, 74-83. https://doi.org/10.1016/j.yjmcc.2018.05.015
Fresquet, F., Pourageaud, F., Leblais, V., Brandes, R. P., Savineau, J. P., Marthan, R., & Muller, B. (2006). Role of reactive oxygen species and gp91phox in endothelial dysfunction of pulmonary arteries induced by chronic hypoxia. British Journal of Pharmacology, 148(5), 714-723. https://doi.org/10.1038/sj.bjp.0706779
Freund-Michel, V., Guibert, C., Dubois, M., Courtois, A., Marthan, R., Savineau, J. P., & Muller, B. (2013). Reactive oxygen species as therapeutic targets in pulmonary hypertension. Therapeutic Advances in Respiratory Disease, 7(3), 175-200. https://doi.org/10.1177/1753465812472940
Freund-Michel, V., Khoyrattee, N., Savineau, J. P., Muller, B., & Guibert, C. (2014). Mitochondria: Roles in pulmonary hypertension. International Journal of Biochemistry and Cell Biology, 55, 93-97. https://doi.org/10.1016/j.biocel.2014.08.012
Genet, N., Billaud, M., Rossignol, R., Dubois, M., Gillibert-Duplantier, J., Isakson, B. E., Marthan, R., Savineau, J. P., & Guibert, C. (2017). Signaling pathways linked to serotonin-induced superoxide anion production: A physiological role for mitochondria in pulmonary arteries. Frontiers in Physiology, 8, 76. https://doi.org/10.3389/fphys.2017.00076
Grogan, A., Lucero, E. Y., Jiang, H., & Rockman, H. A. (2022). Pathophysiology and pharmacology of G protein-coupled receptors in the heart. Cardiovascular Research, 119, 1117-1129. https://doi.org/10.1093/cvr/cvac171
Guibert, C., Marthan, R., & Savineau, J. P. (2004). 5-HT induces an arachidonic acid-sensitive calcium influx in rat small intrapulmonary artery. American Journal of Physiology. Lung Cellular and Molecular Physiology, 286(6), L1228-L1236. https://doi.org/10.1152/ajplung.00265.2003
Gurtler, A., Kunz, N., Gomolka, M., Hornhardt, S., Friedl, A. A., McDonald, K., Kohn, J. E., & Posch, A. (2013). Stain-free technology as a normalization tool in Western blot analysis. Analytical Biochemistry, 433(2), 105-111. https://doi.org/10.1016/j.ab.2012.10.010
Humbert, M., Guignabert, C., Bonnet, S., Dorfmuller, P., Klinger, J. R., Nicolls, M. R., Olschewski, A. J., Pullamsetti, S. S., Schermuly, R. T., Stenmark, K. R., & Rabinovitch, M. (2019). Pathology and pathobiology of pulmonary hypertension: State of the art and research perspectives. European Respiratory Journal, 53, 1801887. https://doi.org/10.1183/13993003.01887-2018
Humbert, M., Kovacs, G., Hoeper, M. M., Badagliacca, R., Berger, R. M. F., Brida, M., Carlsen, J., Coats, A. J. S., Escribano-Subias, P., Ferrari, P., Ferreira, D. S., Ghofrani, H. A., Giannakoulas, G., Kiely, D. G., Mayer, E., Meszaros, G., Nagavci, B., Olsson, K. M., Pepke-Zaba, J., … the ESC/ERS Scientific Document Group. (2022). 2022 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension. European Respiratory Journal, 61, 2200879. https://doi.org/10.1183/13993003.00879-2022
Humbert, M., Lau, E. M., Montani, D., Jais, X., Sitbon, O., & Simonneau, G. (2014). Advances in therapeutic interventions for patients with pulmonary arterial hypertension. Circulation, 130(24), 2189-2208. https://doi.org/10.1161/CIRCULATIONAHA.114.006974
Humbert, M., McLaughlin, V., Gibbs, J. S. R., Gomberg-Maitland, M., Hoeper, M. M., Preston, I. R., Souza, R., Waxman, A., Escribano Subias, P., Feldman, J., Meyer, G., Montani, D., Olsson, K. M., Manimaran, S., Barnes, J., Linde, P. G., de Oliveira Pena, J., Badesch, D. B., & PULSAR Trial Investigators. (2021). Sotatercept for the treatment of pulmonary arterial hypertension. New England Journal of Medicine, 384(13), 1204-1215. https://doi.org/10.1056/NEJMoa2024277
Karamsetty, M. R., Klinger, J. R., & Hill, N. S. (2001). Phytoestrogens restore nitric oxide-mediated relaxation in isolated pulmonary arteries from chronically hypoxic rats. Journal of Pharmacology and Experimental Therapeutics, 297(3), 968-974.
