A bioenergetics assay for studying the effects of environmental stressors on mitochondrial function in vivo in zebrafish larvae

Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology

Volumn 192, Issue , 2017, Pages 23-32

  Raftery, Tara D ^a   Jayasundara, Nishad ^a   Di Giulio, Richard T ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Bioenergetics; Development; Mitochondria; Oxygen consumption; Polycyclic aromatic hydrocarbons (PAHs); Respiration; Triclosan; Zebrafish

Indexed keywords

BENZO( A )PYRENE; FLUORANTHENE; PHENANTHRENE; POLYCYCLIC AROMATIC HYDROCARBON; TRICAINE; TRICLOSAN; UNCLASSIFIED DRUG; BENZO[A]PYRENE; FLUORENE DERIVATIVE; PHENANTHRENE DERIVATIVE; POLLUTANT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BASAL METABOLIC RATE; BIOASSAY; BIOENERGETICS ASSAY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENVIRONMENTAL STRESS; FEMALE; HEART RATE; LARVA; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TOXICITY; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY CHAIN; ZEBRA FISH; ANIMAL; CELL RESPIRATION; DOSE RESPONSE; DRUG EFFECTS; ENERGY METABOLISM; METABOLIC FLUX ANALYSIS; METABOLISM; MITOCHONDRION; POLLUTANT; REPRODUCIBILITY; TIME FACTOR; TOXICITY;

ANIMALS; BENZO(A)PYRENE; CELL RESPIRATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; ENVIRONMENTAL POLLUTANTS; FLUORENES; HEART RATE; LARVA; METABOLIC FLUX ANALYSIS; MITOCHONDRIA; OXYGEN CONSUMPTION; PHENANTHRENES; POLYCYCLIC AROMATIC HYDROCARBONS; REPRODUCIBILITY OF RESULTS; TIME FACTORS; TRICLOSAN; ZEBRAFISH;

EID: 85002625494     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2016.12.001     Document Type: Article

References (73)

