Nitric oxide is involved in the cardioprotection of neonatal rat hearts, but not in neonatal ischemic postconditioning
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
Grantová podpora
LX22NPO5104
National Institute for Research of Metabolic and Cardiovascular Diseases
20-02-00052
Ministry of Health of the Czech Republic
PubMed
39097984
PubMed Central
PMC11298247
DOI
10.14814/phy2.16147
Knihovny.cz E-zdroje
- Klíčová slova
- DEA‐NONO, L‐NAME, SIN‐1, ischemic postconditioning, neonatal hearts, nitric oxide,
- MeSH
- donory oxidu dusnatého farmakologie MeSH
- ischemické přivykání metody MeSH
- ischemický postconditioning * metody MeSH
- krysa rodu Rattus MeSH
- molsidomin farmakologie analogy a deriváty MeSH
- myokard metabolismus MeSH
- NG-nitroargininmethylester * farmakologie MeSH
- novorozená zvířata * MeSH
- oxid dusnatý * metabolismus MeSH
- potkani Wistar * MeSH
- reperfuzní poškození myokardu * prevence a kontrola metabolismus MeSH
- srdce účinky léků MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- donory oxidu dusnatého MeSH
- molsidomin MeSH
- NG-nitroargininmethylester * MeSH
- oxid dusnatý * MeSH
The cardioprotective effect of ischemic preconditioning (IPC) and ischemic postconditioning (IPoC) in adult hearts is mediated by nitric oxide (NO). During the early developmental period, rat hearts exhibit higher resistance to ischemia-reperfusion (I/R) injury, contain higher levels of serum nitrates, and their resistance cannot be further increased by IPC or IPoC. NOS blocker (L-NAME) lowers their high resistance. Wistar rat hearts (postnatal Days 1 and 10) were perfused according to Langendorff and exposed to 40 min of global ischemia followed by reperfusion with or without IPoC. NO and reactive oxygen species donors (DEA-NONO, SIN-1) and L-NAME were administered. Tolerance to ischemia decreased between Days 1 and 10. DEA-NONO (low concentrations) significantly increased tolerance to I/R injury on both Days 1 and 10. SIN-1 increased tolerance to I/R injury on Day 10, but not on Day 1. L-NAME significantly reduced resistance to I/R injury on Day 1, but actually increased resistance to I/R injury on Day 10. Cardioprotection by IPoC on Day 10 was not affected by either NO donors or L-NAME. It can be concluded that resistance of the neonatal heart to I/R injury is NO dependent, but unlike in adult hearts, cardioprotective interventions, such as IPoC, are most likely NO independent.
Department of Pathophysiology 2nd Faculty of Medicine Charles University Prague Czech Republic
Department of Physiology 2nd Faculty of Medicine Charles University Prague Czech Republic
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Abraham, R. A. , Rana, G. , Agrawal, P. K. , Johnston, R. , Sarna, A. , Ramesh, S. , Acharya, R. , Khan, N. , Porwal, A. , Kurundkar, S. B. , Pandey, A. , Pullakhandam, R. , Nair, K. M. , Kumar, G. T. , Sachdev, H. , Kapil, U. , Deb, S. , Wagt, A. , Khera, A. , & Ramakrishnan, L. (2021). The effects of a single freeze‐thaw cycle on concentrations of nutritional, noncommunicable disease, and inflammatory biomarkers in serum samples. Journal of Laboratory Physicians, 13, 6–13. PubMed PMC
Alanova, P. , Kolar, F. , Ostadal, B. , & Neckar, J. (2015). Role of NO/cGMP signaling pathway in cardiac ischemic tolerance of chronically hypoxic rats. Physiological Research, 64, 783–787. PubMed
Babiker, F. , Al‐Jarallah, A. , & AL‐Awadi, M. (2019). Effects of cardiac hypertrophy, diabetes, aging, and pregnancy on the cardioprotective effects of postconditioning in male and female rats. Cardiology Research and Practice, 2019, 3403959. PubMed PMC
Cao, C. M. , Yan, W. Y. , Liu, J. , Kam, K. W. , Zhan, S. Z. , Sham, J. S. , & Wong, T. M. (2006). Attenuation of mitochondrial, but not cytosolic, Ca2+ overload reduces myocardial injury induced by ischemia and reperfusion. Acta Pharmacologica Sinica, 27, 911–918. PubMed
Chauvin, C. , De Oliveira, F. , Ronot, X. , Mousseau, M. , Leverve, X. , & Fontaine, E. (2001). Rotenone inhibits the mitochondrial permeability transition‐induced cell death in U937 and KB cells. The Journal of Biological Chemistry, 276, 41394–41398. PubMed
De Mendiburu, F. , & Simon, R. (2015). Agricolae–ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ PrePrints, 3, e1404v1.