Kass, D. A., & Solaro, R. J. (2006). Mechanisms and use of calcium-sensitizing agents in the failing heart. Circulation, 113(2), 305-315. https://doi.org/10.1161/CIRCULATIONAHA.105.542407
Kereveur, A., Callebert, J., Humbert, M., Herve, P., Simonneau, G., Launay, J. M., & Drouet, L. (2000). High plasma serotonin levels in primary pulmonary hypertension. Effect of long-term epoprostenol (prostacyclin) therapy. Arteriosclerosis, Thrombosis, and Vascular Biology, 20(10), 2233-2239. https://doi.org/10.1161/01.ATV.20.10.2233
Kim, C., Patel, P., Gouvin, L. M., Brown, M. L., Khalil, A., Henchey, E. M., Heuck, A. P., & Yadava, N. (2014). Comparative analysis of the mitochondrial physiology of pancreatic beta cells. Bioenergetics, 3(1), 110. https://doi.org/10.4172/2167-7662.1000110
Lee, S. L., Wang, W. W., & Fanburg, B. L. (1998). Superoxide as an intermediate signal for serotonin-induced mitogenesis. Free Radical Biology and Medicine, 24(5), 855-858. https://doi.org/10.1016/S0891-5849(97)00359-6
Lilley, E., Stanford, S. C., Kendall, D. E., Alexander, S. P. H., Cirino, G., Docherty, J. R., George, C. H., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Sobey, C. G., Stefanska, B., Stephens, G., Teixeira, M., & Ahluwalia, A. (2020). ARRIVE 2.0 and the British Journal of Pharmacology: Updated guidance for 2020. British Journal of Pharmacology, 177(16), 3611-3616. https://doi.org/10.1111/bph.15178
Liu, J. Q., & Folz, R. J. (2004). Extracellular superoxide enhances 5-HT-induced murine pulmonary artery vasoconstriction. American Journal of Physiology. Lung Cellular and Molecular Physiology, 287(1), L111-L118. https://doi.org/10.1152/ajplung.00006.2004
Liu, J. Q., Zelko, I. N., Erbynn, E. M., Sham, J. S., & Folz, R. J. (2006). Hypoxic pulmonary hypertension: Role of superoxide and NADPH oxidase (gp91phox). American Journal of Physiology. Lung Cellular and Molecular Physiology, 290(1), L2-L10. https://doi.org/10.1152/ajplung.00135.2005
Maclean, M. R., & Dempsie, Y. (2010). The serotonin hypothesis of pulmonary hypertension revisited. Advances in Experimental Medicine and Biology, 661, 309-322. https://doi.org/10.1007/978-1-60761-500-2_20
Medvedev, R., Sanchez-Alonso, J. L., Alvarez-Laviada, A., Rossi, S., Dries, E., Schorn, T., Abdul-Salam, V. B., Trayanova, N., Wojciak-Stothard, B., Miragoli, M., Faggian, G., & Gorelik, J. (2021). Nanoscale study of calcium handling remodeling in right ventricular cardiomyocytes following pulmonary hypertension. Hypertension, 77(2), 605-616. https://doi.org/10.1161/HYPERTENSIONAHA.120.14858
Mittal, M., Roth, M., König, P., Hofmann, S., Dony, E., Goyal, P., Selbitz, A. C., Schermuly, R. T., Ghofrani, H. A., Kwapiszewska, G., Kummer, W., Klepetko, W., Hoda, M. A., Fink, L., Hänze, J., Seeger, W., Grimminger, F., Schmidt, H. H., & Weissmann, N. (2007). Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circulation Research, 101(3), 258-267. https://doi.org/10.1161/CIRCRESAHA.107.148015
