Mariacristina Filice, Rosa Mazza, Alfonsina Gattuso, Alessia Caferro, Gaetana Napolitano, Gianluca Fasciolo, Paola Venditti, Sandra Imbrogno, Maria Carmela Cerra
{"title":"The cardiac response of the goldfish Carassius auratus to environmental hypoxia: from hemodynamics to mitochondria.","authors":"Mariacristina Filice, Rosa Mazza, Alfonsina Gattuso, Alessia Caferro, Gaetana Napolitano, Gianluca Fasciolo, Paola Venditti, Sandra Imbrogno, Maria Carmela Cerra","doi":"10.1007/s10695-025-01452-8","DOIUrl":null,"url":null,"abstract":"<p><p>Under low O<sub>2</sub>, the heart of Carassius auratus (goldfish) shows an enhanced hemodynamics. This is observed in ex vivo cardiac preparations from animals acclimated to both normoxia and short-term (4 days) moderate hypoxia and perfused for 90 min with a hypoxic medium. Under short-term hypoxia, this is associated with a higher ventricular muscularity and an expanded mitochondrial compartment. To date, little is known about the putative influence of hypoxia on the mitochondrial contribution to cardiac energy metabolism. Similarly, it remains unexplored whether the exposure to environmental low O<sub>2</sub> affects the cardiac response to preload increases (i.e., the Frank-Starling mechanism). We here observed, on ex vivo isolated and perfused goldfish heart, that 20 days of exposure to moderate water hypoxia are accompanied by a potentiated cardiac performance, analyzed as stroke volume, cardiac output, and stroke work. The sensitivity to preload increases significantly improved after 20 days of hypoxia, while it is similar to normoxia after 4 days of exposure. This suggested a time-dependent response. Mitochondrial O<sub>2</sub> consumption initially decreased during short-term hypoxia but returned to normoxia-like levels after 20 days of exposure. Biomolecular analyses of ventricular extracts revealed a time-dependent regulation of key proteins involved in the mitochondrial biogenesis, including PGC1α, NRF1/2, and TFAM, as well as cytochrome c. Additionally, mitochondrial DNA content was notably increased after 20 days of hypoxia. Our data revealed that, when challenged by chronic environmental hypoxia, the goldfish heart improves its pumping behavior under both basal and loading-stimulated conditions. This is accompanied by a mitochondrial remodeling which likely supports adequate energy supply for the working myocardium.</p>","PeriodicalId":12274,"journal":{"name":"Fish Physiology and Biochemistry","volume":"51 1","pages":"36"},"PeriodicalIF":2.5000,"publicationDate":"2025-01-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11759273/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Fish Physiology and Biochemistry","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1007/s10695-025-01452-8","RegionNum":3,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Under low O2, the heart of Carassius auratus (goldfish) shows an enhanced hemodynamics. This is observed in ex vivo cardiac preparations from animals acclimated to both normoxia and short-term (4 days) moderate hypoxia and perfused for 90 min with a hypoxic medium. Under short-term hypoxia, this is associated with a higher ventricular muscularity and an expanded mitochondrial compartment. To date, little is known about the putative influence of hypoxia on the mitochondrial contribution to cardiac energy metabolism. Similarly, it remains unexplored whether the exposure to environmental low O2 affects the cardiac response to preload increases (i.e., the Frank-Starling mechanism). We here observed, on ex vivo isolated and perfused goldfish heart, that 20 days of exposure to moderate water hypoxia are accompanied by a potentiated cardiac performance, analyzed as stroke volume, cardiac output, and stroke work. The sensitivity to preload increases significantly improved after 20 days of hypoxia, while it is similar to normoxia after 4 days of exposure. This suggested a time-dependent response. Mitochondrial O2 consumption initially decreased during short-term hypoxia but returned to normoxia-like levels after 20 days of exposure. Biomolecular analyses of ventricular extracts revealed a time-dependent regulation of key proteins involved in the mitochondrial biogenesis, including PGC1α, NRF1/2, and TFAM, as well as cytochrome c. Additionally, mitochondrial DNA content was notably increased after 20 days of hypoxia. Our data revealed that, when challenged by chronic environmental hypoxia, the goldfish heart improves its pumping behavior under both basal and loading-stimulated conditions. This is accompanied by a mitochondrial remodeling which likely supports adequate energy supply for the working myocardium.
期刊介绍:
Fish Physiology and Biochemistry is an international journal publishing original research papers in all aspects of the physiology and biochemistry of fishes. Coverage includes experimental work in such topics as biochemistry of organisms, organs, tissues and cells; structure of organs, tissues, cells and organelles related to their function; nutritional, osmotic, ionic, respiratory and excretory homeostasis; nerve and muscle physiology; endocrinology; reproductive physiology; energetics; biochemical and physiological effects of toxicants; molecular biology and biotechnology and more.