Publication Cover
Journal of Environmental Science and Health, Part A
Toxic/Hazardous Substances and Environmental Engineering
Volume 58, 2023 - Issue 3
142
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Effects of exposure to sediment-associated fipronil on cardiac function of Neotropical armored catfish Hypostomus regani

, , & ORCID Icon
Pages 236-245 | Received 04 Oct 2022, Accepted 15 Feb 2023, Published online: 21 Feb 2023

References

  • Tingle, C. C.; Rother, J. A.; Dewhurst, C. F.; Lauer, S.; King, W. J. Fipronil: Environmental Fate, Ecotoxicology, and Human Health Concerns. Rev. Environ. Contam. Toxicol. 2003, 1–66.
  • Wang, X.; Martínez, M. A.; Wu, Q.; Ares, I.; Martinez-Larranaga, M. R.; Anadón, A.; Yuan, Z. Fipronil Insecticide Toxicology: Oxidative Stress and Metabolism. Crit. Rev. Toxicol. 2016, 46, 876–899. DOI: 10.1080/10408444.2016.1223014.
  • Kavallieratos, N. G.; Athanassiou, C. G.; Vayias, B. J.; Betsi, P. C. C. Insecticidal Efficacy of Fipronil against Four Stored-Product Insect Pests: Influence of Commodity, Dose, Exposure Interval, Relative Humidity and Temperature. Pest Manag. Sci. 2010, 66, 640–649. DOI: 10.1002/ps.1923.
  • Suzuki, T.; Hirai, A.; Khidkhan, K.; Nimako, C.; Ichise, T.; Takeda, K.; Mizukawa, H.; Nakayama, S. M.; Nomiyama, K.; Hoshi, N.; others. The Effects of Fipronil on Emotional and Cognitive Behaviors in Mammals. Pestic Biochem. Physiol. 2021, 175, 104847. DOI: 10.1016/j.pestbp.2021.104847.
  • Montagner, C. C.; Sodré, F. F.; Acayaba, R. D.; Vidal, C.; Campestrini, I.; Locatelli, M. A.; Pescara, I. C.; Albuquerque, A. F.; Umbuzeiro, G. A.; Jardim, W. F. Ten Years-Snapshot of the Occurrence of Emerging Contaminants in Drinking, Surface and Ground Waters and Wastewaters from São Paulo State, Brazil. J. Braz. Chem. Soc. 2019, 30, 614–632. DOI: 10.21577/0103-5053.20180232.
  • Singh, N. S.; Sharma, R.; Singh, S. K.; Singh, D. K. A Comprehensive Review of Environmental Fate and Degradation of Fipronil and Its Toxic Metabolites. Environ. Res. 2021, 199, 111316. DOI: 10.1016/j.envres.2021.111316.
  • Peret, A. M.; Oliveira, L. F.; Bianchini, I.; Jr, Seleghim, M. H. R.; Peret, A. C.; Mozeto, A. A. Dynamics of Fipronil in Óleo Lagoon in Jataí Ecological Station, São Paulo-Brazil. Chemosphere 2010, 78, 1225–1229. DOI: 10.1016/j.chemosphere.2009.12.060.
  • Gripp, H. S.; Freitas, J. S.; Almeida, E. A.; Bisinoti, M. C.; Moreira, A. B. Biochemical Effects of Fipronil and Its Metabolites on Lipid Peroxidation and Enzymatic Antioxidant Defense in Tadpoles (Eupemphix nattereri: Leiuperidae). Ecotoxicol. Environ. Saf. 2017, 136, 173–179. DOI: 10.1016/j.ecoenv.2016.10.027.
  • Hook, S. E.; Doan, H.; Gonzago, D.; Musson, D.; Du, J.; Kookana, R.; Sellars, M. J.; Kumar, A. The Impacts of Modern-Use Pesticides on Shrimp Aquaculture: An Assessment for North Eastern Australia. Ecotoxicol. Environ. Saf. 2018, 148, 770–780. DOI: 10.1016/j.ecoenv.2017.11.028.
  • Eadie, A.; Vasquez, I. C.; Liang, X.; Wang, X.; Souders, C. L.; II, El Chehouri, J.; Hoskote, R.; Feswick, A.; Cowie, A. M.; Loughery, J. R.; others. Residual Molecular and Behavioral Effects of the Phenylpyrazole Pesticide Fipronil in Larval Zebrafish (Danio rerio) following a Pulse Embryonic Exposure. Comp. Biochem. Physiol. Part D Genomics Proteomics 2020, 36, 100743. DOI: 10.1016/j.cbd.2020.100743.