Morel, O. E., Buvry, A., Le Corvoisier, P., Tual, L., Favret, F., Leon-Velarde, F., Crozatier, B., & Richalet, J. P. (2003). Effects of nifedipine-induced pulmonary vasodilatation on cardiac receptors and protein kinase C isoforms in the chronically hypoxic rat. Pflügers Archiv/European Journal of Physiology, 446(3), 356-364. https://doi.org/10.1007/s00424-003-1034-y
Negre-Salvayre, A., Coatrieux, C., Ingueneau, C., & Salvayre, R. (2008). Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. British Journal of Pharmacology, 153(1), 6-20. https://doi.org/10.1038/sj.bjp.0707395
Norel, X., Walch, L., Costantino, M., Labat, C., Gorenne, I., Dulmet, E., Rossi, F., & Brink, C. (1996). M1 and M3 muscarinic receptors in human pulmonary arteries. British Journal of Pharmacology, 119(1), 149-157. https://doi.org/10.1111/j.1476-5381.1996.tb15688.x
Nouette-Gaulain, K., Biais, M., Savineau, J. P., Marthan, R., Mazat, J. P., Letellier, T., & Sztark, F. (2011). Chronic hypoxia-induced alterations in mitochondrial energy metabolism are not reversible in rat heart ventricles. Canadian Journal of Physiology and Pharmacology, 89(1), 58-66. https://doi.org/10.1139/y10-105
Nouette-Gaulain, K., Malgat, M., Rocher, C., Savineau, J. P., Marthan, R., Mazat, J. P., & Sztark, F. (2005). Time course of differential mitochondrial energy metabolism adaptation to chronic hypoxia in right and left ventricles. Cardiovascular Research, 66(1), 132-140. https://doi.org/10.1016/j.cardiores.2004.12.023
Orii, R., Sugawara, Y., Sawamura, S., & Yamada, Y. (2010). M(3)muscarinic receptors mediate acetylcholine-induced pulmonary vasodilation in pulmonary hypertension. Bioscience Trends, 4(5), 260-266.
Pak, O., Scheibe, S., Esfandiary, A., Gierhardt, M., Sydykov, A., Logan, A., Fysikopoulos, A., Veit, F., Hecker, M., Kroschel, F., Quanz, K., Erb, A., Schafer, K., Fassbinder, M., Alebrahimdehkordi, N., Ghofrani, H. A., Schermuly, R. T., Brandes, R. P., Seeger, W., … Sommer, N. (2018). Impact of the mitochondria-targeted antioxidant MitoQ on hypoxia-induced pulmonary hypertension. European Respiratory Journal, 51, 1701024. https://doi.org/10.1183/13993003.01024-2017
Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Wurbel, H. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. British Journal of Pharmacology, 177(16), 3617-3624. https://doi.org/10.1111/bph.15193
Piao, L., Marsboom, G., & Archer, S. L. (2010). Mitochondrial metabolic adaptation in right ventricular hypertrophy and failure. Journal of Molecular Medicine (Berlin, Germany), 88(10), 1011-1020. https://doi.org/10.1007/s00109-010-0679-1
Powell, C. R., Dillon, K. M., & Matson, J. B. (2018). A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochemical Pharmacology, 149, 110-123. https://doi.org/10.1016/j.bcp.2017.11.014
Rodat, L., Savineau, J. P., Marthan, R., & Guibert, C. (2007). Effect of chronic hypoxia on voltage-independent calcium influx activated by 5-HT in rat intrapulmonary arteries. Pflügers Archiv/European Journal of Physiology, 454(1), 41-51. https://doi.org/10.1007/s00424-006-0178-y
Rodat-Despoix, L., Aires, V., Ducret, T., Marthan, R., Savineau, J. P., Rousseau, E., & Guibert, C. (2009). Signalling pathways involved in the contractile response to 5-HT in the human pulmonary artery. European Respiratory Journal, 34(6), 1338-1347. https://doi.org/10.1183/09031936.00143808