1. Addya, S., Anandatheerthavarada, H.K., Biswas, G., Bhagwat, S.V., Mullick, J., Avadhani, N.G., Targeting of NH2-terminal-processed microsomal protein to mitochondria: a novel pathway for the biogenesis of hepatic mitochondrial P450MT2. J. Cell Biol. 139 (1997), 589–599.
2. Affourtit, C., Brand, M.D., Measuring mitochondrial bioenergetics in INS-1E insulinoma cells. Methods Enzymol. 457 (2009), 405–424.
3. Agency for Toxic Substances and Disease Registry (ATSDR), Toxicological Profile for Polycyclic Aromatic Hydrocarbons (PAHs). 1995, Department of Health and Human Services, Public Health Service, Atlanta, GA.
4. Ansari, S., Ansari, B.A., Embryo and fingerling toxicity of dimethoate and effect on fecundity, viability, hatchability and survival of zebrafish, Danio rerio. World J. Fish Mar. Sci. 3 (2011), 167–173.
5. Ansari, S., Ansari, B.A., Effects of heavy metals on the embryo and larvae of zebrafish, Danio rerio (Cyprinidae). Sch. Acad. J. Biosci. 3 (2015), 52–56.
6. Arkoosh, M.R., Kaattari, S.L., Development of immunological memory in rainbow trout (Oncorhynchus mykiss). I. An immunochemical and cellular analysis of the B cell response. Dev. Comp. Immunol. 15 (1991), 279–293.
7. Arzuaga, X., Elskus, A., Polluted-site killifish (Fundulus heteroclitus) embryos are resistant to organic pollutant-mediated induction of CYP1A activity, reactive oxygen species, and heart deformities. Environ. Toxicol. Chem. 29 (2010), 676–682.
8. Backer, J.M., Weinstein, I.B., Mitochondrial DNA is a major cellular target for a dihydrodiol-epoxide derivative of benzo[a]pyrene. Science 209 (1980), 297–299.
9. Ballinger, S.W., Mitochondrial dysfunction in cardiovascular disease. Free Radic. Biol. Med. 38 (2005), 1278–1295.
10. Billiard, S.M., Timme-Laragy, A.R., Wassenberg, D.M., Cockman, C., Di Giulio, R.T., The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol. Sci. 92 (2006), 526–536.
11. Bishop, T., Brand, M.D., Processes contributing to metabolic depression in hepatopancreas cells from the snail Helix aspersa. J. Exp. Biol. 203 (2000), 3603–3612.
12. Brand, M.D., Nicholls, D.G., Assessing mitochondrial dysfunction in cells. Biochem. J. 435 (2011), 297–312.
13. Brette, F., Machado, B., Cros, C., Incardona, J.P., Scholz, N.L., Block, B.A., Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343 (2014), 772–776.
14. Brown, D.R., Bailey, J.M., Oliveri, A.N., Levin, E.D., Di Giulio, R.T., Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish. Neurotoxicol. Teratol. 53 (2016), 55–63.
15. Brown, D.R., Thompson, J., Chernick, M., Hinton, D.E., Di Giulio, R.T., Later life swimming performance and persistent heart damage following subteratogenic PAH mixture exposure in the Atlantic killifish Fundulus heteroclitus). Environ. Toxicol. Chem., 2016 (in review).
16. Burns, C.G., Milan, D.J., Grande, E.J., Rottbauer, W., MacRae, C.A., Fishman, M.C., High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat. Chem. Biol. 1 (2005), 263–264.
17. Chance, B., Williams, G.R., Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem. 217 (1955), 383–393.
18. Chapman, T.P., Hadley, G., Fratter, C., Cullen, S.N., Bax, B.E., Bain, M.D., Sapsford, R.A., Poulton, J., Travis, S.P., Unexplained gastrointestinal symptoms: think mitochondrial disease. Dig. Liver Dis. 46 (2014), 1–8.
19. Coskun, P., Wyrembak, J., Schriner, S.E., Chen, H.W., Marciniack, C., Laferla, F., Wallace, D.C., A mitochondrial etiology of Alzheimer and Parkinson disease. Biochim. Biophys. Acta 1820 (2012), 553–564.
20. Cousin, X., Cachot, J., PAHs and fish—exposure monitoring and adverse effects—from molecular to individual level. Environ. Sci. Pollut. Res. Int. 21 (2014), 13685–13688.