  • Deiú, A. S.; Ondarza, P. M.; Miglioranza, K. S.; Fernando, R. Multibiomarker Responses and Bioaccumulation of Fipronil in Prochilodus lineatus Exposed to Spiked Sediments: Oxidative Stress and Antioxidant Defenses. Pestic Biochem. Physiol. 2021, 177, 104876. DOI: 10.1016/j.pestbp.2021.104876.
  • Gan, J.; Bondarenko, S.; Oki, L.; Haver, D.; Li, J. X. Occurrence of Fipronil and Its Biologically Active Derivatives in Urban Residential Runoff. Environ. Sci. Technol. 2012, 46, 1489–1495. DOI: 10.1021/es202904x.
  • Sadaria, A. M.; Labban, C. W.; Steele, J. C.; Maurer, M. M.; Halden, R. U. Retrospective Nationwide Occurrence of Fipronil and Its Degradates in US Wastewater and Sewage Sludge from 2001-2016. Water Res. 2019, 155, 465–473. DOI: 10.1016/j.watres.2019.02.045.
  • Companhia Ambiental do Estado de São Paulo. Qualidade das Águas Superficiais no Estado de São Paulo 2017. CETESB, São Paulo, 2018. https://cetesb.sp.gov.br/aguas-interiores/wp-content/uploads/sites/12/2018/06/Relatório-de-Qualidade-das-Águas-Interiores-no-Estado-de-São-Paulo-2017.pdf. (accessed Sep 28, 2022).
  • Marchesan, E.; Sartori, G. M. S.; Avila, L. A.; Machado, S. L. O.; Zanella, R.; Primel, E. G.; Macedo, V. R. M.; Marchezan, M. G. Residues of Pesticides in the Water of the Depression Central Rivers in the State of Rio Grande Do Sul, Brazil. Cienc. Rural Times 2010, 40, 1053–1059. DOI: 10.1590/S0103-84782010005000078.
  • Miller, J. L.; Schmidt, T. S.; Van Metre, P. C.; Mahler, B. J.; Sandstrom, M. W.; Nowell, L. H.; Carlisle, D. M.; Moran, P. W. Common Insecticide Disrupts Aquatic Communities: A Mesocosm-to-Field Ecological Risk Assessment of Fipronil and Its Degradates in US Streams. Sci. Adv. 2020, 6, eabc1299. DOI: 10.1126/sciadv.abc1299.
  • Kurz, M. H. S.; Martel, S.; Gonçalves, F. F.; Prestes, O. D.; Martins, M. L.; Zanella, R.; Adaime, M. B. Development of a Fast Method for the Determination of the Insecticide Fipronil and Its Metabolites in Environmental Waters by SPE and GC-ECD. J. Braz. Chem. Soc. 2013, 24, 631–638.
  • Brennan, A. A.; Harwood, A. D.; You, J.; Landrum, P. F.; Lydy, M. J. Degradation of Fipronil in Anaerobic Sediments and the Effect on Porewater Concentrations. Chemosphere 2009, 77, 22–28. DOI: 10.1016/j.chemosphere.2009.06.019.
  • Lin, K.; Haver, D.; Oki, L.; Gan, J. Transformation and Sorption of Fipronil in Urban Stream Sediments. J. Agric. Food Chem. 2008, 56, 8594–8600. DOI: 10.1021/jf8018886.
  • Margarido, T. C. S.; Felício, A. A.; de Cerqueira Rossa-Feres, D.; Almeida, E. A. Biochemical Biomarkers in Scinax fuscovarius Tadpoles Exposed to a Commercial Formulation of the Pesticide Fipronil. Mar. Environ. Res. 2013, 91, 61–67. DOI: 10.1016/j.marenvres.2013.02.001.
  • Dallarés, S.; Dourado, P.; Sanahuja, I.; Solovyev, M.; Gisbert, E.; Montemurro, N.; Torreblanca, A.; Blázquez, M.; Solé, M. Multibiomarker Approach to Fipronil Exposure in the Fish Dicentrarchus labrax under Two Temperature Regimes. Aquat. Toxicol. 2020, 219, 105378. DOI: 10.1016/j.aquatox.2019.105378.