Doul, J. , Charvatova, Z. , Ostadalova, I. , Kohutiar, M. , Maxova, H. , & Ostadal, B. (2015). Neonatal rat hearts cannot be protected by ischemic postconditioning. Physiological Research, 64, 789–794. PubMed
Doul, J. , Mikova, D. , Raskova, M. , Ostadalova, I. , Maxova, H. , Ostadal, B. , & Charvatova, Z. (2019). Possible role of mitochondrial K‐ATP channel and nitric oxide in protection of the neonatal rat heart. Molecular and Cellular Biochemistry, 450, 35–42. PubMed PMC
Drahota, Z. , Milerova, M. , Endlicher, R. , Rychtrmoc, D. , Cervinkova, Z. , & OST'adal, B. (2012). Developmental changes of the sensitivity of cardiac and liver mitochondrial permeability transition pore to calcium load and oxidative stress. Physiological Research, 61(Suppl 1), S165–S172. PubMed
Gonzalez Arbelaez, L. F. , Ciocci Pardo, A. , Fantinelli, J. C. , & Mosca, S. M. (2016). Cyclosporine‐a mimicked the ischemic pre‐ and postconditioning‐mediated cardioprotection in hypertensive rats: Role of PKCepsilon. Experimental and Molecular Pathology, 100, 266–275. PubMed
Grievink, H. , Zeltcer, G. , Drenger, B. , Berenshtein, E. , & Chevion, M. (2016). Protection by nitric oxide donors of isolated rat hearts is associated with activation of redox metabolism and ferritin accumulation. PLoS One, 11, e0159951. PubMed PMC
Hausenloy, D. J. , Ong, S. B. , & Yellon, D. M. (2009). The mitochondrial permeability transition pore as a target for preconditioning and postconditioning. Basic Research in Cardiology, 104, 189–202. PubMed
Heusch, G. (2015). Molecular basis of cardioprotection: Signal transduction in ischemic pre‐, post‐, and remote conditioning. Circulation Research, 116, 674–699. PubMed
Heusch, G. (2020). Myocardial ischaemia‐reperfusion injury and cardioprotection in perspective. Nature Reviews Cardiology, 17, 773–789. PubMed
Heusch, G. (2024). Myocardial ischemia/reperfusion: Translational pathophysiology of ischemic heart disease. Medicamundi, 5, 10–31. PubMed
Jekabsone, A. , Ivanoviene, L. , Brown, G. C. , & Borutaite, V. (2003). Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. Journal of Molecular and Cellular Cardiology, 35, 803–809. PubMed
Jones, D. A. , Pellaton, C. , Velmurugan, S. , Rathod, K. S. , Andiapen, M. , Antoniou, S. , van Eijl, S. , Webb, A. J. , Westwood, M. A. , Parmar, M. K. , Mathur, A. , & Ahluwalia, A. (2015). Randomized phase 2 trial of intracoronary nitrite during acute myocardial infarction. Circulation Research, 116(3), 437–447. PubMed PMC
Kaljusto, M. L. , Rutkovsky, A. , Stenslokken, K. O. , & Vaage, J. (2010). Postconditioning in mouse hearts is inhibited by blocking the reverse mode of the sodium‐calcium exchanger. Interactive Cardiovascular and Thoracic Surgery, 10, 743–748. PubMed
Karch, J. , Kanisicak, O. , Brody, M. J. , Sargent, M. A. , Michael, D. M. , & Molkentin, J. D. (2015). Necroptosis interfaces with MOMP and the MPTP in mediating cell death. PLoS One, 10, e0130520. PubMed PMC
Lencova‐Popelova, O. , Jansova, H. , Jirkovsky, E. , Bures, J. , Jirkovska‐Vavrova, A. , Mazurova, Y. , Reimerova, P. , Vostatkova, L. , Adamcova, M. , Hroch, M. , Pokorna, Z. , Kovarikova, P. , Simunek, T. , & Sterba, M. (2016). Are cardioprotective effects of NO‐releasing drug molsidomine translatable to chronic anthracycline cardiotoxicity settings? Toxicology, 372, 52–63. PubMed
Liaw, N. Y. , Hoe, L. S. , Sheeran, F. L. , Peart, J. N. , Headrick, J. P. , Cheung, M. M. , & Pepe, S. (2013). Postnatal shifts in ischemic tolerance and cell survival signaling in murine myocardium. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 305, R1171–R1181. PubMed
Lieder, H. R. , Irmert, A. , Kamler, M. , Heusch, G. , & Kleinbongard, P. (2019). Sex is no determinant of cardioprotection by ischemic preconditioning in rats, but ischemic/reperfused tissue mass is for remote ischemic preconditioning. Physiological Reports, 7, e14146. PubMed PMC
Litchfield, J. (1958). Blood pressure in infant rats. Physiological Zoology, 31, 1–6.