21. Dumollard, R., Duchen, M., Carroll, J., The role of mitochondrial function in the oocyte and embryo. Curr. Top. Dev. Biol. 77 (2007), 21–49.
22. Eisler, R., Polycyclic Aromatic Hydrocarbon Hazards to Fish, Wildlife, and Invertebrates: A Synoptic Review. 1987, U.S. Fish and Wildlife Service, Patuxent Wildlife Research Center.
23. Engeszer, R.E., Patterson, L.B., Rao, A.A., Parichy, D.M., Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4 (2007), 21–40.
24. Gerger, C.J., Thomas, J.K., Janz, D.M., Weber, L.P., Acute effects of beta-naphthoflavone on cardiorespiratory function and metabolism in adult zebrafish (Danio rerio). Fish Physiol. Biochem. 41 (2015), 289–298.
25. Gibert, Y., McGee, S.L., Ward, A.C., Metabolic profile analysis of zebrafish embryos. J. Vis. Exp., 2013, e4300.
26. Graziewicz, M.A., Sayer, J.M., Jerina, D.M., Copeland, W.C., Nucleotide incorporation by human DNA polymerase gamma opposite benzo[a]pyrene and benzo[c]phenanthrene diol epoxide adducts of deoxyguanosine and deoxyadenosine. Nucleic Acids Res. 32 (2004), 397–405.
27. Grone, B.P., Marchese, M., Hamling, K.R., Kumar, M.G., Krasniak, C.S., Sicca, F., Santorelli, F.M., Patel, M., Baraban, S.C., Epilepsy, behavioral abnormalities, and physiological comorbidities in syntaxin-binding protein 1 (STXBP1) mutant zebrafish. PLoS One, 11, 2016, e0151148.
28. Gruber, J., Ng, L.F., Fong, S., Wong, Y.T., Koh, S.A., Chen, C.B., Shui, G., Cheong, W.F., Schaffer, S., Wenk, M.R., Halliwell, B., Mitochondrial changes in ageing Caenorhabditis elegans—what do we learn from superoxide dismutase knockouts?. PLoS One, 6, 2011, e19444.
29. Hawkins, W.E., Walker, W.W., Overstreet, R.M., Lytle, J.S., Lytle, T.F., Carcinogenic effects of some polycyclic aromatic hydrocarbons on the Japanese medaka and guppy in waterborne exposures. Sci. Total Environ. 94 (1990), 155–167.
30. Herst, P.M., Tan, A.S., Scarlett, D.J., Berridge, M.V., Cell surface oxygen consumption by mitochondrial gene knockout cells. Biochim. Biophys. Acta 1656 (2004), 79–87.
31. Hicken, C.E., Linbo, T.L., Baldwin, D.H., Willis, M.L., Myers, M.S., Holland, L., Larsen, M., Stekoll, M.S., Rice, S.D., Collier, T.K., Scholz, N.L., Incardona, J.P., Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 7086–7090.
32. Hwang, H.J., Dornbos, P., Steidemann, M., Dunivin, T.K., Rizzo, M., LaPres, J.J., Mitochondrial-targeted aryl hydrocarbon receptor and the impact of 2,3,7,8-tetrachlorodibenzo-p-dioxin on cellular respiration and the mitochondrial proteome. Toxicol. Appl. Pharmacol. 304 (2016), 121–132.
33. Incardona, J.P., Collier, T.K., Scholz, N.L., Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 196 (2004), 191–205.
34. Incardona, J.P., Carls, M.G., Teraoka, H., Sloan, C.A., Collier, T.K., Scholz, N.L., Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ. Health Perspect. 113 (2005), 1755–1762.
35. Incardona, J.P., Linbo, T.L., Scholz, N.L., Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol. Appl. Pharmacol. 257 (2011), 242–249.
36. Jayasundara, N., Kozal, J.S., Arnold, M.C., Chan, S.S., Di Giulio, R.T., High-throughput tissue bioenergetics analysis reveals identical metabolic allometric scaling for teleost hearts and whole organisms. PLoS One, 10, 2015, e0137710.
37. Jayasundara, N., Van Tiem Garner, L., Meyer, J.N., Erwin, K.N., Di Giulio, R.T., AHR2-mediated transcriptomic responses underlying the synergistic cardiac developmental toxicity of PAHs. Toxicol. Sci. 143 (2015), 469–481.
38. Johnson, L.L., Casillas, E., Collier, T.K., McCain, B.B., Varanasi, U., Contaminant effects on ovarian development in english sole (Parophrys vetulus) from Puget Sound, Washington. Can. J. Fish. Aquat. Sci. 45 (1988), 2133–2146.