  • Gupta, S. K.; Pal, A. K.; Sahu, N. P.; Saharan, N.; Prakash, C.; Akhtar, M. S.; Kumar, S. Haemato-Biochemical Responses in Cyprinus carpio (Linnaeus, 1758) Fry Exposed to Sub-Lethal Concentration of a Phenylpyrazole Insecticide, Fipronil. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 2014, 84, 113–122. DOI: 10.1007/s40011-013-0201-y.
  • Ardeshir, R. A.; Zolgharnein, H.; Movahedinia, A.; Salamat, N.; Zabihi, E. Comparison of Waterborne and Intraperitoneal Exposure to Fipronil in the Caspian white Fish (Rutilus frisii) on Acute Toxicity and Histopathology. Toxicol. Rep. 2017, 4, 348–357. DOI: 10.1016/j.toxrep.2017.06.010.
  • Wagner, S. D.; Kurobe, T.; Hammock, B. G.; Lam, C. H.; Wu, G.; Vasylieva, N.; Gee, S. J.; Hammock, B. D.; Teh, S. J. Developmental Effects of Fipronil on Japanese Medaka (Oryzias latipes) Embryos. Chemosphere 2017, 166, 511–520. DOI: 10.1016/j.chemosphere.2016.09.069.
  • Ghaffar, A.; Hussain, R.; Abbas, G.; Kalim, M.; Khan, A.; Ferrando, S.; Gallus, L.; Ahmed, Z. Fipronil (Phenylpyrazole) Induces Hemato-Biochemical, Histological and Genetic Damage at Low Doses in Common Carp, Cyprinus carpio (Linnaeus, 1758). Ecotoxicology 2018, 27, 1261–1271. DOI: 10.1007/s10646-018-1979-4.
  • Silva Pinto, T. d.; Moreira, R. A.; da ilva, L.; Yoshii, M. P. C.; Goulart, B. V.; Fraga, P. D.; Montagner, C. C.; Daam, M. A.; Espindola, E. L. G. Impact of 2, 4-D and Fipronil on the Tropical Midge Chironomus sancticaroli (Diptera: Chironomidae). Ecotoxicol. Environ. Saf. 2021, 209, 111778. DOI: 10.1016/j.ecoenv.2020.111778.
  • McKenzie, D. J.; Garofalo, E.; Winter, M.; Ceradini, S.; Verweij, F.; Day, N.; Hayes, R.; Van der Oost, R.; Butler, P.; Chipman, J.; others. Complex Physiological Traits as Biomarkers of the Sub-Lethal Toxicological Effects of Pollutant Exposure in Fishes. Philos. Trans. R. Soc. B: Biol. Sci. 2007, 362, 2043–2059. DOI: 10.1098/rstb.2007.2100.
  • Villares-Junior, G.; Cardone, I.; Goitein, R. Comparative Feeding Ecology of Four Syntopic Hypostomus Species in a Brazilian Southeastern River. Braz. J. Biol. 2016, 76, 692–699. DOI: 10.1590/1519-6984.00915.
  • Brosset, P.; Cooke, S. J.; Schull, Q.; Trenkel, V. M.; Soudant, P.; Lebigre, C. Physiological Biomarkers and Fisheries Management. Rev. Fish Biol. Fish. 2021, 31, 797–819. DOI: 10.1007/s11160-021-09677-5.
  • Organization for Economic Cooperation and Development. Test No. 218: Sediment-Water Chironomid Toxicity Using Spiked Sediment. OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing: Paris, 2004. DOI: 10.1787/9789264070264-en.
  • Arrate, J. A.; Rodriguez, P.; Martinez-Madrid, M. Tubifex tubifex Chronic Toxicity Test Using Artificial Sediment: Methodological Issues. Limnetica 2004, 23, 25–36. DOI: 10.23818/limn.23.03.
  • da Cunha-Santino, M. B.; Bianchini, I. Tropical Macrophyte Degradation Dynamics in Freshwater Sediments: Relationship to Greenhouse Gas Production. J. Soils Sediments 2013, 13, 1461–1468. DOI: 10.1007/s11368-013-0735-x.
  • American Veterinary Medical Association. 2000 Report of the AVMA Panel on Euthanasia. J. Am. Vet. Med. Assoc 2001, 218, 669–696.
