Skip to main content
SpringerLink
Log in

Acute effects of β-naphthoflavone on cardiorespiratory function and metabolism in adult zebrafish (Danio rerio)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Aryl hydrocarbon receptor (AhR) agonists are known to cause lethal cardiovascular deformities in fish after developmental exposure. Acute adult fish toxicity of AhR agonists is thought to be minimal, but limited evidence suggests sublethal effects may also involve the cardiac system in fish. In the present study, adult zebrafish (Danio rerio) were aqueously exposed to solvent control or three nominal concentrations of the commonly used model AhR agonist, β-naphthoflavone (BNF), for 48 h. Following exposure, fish were subjected to echocardiography to determine cardiac function or swimming tests with concurrent oxygen consumption measurement. Critical swimming speed and standard metabolic rate were not significantly changed, while active metabolic rate decreased with increasing BNF exposure, reaching statistical significance at the highest BNF exposure. Factorial aerobic scope was the most sensitive end-point and was decreased at even lower BNF concentrations, indicating a reduced aerobic capacity after acute AhR agonist exposure in adult fish. The highest BNF concentration caused a significant decrease in cardiac output, while increasing the ratio of atrial to ventricular heart rate (indicating atrioventricular conduction blockade). In conclusion, the effect of acute BNF exposure on zebrafish metabolic capacity and cardiac function is likely to be physiologically important given that fish have a critical need for adequate oxygen to fuel essential survival behaviors such as swimming, growth, and reproduction. Future studies should be directed at examining the effects of other polycyclic aromatic hydrocarbons on fish cardiorespiratory function to determine whether their effects and modes of action are similar to BNF.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AhR:

Aryl hydrocarbon receptor

BNF:

β-Naphthoflavone

U crit :

Critical swimming speed

MO2 :

Oxygen consumption rate

SMR:

Standard metabolic rate

AMR:

Active metabolic rate

F-AS:

Factorial aerobic scope

U i :

Highest velocity maintained for an entire time interval during swim testing

T i :

Time that elapsed at fatigue velocity

U ii :

Increment by which water velocity was increased for each interval during swim testing

T ii :

Time for each swimming velocity interval

Q :

Cardiac output

f H :

Heart rate

V S :

Stroke volume

References

  • Aluru N, Vijayan MM (2004) β-naphthoflavone disrupts cortisol production and liver glucocorticoid responsiveness in rainbow trout. Aquat Toxicol 67:273–285

    Article  CAS  PubMed  Google Scholar 

  • Bains OS, Kennedy CJ (2004) Energetic costs of pyrene metabolism in isolated hepatocytes of rainbow trout, Oncorhynchus mykiss. Aquat Toxicol 67:217–226

    Article  CAS  PubMed  Google Scholar 

  • Beyers DW, Rice JA, Clements WH, Henry CJ (1999) Estimating physiological cost of chemical exposure: integrating energetics and stress to quantify toxic effects in fish. Can J Fish Aquat Sci 56:814–822

    Article  CAS  Google Scholar 

  • Billiard SM, Timme-Laragy AR, Wassgenberg DM, Cockman C, Di Giulio RT (2006) The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity to polycyclic aromatic hydrocarbons in zebrafish. Toxicol Sci 92:526–536

    Article  CAS  PubMed  Google Scholar 

  • Blank JM, Morrissette JM, Davie PS, Block BA (2002) Effects of temperature, epinephrine and Ca2+ on the hearts of yellowfish tuna (Thunnus albacores). J Exp Biol 205:1881–1888

    CAS  PubMed  Google Scholar 

  • Blank JM, Morrissette JM, Landeira-Fernandez AM, Blackwell SB, Williams TD, Lock BA (2004) In situ cardiac performance of Pacific bluefin tuna hearts in response to acute temperature change. J Exp Biol 207:881–890

    Article  PubMed  Google Scholar 

  • Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183–1226

    Article  Google Scholar 

  • Claireaux G, Davoodi F (2010) Effect of exposure to petroleum hydrocarbons upon cardio-respiratory function in the common sole (Solea solea). Aquat Toxicol 98:113–119

    Article  CAS  PubMed  Google Scholar 

  • Di Bello D, Vaccaro E, Longo V, Regoli F, Nigro M, Benedetti MPG, Pretti C (2007) Presence and inducibility by β-naphthoflavone of CYP1A1, CYP1B1 and phase II enzymes in Trematomus bernacchii, an Antarctic fish. Aquat Toxicol 84:19–26

    Article  PubMed  Google Scholar 

  • Diercks AR, Highsmith RC, Asper VL, Joung DJ, Zhou ZZ, Guo LD et al (2010) Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site. Geophys Res Lett 37:L20602. doi:10.1029/2010GL045046

    Article  Google Scholar 

  • Gomez-Duran A, Carvajal-Gonzalez JM, Mulero-Navarro S, Santiago-Josefat B, Puga A, Fernandez-Salguero PM (2009) Fitting a xenobiotic receptor into cell homeostasis: How the dioxin receptor interacts with TGFβ signaling. Biochem Pharmacol 77:700–712