39. Jung, D., Di Giulio, R.T., Identification of mitochondrial cytochrome P450 induced in response to polycyclic aromatic hydrocarbons in the mummichog (Fundulus heteroclitus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 151 (2010), 107–112.
40. Jung, D., Cho, Y., Collins, L.B., Swenberg, J.A., Di Giulio, R.T., Effects of benzo[a]pyrene on mitochondrial and nuclear DNA damage in Atlantic killifish (Fundulus heteroclitus) from a creosote-contaminated and reference site. Aquat. Toxicol. 95 (2009), 44–51.
41. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., Schilling, T.F., Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995), 253–310.
42. Kumar, M.G., Rowley, S., Fulton, R., Dinday, M.T., Baraban, S.C., Patel, M., Altered glycolysis and mitochondrial respiration in a zebrafish model of Dravet syndrome. eNeuro, 3(2), 2016 (ENEURO.0008–16.2016).
43. Latimer, J.S., Zheng, J., The sources, transport, and fate of PAHS in the marine environment. Douben, P.E.T., (eds.) PAHs: An Ecotoxicological Perspective, 2003, John Wiley & Sons, Ltd., Chichester, UK.
44. Li, N., Sioutas, C., Cho, A., Schmitz, D., Misra, C., Sempf, J., Wang, M., Oberley, T., Froines, J., Nel, A., Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ. Health Perspect. 111 (2003), 455–460.
45. Lieschke, G.J., Currie, P.D., Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 8 (2007), 353–367.
46. Lima, A.L., Eglinton, T.I., Reddy, C.M., High-resolution record of pyrogenic polycyclic aromatic hydrocarbon deposition during the 20th century. Environ. Sci. Technol. 37 (2003), 53–61.
47. Meyer, J.N., Leung, M.C., Rooney, J.P., Sendoel, A., Hengartner, M.O., Kisby, G.E., Bess, A.S., Mitochondria as a target of environmental toxicants. Toxicol. Sci. 134 (2013), 1–17.
48. Nisbet, R.M., Muller, E.B., Lika, K., Kooijman, S., From molecules to ecosystems through dynamic energy budget models. J. Anim. Ecol. 69 (2000), 913–926.
49. Parichy, D.M., Advancing biology through a deeper understanding of zebrafish ecology and evolution. Elife, 4, 2015, e05635.
50. Pavanello, S., Dioni, L., Hoxha, M., Fedeli, U., Mielzynska-Svach, D., Baccarelli, A.A., Mitochondrial DNA copy number and exposure to polycyclic aromatic hydrocarbons. Cancer Epidemiol. Biomark. Prev. 22 (2013), 1722–1729.
51. Pieters, N., Koppen, G., Smeets, K., Napierska, D., Plusquin, M., De Prins, S., Van De Weghe, H., Nelen, V., Cox, B., Cuypers, A., Hoet, P., Schoeters, G., Nawrot, T.S., Decreased mitochondrial DNA content in association with exposure to polycyclic aromatic hydrocarbons in house dust during wintertime: from a population enquiry to cell culture. PLoS One, 8, 2013, e63208.
52. Rolfe, D.F., Newman, J.M., Buckingham, J.A., Clark, M.G., Brand, M.D., Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am. J. Phys. 276 (1999), C692–C699.
53. Rolo, A.P., Palmeira, C.M., Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 212 (2006), 167–178.
54. Santo-Domingo, J., Demaurex, N., Calcium uptake mechanisms of mitochondria. Biochim. Biophys. Acta 1797 (2010), 907–912.
55. Senft, A.P., Dalton, T.P., Nebert, D.W., Genter, M.B., Puga, A., Hutchinson, R.J., Kerzee, J.K., Uno, S., Shertzer, H.G., Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radic. Biol. Med. 33 (2002), 1268–1278.
56. Shim, J., Weatherly, L.M., Luc, R.H., Dorman, M.T., Neilson, A., Ng, R., Kim, C.H., Millard, P.J., Gosse, J.A., Triclosan is a mitochondrial uncoupler in live zebrafish. J. Appl. Toxicol., 2016, 10.1002/jat.3311.
57. Singh, K.K., Mitochondria damage checkpoint, aging, and cancer. Ann. N. Y. Acad. Sci. 1067 (2006), 182–190.