  • Conselho Nacional de Controle e Experimentação Animal. Diretrizes da prática de eutanásia do CONCEA; Ministério da Ciência, Tecnologia e Inovação, Brasília, Brasil, 2013; p 54.
  • Hill, J.; Davison, W.; Forster, M. The Effects of Fish Anaesthetics (MS222, Metomidate and AQUI-S) on Heart Ventricle, the Cardiac Vagus and Branchial Vessels from Chinook Salmon (Oncorhynchus tshawytscha). Fish. Physiol. Biochem. 2002, 27, 19–28. DOI: 10.1023/B:FISH.0000021742.30567.2d.
  • Monteiro, D. A.; Taylor, E. W.; Rantin, F. T.; Kalinin, A. L. Impact of Waterborne and Trophic Mercury Exposures on Cardiac Function of Two Ecologically Distinct Neotropical Freshwater Fish Brycon amazonicus and Hoplias malabaricus. Comp. Biochem. Physiol. Part - C: Toxicol. 2017, 201, 26–34. DOI: 10.1016/j.cbpc.2017.09.004.
  • Monteiro, D. A.; Lopes, A. G.; Jejcic, N. U.; Silva Vasconcelos, E.; Da; Kalinin, A. L.; Rantin, F. T. Cardiac Contractility of the African Sharptooth Catfish, Clarias gariepinus: Role of Extracellular Ca2+, Sarcoplasmic Reticulum, and β-Adrenergic Stimulation. Fish. Physiol. Biochem. 2021, 47, 1969–1982.
  • Costa, M. J.; Rivaroli, L.; Rantin, F. T.; Kalinin, A. L. Cardiac Tissue Function of the Teleost Fish Oreochromis niloticus under Different Thermal Conditions. J. Therm. Biol. 2000, 25, 373–379. DOI: 10.1016/s0306-4565(99)00109-6.
  • Smith, G. L.; Allen, D. Effects of Metabolic Blockade on Intracellular Calcium Concentration in Isolated Ferret Ventricular Muscle. Circ. Res. 1988, 62, 1223–1236. DOI: 10.1161/01.res.62.6.1223.
  • Grupp, G.; Grupp, I. L.; Ghysel-Burton, J.; Godfraind, T.; De Pover, A.; Schwartz, A. Contractile Force Effects of Low Concentrations of Ouabain in Isolated Guinea Pig, Rabbit, Cat, and Rat Atria and Ventricles. In Current Topics in Membranes and Transport; Bronner, F.; Kleinzeller, A., Eds.; Academic Press, Elsevier, 1983; Vol. 19; pp. 897–902.
  • Vasilets, L. A.; Takeda, K.; Kawamura, M.; Schwarz, W. Significance of the Glutamic Acid Residues Glu334, Glu959, and Glu960 of the α Subunits of Torpedo Na+,K+ Pumps for Transport Activity and Ouabain Binding. Biochim. Biophys. Acta 1998, 1368, 137–149. DOI: 10.1016/s0005-2736(97)00195-8.
  • Rocha, M. L.; Rantin, F. T.; Kalinin, A. L. Effects of Temperature and Calcium Availability on Cardiac Contractility in Synbranchus marmoratus, a Neotropical Teleost. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2007, 146, 544–550. DOI: 10.1016/j.cbpa.2006.03.002.
  • Layland, J.; Young, I. S.; Altringham, J. D. The Length Dependence of Work Production in Rat Papillary Muscles in Vitro. J. Exp. Biol. 1995, 198, 2491–2499. DOI: 10.1242/jeb.198.12.2491.
  • Celichowski, J.; Bichler, E. The Time Course of the Last Contractions during Incompletely Fused Tetani of Motor Units in Rat Skeletal Muscle. Acta Neurobiol. Exp. 2002, 62, 7–18.
  • Thomaz, J. M.; Martins, N. D.; Monteiro, D. A.; Rantin, F. T.; Kalinin, A. L. Cardio-Respiratory Function and Oxidative Stress Biomarkers in Nile Tilapia Exposed to the Organophosphate Insecticide Trichlorfon (NEGUVON®). Ecotoxicol. Environ. Saf. 2009, 72, 1413–1424. DOI: 10.1016/j.ecoenv.2008.11.003.
  • Matikainen, N.; Vornanen, M. Effect of Season and Temperature Acclimation on the Function of Crucian Carp (Carassius carassius) Heart. J. Exp. Biol. 1992, 167, 203–220. DOI: 10.1242/jeb.167.1.203.