Matejikova, J. , Kucharska, J. , Pinterova, M. , Pancza, D. , & Ravingerova, T. (2009). Protection against ischemia‐induced ventricular arrhythmias and myocardial dysfunction conferred by preconditioning in the rat heart: Involvement of mitochondrial K(ATP) channels and reactive oxygen species. Physiological Research, 58, 9–19. PubMed
Milerova, M. , Charvatova, Z. , Skarka, L. , Ostadalova, I. , Drahota, Z. , Fialova, M. , & Ostadal, B. (2010). Neonatal cardiac mitochondria and ischemia/reperfusion injury. Molecular and Cellular Biochemistry, 335, 147–153. PubMed
Milerova, M. , Drahota, Z. , Chytilova, A. , Tauchmannova, K. , Houstek, J. , & Ostadal, B. (2016). Sex difference in the sensitivity of cardiac mitochondrial permeability transition pore to calcium load. Molecular and Cellular Biochemistry, 412, 147–154. PubMed
Modi, P. , Imura, H. , Caputo, M. , Pawade, A. , Parry, A. , Angelini, G. D. , & Suleiman, M. S. (2002). Cardiopulmonary bypass‐induced myocardial reoxygenation injury in pediatric patients with cyanosis. The Journal of Thoracic and Cardiovascular Surgery, 124, 1035–1036. PubMed
Morrison, R. R. , Tan, X. L. , Ledent, C. , Mustafa, S. J. , & Hofmann, P. A. (2007). Targeted deletion of A2A adenosine receptors attenuates the protective effects of myocardial postconditioning. American Journal of Physiology. Heart and Circulatory Physiology, 293, H2523–H2529. PubMed
Okamoto, F. , Allen, B. S. , Buckberg, G. D. , Bugyi, H. , & Leaf, J. (1986). Reperfusion conditions: Importance of ensuring gentle versus sudden reperfusion during relief of coronary occlusion. The Journal of Thoracic and Cardiovascular Surgery, 92, 613–620. PubMed
Ostadal, B. , Drahota, Z. , Houstek, J. , Milerova, M. , Ostadalova, I. , Hlavackova, M. , & Kolar, F. (2019). Developmental and sex differences in cardiac tolerance to ischemia‐reperfusion injury: The role of mitochondria. Canadian Journal of Physiology and Pharmacology, 97, 808–814. PubMed
Ostadal, B. , Netuka, I. , Maly, J. , Besik, J. , & Ostadalova, I. (2009). Gender differences in cardiac ischemic injury and protection—Experimental aspects. Experimental Biology and Medicine (Maywood, N.J.), 234, 1011–1019. PubMed
Ostadal, B. , & Ostadal, P. (2014). Sex‐based differences in cardiac ischaemic injury and protection: Therapeutic implications. British Journal of Pharmacology, 171, 541–554. PubMed PMC
Ostadal, B. , Ostadalova, I. , & Dhalla, N. S. (1999). Development of cardiac sensitivity to oxygen deficiency: Comparative and ontogenetic aspects. Physiological Reviews, 79, 635–659. PubMed
Ostadalova, I. , Kolar, F. , Ostadal, B. , Rohlicek, V. , Rohlicek, J. , & Prochazka, J. (1993). Early postnatal development of contractile performance and responsiveness to Ca2+, verapamil and ryanodine in the isolated rat heart. Journal of Molecular and Cellular Cardiology, 25, 733–740. PubMed
Ostadalova, I. , Ostadal, B. , Jarkovska, D. , & Kolar, F. (2002). Ischemic preconditioning in chronically hypoxic neonatal rat heart. Pediatric Research, 52, 561–567. PubMed
Ostadalova, I. , Ostadal, B. , Kolar, F. , Parratt, J. R. , & Wilson, S. (1998). Tolerance to ischaemia and ischaemic preconditioning in neonatal rat heart. Journal of Molecular and Cellular Cardiology, 30, 857–865. PubMed
Ovize, M. , Baxter, G. F. , DI Lisa, F. , Ferdinandy, P. , Garcia‐Dorado, D. , Hausenloy, D. J. , Heusch, G. , Vinten‐Johansen, J. , Yellon, D. M. , Schulz, R. , & Working Group of Cellular Biology of Heart of European Society of, Cardiology . (2010). Postconditioning and protection from reperfusion injury: Where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovascular Research, 87, 406–423. PubMed
Pasdois, P. , Parker, J. E. , Griffiths, E. J. , & Halestrap, A. P. (2013). Hexokinase II and reperfusion injury: TAT‐HK2 peptide impairs vascular function in Langendorff‐perfused rat hearts. Circulation Research, 112, e3–e7. PubMed