Roubenne, L., Marthan, R., Le Grand, B., & Guibert, C. (2021). Hydrogen sulfide metabolism and pulmonary hypertension. Cell, 10, 1477. https://doi.org/10.3390/cells10061477
Savale, L., Guignabert, C., Weatherald, J., & Humbert, M. (2018). Precision medicine and personalising therapy in pulmonary hypertension: Seeing the light from the dawn of a new era. European Respiratory Review: an Official Journal of the European Respiratory Society, 27, 180004. https://doi.org/10.1183/16000617.0004-2018
Shults, N. V., Melnyk, O., Suzuki, D. I., & Suzuki, Y. J. (2018). Redox biology of right-sided heart failure. Antioxidants (Basel), 7, 106. https://doi.org/10.3390/antiox7080106
Singh, N., Dorfmuller, P., Shlobin, O. A., & Ventetuolo, C. E. (2022). Group 3 pulmonary hypertension: From bench to bedside. Circulation Research, 130(9), 1404-1422. https://doi.org/10.1161/CIRCRESAHA.121.319970
Smith, K. A., Waypa, G. B., Dudley, V. J., Budinger, G. R. S., Abdala-Valencia, H., Bartom, E., & Schumacker, P. T. (2020). Role of hypoxia-inducible factors in regulating right ventricular function and remodeling during chronic hypoxia-induced pulmonary hypertension. American Journal of Respiratory Cell and Molecular Biology, 63(5), 652-664. https://doi.org/10.1165/rcmb.2020-0023OC
Smolders, V., Rodriguez, C., Blanco, I., Szulcek, R., Timens, W., Piccari, L., Roger, Y., Hu, X., Moren, C., Bonjoch, C., Sebastian, L., Castella, M., Osorio, J., Peinado, V. I., Bogaard, H. J., Quax, P. H. A., Cascante, M., Barbera, J. A., & Tura-Ceide, O. (2022). Metabolic profile in endothelial cells of chronic thromboembolic pulmonary hypertension and pulmonary arterial hypertension. Scientific Reports, 12(1), 2283. https://doi.org/10.1038/s41598-022-06238-z
Ukai, Y., Taniguchi, N., Takeshita, K., Kimura, K., & Enomoto, H. (1984). Chronic anethole trithione treatment enhances the salivary secretion and increases the muscarinic acetylcholine receptors in the rat submaxillary gland. Archives Internationales de Pharmocodynamie et de Thérapie, 271(2), 206-212.
Veksler, V. I., Kuznetsov, A. V., Sharov, V. G., Kapelko, V. I., & Saks, V. A. (1987). Mitochondrial respiratory parameters in cardiac tissue: A novel method of assessment by using saponin-skinned fibers. Biochimica et Biophysica Acta, 892(2), 191-196. https://doi.org/10.1016/0005-2728(87)90174-5
Vonk Noordegraaf, A., Chin, K. M., Haddad, F., Hassoun, P. M., Hemnes, A. R., Hopkins, S. R., Kawut, S. M., Langleben, D., Lumens, J., & Naeije, R. (2019). Pathophysiology of the right ventricle and of the pulmonary circulation in pulmonary hypertension: An update. European Respiratory Journal, 53, 1801900. https://doi.org/10.1183/13993003.01900-2018
Yu, H. Z., Han, S. F., Li, P., Zhu, C. L., Zhang, X. X., Gan, L., & Gan, Y. (2011). An examination of the potential effect of lipids on the first-pass metabolism of the lipophilic drug anethol trithione. Journal of Pharmaceutical Sciences, 100(11), 5048-5058. https://doi.org/10.1002/jps.22702