  • Shiels, H.; Farrell, A. The Effect of Temperature and Adrenaline on the Relative Importance of the Sarcoplasmic Reticulum in Contributing Ca2+ to Force Development in Isolated Ventricular Trabeculae from Rainbow Trout. J. Exp. Biol. 1997, 200, 1607–1621. DOI: 10.1242/jeb.200.11.1607.
  • Rodnick, K. J.; Gesser, H. Cardiac Energy Metabolism. In Fish Physiology; Gamperl, A. K.; Gillis, T. E.; Farrell, A. P.; Brauner, C. J., Eds.; Academic Press, Elsevier, 2017; Vol. 36; pp. 317–367.
  • Gamperl, A. K.; Farrell, A. P. Cardiac Plasticity in Fishes: Environmental Influences and Intraspecific Differences. J. Exp. Biol. 2004, 207, 2539–2550. DOI: 10.1242/jeb.01057.
  • Perrichon, P.; Pasparakis, C.; Mager, E. M.; Stieglitz, J. D.; Benetti, D. D.; Grosell, M.; Burggren, W. W. Morphology and Cardiac Physiology Are Differentially Affected by Temperature in Developing Larvae of the Marine Fish Mahi-Mahi (Coryphaena hippurus). Biol. Open 2017, 15, 800–809. DOI:10.1242/bio.025692
  • King, J.; Lowery, D. R. Physiology, Cardiac Output; StatPearls Publishing: Treasure Island, FL, 2022.
  • Driedzic, W. R.; Gesser, H. Energy Metabolism and Contractility in Ectothermic Vertebrate Hearts: Hypoxia, Acidosis, and Low Temperature. Physiol. Rev. 1994, 74, 221–258. DOI: 10.1152/physrev.1994.74.1.221.
  • Shiels, H. A.; Calaghan, S. C.; White, E. The Cellular Casis for Enhanced Volume-Modulated Cardiac Output in Fish Hearts. J. Gen. Physiol. 2006, 128, 37–44. DOI: 10.1085/jgp.200609543.
  • Beggel, S.; Werner, I.; Connon, R. E.; Geist, J. P. Impacts of the Phenylpyrazole Insecticide Fipronil on Larval Fish: Time-Series Gene Transcription Responses in Fathead Minnow (Pimephales promelas) following Short-Term Exposure. Sci. Total Environ. 2012, 426, 160–165. DOI: 10.1016/j.scitotenv.2012.04.005.
  • El-Murr, A.; Hakim, Y.; Imam, T. S.; Ghonimi, W. A. Histopathological, Immunological, Hematological and Biochemical Effects of Fipronil on Nile Tilapia (Oreochromis niloticus). J. Vet. Sci. Technol. 2015, 6, 1–9. DOI: 10.4172/2157-7579.1000252
  • Petitjean, Q.; Jean, S.; Gandar, A.; Côte, J.; Laffaille, P.; Jacquin, L. Stress Responses in Fish: From Molecular to Evolutionary Processes. Sci. Total Environ. 2019, 684, 371–380. DOI: 10.1016/j.scitotenv.2019.05.357.
  • Barton, B. A. Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids. Integr. Comp. Biol. 2002, 42, 517–525. DOI: 10.1093/icb/42.3.517.
  • Bownik, A.; Szabelak, A. Short-Term Effects of Pesticide Fipronil on Behavioral and Physiological Endpoints of Daphnia magna. Environ. Sci. Pollut. Res. Int. 2021, 28, 33254–33264. DOI: 10.1007/s11356-021-13091-6.
  • Mason, K. P.; Lönnqvist, P.-A. Bradycardia in Perspective-Not All Reductions in Heart Rate Need Immediate Intervention. Paediatr. Anaesth. 2015, 25, 44–51. DOI: 10.1111/pan.12584.
  • Costa, M. J.; Monteiro, D. A.; Oliveira-Neto, A. L.; Rantin, F. T.; Kalinin, A. L. Oxidative Stress Biomarkers and Heart Function in Bullfrog Tadpoles Exposed to Roundup Original®. Ecotoxicology 2008, 17, 153–163. DOI: 10.1007/s10646-007-0178-5.
  • Bers, D. M. Cardiac Excitation–Contraction Coupling. Nature 2002, 415, 198–205. DOI: 10.1038/415198a.