Penna, C. , Cappello, S. , Mancardi, D. , Raimondo, S. , Rastaldo, R. , Gattullo, D. , Losano, G. , & Pagliaro, P. (2006). Post‐conditioning reduces infarct size in the isolated rat heart: Role of coronary flow and pressure and the nitric oxide/cGMP pathway. Basic Research in Cardiology, 101, 168–179. PubMed
Penna, C. , Rastaldo, R. , Mancardi, D. , Raimondo, S. , Cappello, S. , Gattullo, D. , Losano, G. , & Pagliaro, P. (2006). Post‐conditioning induced cardioprotection requires signaling through a redox‐sensitive mechanism, mitochondrial ATP‐sensitive K+ channel and protein kinase C activation. Basic Research in Cardiology, 101, 180–189. PubMed
Piot, C. , Croisille, P. , Staat, P. , Thibault, H. , Rioufol, G. , Mewton, N. , Elbelghiti, R. , Cung, T. T. , Bonnefoy, E. , Angoulvant, D. , Macia, C. , Raczka, F. , Sportouch, C. , Gahide, G. , Finet, G. , André‐Fouët, X. , Revel, D. , Kirkorian, G. , Monassier, J.‐P. , … Ovize, M. (2008). Effect of cyclosporine on reperfusion injury in acute myocardial infarction. New England Journal of Medicine, 359(5), 473–481. PubMed
R Core Team . (2023). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/
Reichelt, M. E. , Willems, L. , Hack, B. A. , Peart, J. N. , & Headrick, J. P. (2009). Cardiac and coronary function in the Langendorff‐perfused mouse heart model. Experimental Physiology, 94, 54–70. PubMed
Sanghvi, S. , Szteyn, K. , Ponnalagu, D. , Sridharan, D. , Lam, A. , Hansra, I. , Chaudhury, A. , Majumdar, U. , Kohut, A. R. , Gururaja Rao, S. , Khan, M. , Garg, V. , & Singh, H. (2022). Inhibition of BK(Ca) channels protects neonatal hearts against myocardial ischemia and reperfusion injury. Cell Death Discovery, 8, 175. PubMed PMC
Shintani‐Ishida, K. , Inui, M. , & Yoshida, K. (2012). Ischemia‐reperfusion induces myocardial infarction through mitochondrial Ca2+ overload. Journal of Molecular and Cellular Cardiology, 53, 233–239. PubMed
Simoncini, T. , Hafezi‐Moghadam, A. , Brazil, D. P. , Ley, K. , Chin, W. W. , & Liao, J. K. (2000). Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol‐3‐OH kinase. Nature, 407(6803), 538–541. PubMed PMC
Skyschally, A. , Van Caster, P. , Iliodromitis, E. K. , Schulz, R. , Kremastinos, D. T. , & Heusch, G. (2009). Ischemic postconditioning: Experimental models and protocol algorithms. Basic Research in Cardiology, 104, 469–483. PubMed
Sun, J. , Aponte, A. M. , Kohr, M. J. , Tong, G. , Steenbergen, C. , & Murphy, E. (2013). Essential role of nitric oxide in acute ischemic preconditioning: S‐nitros(yl)ation versus sGC/cGMP/PKG signaling? Free Radical Biology & Medicine, 54, 105–112. PubMed PMC
Tan, W. , Zhang, C. , Liu, J. , Li, X. , Chen, Y. , & Miao, Q. (2018). Remote ischemic preconditioning has a cardioprotective effect in children in the early postoperative phase: A meta‐analysis of randomized controlled trials. Pediatric Cardiology, 39, 617–626. PubMed
Tsang, A. , Hausenloy, D. J. , Mocanu, M. M. , & Yellon, D. M. (2004). Postconditioning: A form of “modified reperfusion” protects the myocardium by activating the phosphatidylinositol 3‐kinase‐Akt pathway. Circulation Research, 95, 230–232. PubMed
Yang, X. M. , Proctor, J. B. , Cui, L. , Krieg, T. , Downey, J. M. , & Cohen, M. V. (2004). Multiple, brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways. Journal of the American College of Cardiology, 44, 1103–1110. PubMed
Zhang, S. Z. , Gao, Q. , Cao, C. M. , Bruce, I. C. , & Xia, Q. (2006). Involvement of the mitochondrial calcium uniporter in cardioprotection by ischemic preconditioning. Life Sciences, 78, 738–745. PubMed
Zicha, J. , Kunes, J. , & Jelinek, J. (1986). Experimental hypertension in young and adult animals. Hypertension, 8, 1096–1104. PubMed