    Article  CAS  PubMed  Google Scholar 

  • Hill AJ, Teraoka H, Heideman W, Peterson RE (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86:6–19

    Article  CAS  PubMed  Google Scholar 

  • Hu N, Yost HJ, Clark EB (2001) Cardiac morphology and blood pressure in adult zebrafish. Anat Rec 264:1–12

    Article  CAS  PubMed  Google Scholar 

  • Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharm 196:191–205

    Article  CAS  Google Scholar 

  • Incardona JP, Carls MG, Teraoka H, Sloan CA, Collier TK, Sholz NL (2005) Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ Health Perspect 113:1755–1762

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Incardona JP, Carls MG, Day HL, Sloan CA, Bolton JL, Collier TK, Scholz NL (2009) Cardiac arrhythmia is the primary response of embryonic Pacific herring (Clupea pallasi) exposed to crude oil during weathering. Environ Sci Technol 43:201–207

    Article  CAS  PubMed  Google Scholar 

  • Itakura T, El-Kady M, Mitsuo R, Kaminishi Y (2005) Complementary DNA cloning and constitutive expression of cytochrome P450 1C1 in the gills of carp (Cyprinus carpio). Environ Sci 12(2):111–120

    CAS  PubMed  Google Scholar 

  • Jain KE, Birtwell IK, Farrell AP (1998) Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Can J Zool 76:1488–1496

    Article  Google Scholar 

  • Karchner SI, Franks DG, Hahn ME (2005) AHR1B, a new functional aryl hydrocarbon receptor in zebrafish: tandem arrangement of ahr1b and ahr2 genes. Biochemistry 392:153–161

    Article  CAS  Google Scholar 

  • Kennedy CJ, Farrell AP (2006) Effects of exposure to the water-soluble fraction of crude oil on the swimming performance and the metabolic ionic recovery post-exercise in Pacific herring (Clupea pallasi). Environ Toxicol Chem 25:2715–2724

    Article  CAS  PubMed  Google Scholar 

  • Killen SS, Costa I, Brown JA, Gamperl AK (2007) Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proc R Soc B 274:431–438

    Article  PubMed Central  PubMed  Google Scholar 

  • Korashy HM, El-Kadi AO (2006) The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular disease. Drug Metab Rev 38:411–450

    Article  CAS  PubMed  Google Scholar 

  • Latimer JS, Zheng J (2003) The sources, transport, and fate of PAHs in the marine environment. In: Douben PET (ed) PAHs: an eco-toxicological perspective. Wiley, West Sussex, pp 9–33

    Google Scholar 

  • MacKinnon DL, Farrell AP (1992) The effect of 2-(thiocyanomethyl) benzothiazole on juvenile coho salmon (Oncorhynchus kisutch): sublethal toxicity testing. Environ Toxicol Chem 11:1541–1548

    Article  CAS  Google Scholar 

  • Mager EM, Grosell M (2011) Effects of acute and chronic waterborne lead exposure on the swimming performance and aerobic scope of fathead minnows (Pimephales promelas). Comp Biochem Physiol Part C 154:7–13

    Google Scholar 

  • Marit JS, Weber LP (2012) Persistent effects on adult swim performance and energetics in zebrafish developmentally exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Aquat Toxicol 106–107:131–139

    Article  PubMed  Google Scholar 

  • McKenzie DJ, Garofalo E, Winter MJ, Ceradini S, Verweij F, Day N, Hayes R, van der Oost R, Butler PJ, Chipman JK, Taylor EW (2007) Complex physiological traits as biomarkers of the sub-lethal toxicological effects of pollutant exposure in fishes. Philos Trans R Soc B 362:2043–2059

    Article  CAS  Google Scholar 

  • Mercier JC, DiSessa TG, Jarmakani JM, Nakanishi T, Hiraishi S, Isabel-Jones J, Friedman WF (1982) Two-dimensional echocardiographic assessment of left ventricular volumes and ejection fraction in children. Circulation 65:962–969

    Article  CAS  PubMed  Google Scholar 

  • Nebert DW, Dalton TP, Okey AB, Gonzalez FJ (2004) Role of aryl hydrocarbon receptor mediated induction of the CYP1A enzymes in environmental toxicity and cancer. J Biol Chem 279:23847–23850

    Article  CAS  PubMed  Google Scholar 

  • Olson KR, Farrell AP (2006) The cardiovascular system. In: Mann DL, Zipes DP, Libby P (eds) The physiology of fishes, 3rd edn. CRC Press, Taylor & Francis Group, Boca Raton, FL, pp 119–152

  • Pacheco M, Santos MA (2001) Biotransformation, endocrine, and genetic responses of Anguilla anguilla L. to petroleum distillate products and environmentally contaminated waters. Ecotoxicol Environ Saf 49:64–75

    Article  CAS  PubMed  Google Scholar 

  • Pacheco M, Santos MA (2002) Naphthalene and β-naphthoflavone effects on Anguilla anguilla L. hepatic metabolism and erythrocytic abnormalities. Environ Int 28:285–293