  • Wang, Y.; Shi, Q.; Li, M.; Zhao, M.; Reddy Gopireddy, R.; Teoh, J.-P.; Xu, B.; Zhu, C.; Ireton, K. E.; Srinivasan, S.; et al. Intracellular β 1 -Adrenergic Receptors and Organic Cation Transporter 3 Mediate Phospholamban Phosphorylation to Enhance Cardiac Contractility. Circ. Res. 2021, 128, 246–261. DOI: 10.1161/CIRCRESAHA.120.317452.
  • Li, L.; Cai, H.; Liu, H.; Guo, T. β-Adrenergic Stimulation Activates Protein Kinase Cε and Induces Extracellular Signal-Regulated Kinase Phosphorylation and Cardiomyocyte Hypertrophy. Mol. Med. Rep. 2015, 11, 4373–4380. DOI: 10.3892/mmr.2015.3316.
  • Driedzic, W. R.; Gesser, H. Ca2+ Protection from the Negative Inotropic Effect of Contraction Frequency on Teleost Hearts. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 1985, 156, 135–142. DOI: 10.1007/BF00692936.
  • Shiels, H. A.; Vornanen, M.; Farrell, A. P. The Force–Frequency Relationship in Fish Hearts - a Review. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 132, 811–826. DOI: 10.1016/s1095-6433(02)00050-8.
  • Pieske, B.; Sütterlin, M.; Schmidt-Schweda, S.; Minami, K.; Meyer, M.; Olschewski, M.; Holubarsch, C.; Just, H.; Hasenfuss, G. Diminished Post-Rest Potentiation of Contractile Force in Human Dilated Cardiomyopathy. Functional Evidence for Alterations in Intracellular Ca2+ Handling. J. Clin. Invest. 1996, 98, 764–776. DOI: 10.1172/JCI118849.
  • Aho, E.; Vornanen, M. Contractile Properties of Atrial and Ventricular Myocardium of the Heart of Rainbow Trout Oncorhynchus mykiss: Effects of Thermal Acclimation. J. Exp. Biol. 1999, 202, 2663–2677. DOI: 10.1242/jeb.202.19.2663.
  • Rivaroli, L. Respostas cronotrópicas e inotrópicas do miocárdio ventricular de três espécies de peixes tropicais ecologicamente distintas: curimbatá, Prochilodus lineatus, traíra, Hoplias malabaricus, e cascudo, Hypostomus regani. Unpublished MSc. Dissertation, Federal University of São Carlos, São Carlos, S.P., Brazil, 2002.
  • McKenzie, D. J.; Campbell, H. A.; Taylor, E. W.; Micheli, M.; Rantin, F. T.; Abe, A. S. The Autonomic Control and Functional Significance of the Changes in Heart Rate Associated with Air Breathing in the Jeju, Hoplerythrinus unitaeniatus. J. Exp. Biol. 2007, 210, 4224–4232. DOI: 10.1242/jeb.009266.
  • Nelson, J. A.; Rios, F.; Sanches, J.; Fernandes, M.; Rantin, F. T. Environmental Influences on the Respiratory Physiology and Gut Chemistry of a Facultatively Air-Breathing, Tropical Herbivorous Fish (Hypostomus Regani). In Fish Respiration and Environment, Science Publishers: Enfield, USA, 2007; pp. 191–217.
  • Belão, T. C.; Leite, C. A. C.; Florindo, L. H.; Kalinin, A. L.; Rantin, F. T. Cardiorespiratory Responses to Hypoxia in the African Catfish, Clarias gariepinus (Burchell 1822), an Air-Breathing Fish. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 2011, 181, 905–916.
  • Hove-Madsen, L.; Tort, L. Characterization of the Relationship between Na+–Ca2+ Exchange Rate and Cytosolic Calcium in Trout Cardiac Myocytes. Pflug. Arch. Eur. J. Physiol. 2001, 441, 701–708. DOI: 10.1007/s004240000470.
  • Vornanen, M.; Shiels, H. A.; Farrell, A. P. Plasticity of Excitation–Contraction Coupling in Fish Cardiac Myocytes. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2002, 132, 827–846. DOI: 10.1016/s1095-6433(02)00051-x.
  • Bers, D. M. Calcium Cycling and Signaling in Cardiac Myocytes. Annu. Rev. Physiol. 2008, 70, 23–49. DOI: 10.1146/annurev.physiol.70.113006.100455.