    Article  CAS  PubMed  Google Scholar 

  • Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol 131:41–50

    Article  CAS  Google Scholar 

  • Schmidt JV, Bradfield CA (1996) AH receptor signaling pathways. Annu Rev Cell Dev Biol 12:55–89

    Article  CAS  PubMed  Google Scholar 

  • Shingles A, McKenzie DJ, Taylor EW, Moretti A, Butler PJ, Ceradini S (2001) Effects of sublethal ammonia exposure on swimming performance in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204:2691–2698

    CAS  PubMed  Google Scholar 

  • Smith EM, Wilson JY (2010) Assessment of cytochrome P450 fluorometric substrates with rainbow trout and killifish exposed to dexamethasone, pregnenolone-16α-carbonitrile, rifampicin, and β-naphthoflavone. Aquat Toxicol 97(4):324–333

    Article  CAS  PubMed  Google Scholar 

  • Smolders R, Bervoets L, De Boeck G, Blust R (2002) Integrated condition indices as a measure of whole effluent toxicity in zebrafish (Danio rerio). Environ Toxicol Chem 21:87–93

    Article  CAS  PubMed  Google Scholar 

  • Sprague JB (1971) Measurement of pollutant toxicity in fish – III: sublethal effects and “safe” concentrations. Water Res 5:245–266

    Article  CAS  Google Scholar 

  • Sun L, Lien C, Xu X, Shung KK (2008) In vivo cardiac imaging of adult zebrafish using high frequency ultrasound (45-75 MHz). Ultrasound Med Biol 34:31–39

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas JK, Janz DM (2011) Dietary selenomethionine exposure in adult zebrafish alters swimming performance, energetics, and the physiological stress response. Aquat Toxicol 102:79–86

    Article  CAS  PubMed  Google Scholar 

  • Thomas JK, Wiseman S, Giesy JP, Janz DM (2013) Effects of chronic dietary selenomethionine exposure on repeat swimming performance, aerobic metabolism and methionine catabolism in adult zebrafish (Danio rerio). Aquat Toxicol 130–131:112–122

    Article  PubMed  Google Scholar 

  • Tintos A, Gesto M, Míguez JM, Soengas JL (2008) β-Naphthoflavone and benzo(a)pyrene treatment affect liver intermediary metabolism and plasma cortisol levels in rainbow trout Oncorhynchus mykiss. Ecotoxicol Environ Saf 69:180–186

    Article  CAS  PubMed  Google Scholar 

  • Visualsonics (2008) VisualSonics workbook: guide to micro-echocardiography study using the Vevo 770, Rev.1.0. VisualSonics Inc., Markham

    Google Scholar 

  • Wang Q, Chen J, Ko CI, Fan Y, Carreira V, Chen Y et al (2013) Disruption of aryl hydrocarbon receptor homeostatic levels during embryonic stem cell differentiation alters expression of homeobox transcription factors that control cardiomyogenesis. Environ Health Perspect 121:1331–1343

    Google Scholar 

  • Xiong KM, Peterson RE, Heideman W (2008) AHR-mediated down-regulation of Sox9b causes jaw malformation in zebrafish embryos. Mol Pharm 74:1544–1553  

  • Zhang N, Agbor LN, Scott JA, Zalowbowski T, Elased KM, Trujillo A et al (2010) An activated renin-angiotensin system maintains normal blood pressure in aryl hydrocarbon receptor heterozygous mice but not in null mice. Biochem Pharmacol 80:197–201

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Huang L, Zuo Z, Chen Y, Wang C (2013) Phenanthrene causes cardiac arrhythmia in embryonic zebrafish via perturbing calcium handling. Aquat Toxicol 142–143:26–32

    Article  PubMed  Google Scholar 

  • Zipes DP (1997) Specific arrhythmias: diagnosis and treatment. In: Braunwald E (ed) Heart disease: a textbook of cardiovascular medicine, 5th edn. W.B. Saunders Company, Philadelphia, pp 640–704

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Natural Sciences and Engineering Research Council of Canada (NSERC) for providing research funds for the work in this study (Discovery Grant to LPW) and a postgraduate scholarship (PGS-M to CJG).

Author information

Authors and Affiliations

  1. Toxicology Centre, University of Saskatchewan, Saskatoon, SK, S7N 5B3, Canada

    Courtney J. Gerger, Jith K. Thomas, David M. Janz & Lynn P. Weber

  2. Department of Veterinary Biomedical Sciences, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK, S7N 5B4, Canada

    Courtney J. Gerger, David M. Janz & Lynn P. Weber

Authors
  1. Courtney J. Gerger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jith K. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David M. Janz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lynn P. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lynn P. Weber.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gerger, C.J., Thomas, J.K., Janz, D.M. et al. Acute effects of β-naphthoflavone on cardiorespiratory function and metabolism in adult zebrafish (Danio rerio). Fish Physiol Biochem 41, 289–298 (2015). https://doi.org/10.1007/s10695-014-9982-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-014-9982-z

Keywords

Search

Navigation