  • Sipido, K. R.; Volders, P. G.; Vos, M. A.; Verdonck, F. Altered Na/Ca Exchange Activity in Cardiac Hypertrophy and Heart Failure: A New Target for Therapy? Cardiovasc. Res. 2002, 53, 782–805. DOI: 10.1016/s0008-6363(01)00470-9.
  • Hudecova, S.; Kubovcakova, L.; Kvetnansky, R.; Kopacek, J.; Pastorekova, S.; Novakova, M.; Knezl, V.; Tarabova, B.; Lacinova, L.; Sulova, Z.; et al. Modulation of Expression of Na+/Ca2+ Exchanger in Heart of Rat and Mouse under Stress. Acta Physiol. (Oxf) 2007, 190, 127–136. DOI: 10.1111/j.1748-1716.2007.01673.x.
  • Deslauriers, Y.; Ruiz-Ceretti, E.; Schanne, O. F.; Payet, M. D. The Toxic Effects of Ouabain: A Voltage-Clamp Study. Can. J. Physiol. Pharmacol. 1982, 60, 1153–1159. DOI: 10.1139/y82-167.
  • Herzig, S.; Mohr, K. Action of Ouabain on Rat Heart: Comparison with Its Effect on Guinea-Pig Heart. Br. J. Pharmacol. 1984, 82, 135–142. DOI: 10.1111/j.1476-5381.1984.tb16450.x.
  • Langer, G. A. Effects of Digitalis on Myocardial Ionic Exchange. Circulation 1972, 46, 180–187. DOI: 10.1161/01.cir.46.1.180.
  • Vemuri, R.; Philipson, K. Influence of Sterols and Phospholipids on Sarcolemmal and Sarcoplasmic Reticular Cation Transporters. J. Biol. Chem. 1989, 264, 8680–8685. DOI: 10.1016/S0021-9258(18)81846-4.
  • Ottolia, M.; Torres, N.; Bridge, J. H. B.; Philipson, K. D.; Goldhaber, J. I. Na/Ca Exchange and Contraction of the Heart. J. Mol. Cell Cardiol. 2013, 61, 28–33. DOI: 10.1016/j.yjmcc.2013.06.001.
  • Satoh, H.; Ginsburg, K. S.; Qing, K.; Terada, H.; Hayashi, H.; Bers, D. M. KB-R7943 Block of Ca 2+ Influx via Na+/Ca2+ Exchange Does Not Alter Twitches or Glycoside Inotropy but Prevents Ca2+ Overload in Rat Ventricular Myocytes. Circulation 2000, 101, 1441–1446. DOI: 10.1161/01.cir.101.12.1441.
  • Bögeholz, N.; Pauls, P.; Bauer, B. K.; Schulte, J. S.; Frommeyer, G.; Dechering, D. G.; Boknik, P.; Kirchhefer, U.; Müller, F. U.; Pott, C.; others. Overexpression of the Na+/Ca2+ Exchanger Influences Ouabain-Mediated Spontaneous Ca2+ Activity but Not Positive Inotropy. Fundam. Clin. Pharmacol. 2019, 33, 43–51. DOI: 10.1111/fcp.12404.
  • Fiolet, J. W.; Baartscheer, A.; Schumacher, C. A. Transsarcolemmal Sodium-Calcium Exchange and Myocardial Oxygen Consumption in Isolated Rat Ventricular Myocytes. J. Mol. Cell Cardiol. 1991, 23, 735–748. DOI: 10.1016/0022-2828(91)90983-s.
  • Fiolet, J.; Baartscheer, A.; Schumacher, C. Intracellular [Ca2+] and VO2 after Manipulation of the Free-Energy of the Na+/Ca2+-Exchanger in Isolated Rat Ventricular Myocytes. J. Mol. Cell Cardiol. 1995, 27, 1513–1525. DOI: 10.1016/s0022-2828(95)90260-0.
  • Rantin, F.; Gesser, H.; Kalinin, A.; Guerra, C.; De Freitas, J.; Driedzic, W. Heart Performance, Ca2+ Regulation and Energy Metabolism at High Temperatures in Bathygobius soporator, a Tropical Marine Teleost. J. Therm. Biol. 1998, 23, 31–39. DOI: 10.1016/S0306-4565(97)00043-0.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.