58. Spence, R., Gerlach, G., Lawrence, C., Smith, C., The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. Camb. Philos. Soc. 83 (2008), 13–34.
59. Stackley, K.D., Beeson, C.C., Rahn, J.J., Chan, S.S., Bioenergetic profiling of zebrafish embryonic development. PLoS One, 6, 2011, e25652.
60. Tappenden, D.M., Lynn, S.G., Crawford, R.B., Lee, K., Vengellur, A., Kaminski, N.E., Thomas, R.S., LaPres, J.J., The aryl hydrocarbon receptor interacts with ATP5alpha1, a subunit of the ATP synthase complex, and modulates mitochondrial function. Toxicol. Appl. Pharmacol. 254 (2011), 299–310.
61. Tappenden, D.M., Hwang, H.J., Yang, L., Thomas, R.S., Lapres, J.J., The aryl-hydrocarbon receptor protein interaction network (AHR-PIN) as identified by tandem affinity purification (TAP) and mass spectrometry. J. Toxicol., 2013, 2013, 279829.
62. Tiernan, C.T., Edwin, E.A., Hawong, H.Y., Rios-Cabanillas, M., Goudreau, J.L., Atchison, W.D., Lookingland, K.J., Methylmercury impairs canonical dopamine metabolism in rat undifferentiated pheochromocytoma (PC12) cells by indirect inhibition of aldehyde dehydrogenase. Toxicol. Sci. 144 (2015), 347–356.
63. Timme-Laragy, A.R., Van Tiem, L.A., Linney, E.A., Di Giulio, R.T., Antioxidant responses and NRF2 in synergistic developmental toxicity of PAHs in zebrafish. Toxicol. Sci. 109 (2009), 217–227.
64. van den Bosch, H., Schutgens, R.B.H., Wanders, R.J.A., Tager, J.M., Biochemistry of peroxisomes. Annu. Rev. Biochem. 61 (1992), 157–197.
65. Van Tiem, L.A., Di Giulio, R.T., AHR2 knockdown prevents PAH-mediated cardiac toxicity and XRE- and ARE-associated gene induction in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 254 (2011), 280–287.
66. Vignet, C., Devier, M.H., Le Menach, K., Lyphout, L., Potier, J., Cachot, J., Budzinski, H., Begout, M.L., Cousin, X., Long-term disruption of growth, reproduction, and behavior after embryonic exposure of zebrafish to PAH-spiked sediment. Environ. Sci. Pollut. Res. Int. 21 (2014), 13877–13887.
67. Vignet, C., Le Menach, K., Lyphout, L., Guionnet, T., Frere, L., Leguay, D., Budzinski, H., Cousin, X., Begout, M.L., Chronic dietary exposure to pyrolytic and petrogenic mixtures of PAHs causes physiological disruption in zebrafish—part II: behavior. Environ. Sci. Pollut. Res. Int. 21 (2014), 13818–13832.
68. Wassenberg, D.M., Di Giulio, R.T., Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ. Health Perspect. 112 (2004), 1658–1664.
69. Wilk, A., Waligorski, P., Lassak, A., Vashistha, H., Lirette, D., Tate, D., Zea, A.H., Koochekpour, S., Rodriguez, P., Meggs, L.G., Estrada, J.J., Ochoa, A., Reiss, K., Polycyclic aromatic hydrocarbons-induced ROS accumulation enhances mutagenic potential of T-antigen from human polyomavirus JC. J. Cell. Physiol. 228 (2013), 2127–2138.
70. Wills, L.P., Beeson, G.C., Hoover, D.B., Schnellmann, R.G., Beeson, C.C., Assessment of ToxCast phase II for mitochondrial liabilities using a high-throughput respirometric assay. Toxicol. Sci. 146 (2015), 226–234.
71. Xia, T., Korge, P., Weiss, J.N., Li, N., Venkatesen, M.I., Sioutas, C., Nel, A., Quinones and aromatic chemical compounds in particulate matter induce mitochondrial dysfunction: implications for ultrafine particle toxicity. Environ. Health Perspect. 112 (2004), 1347–1358.
72. Yozzo, K.L., Isales, G.M., Raftery, T.D., Volz, D.C., High-content screening assay for identification of chemicals impacting cardiovascular function in zebrafish embryos. Environ. Sci. Technol. 47 (2013), 11302–11310.
73. Zhu, H., Li, Y., Trush, M.A., Characterization of benzo[a]pyrene quinone-induced toxicity to primary cultured bone marrow stromal cells from DBA/2 mice: potential role of mitochondrial dysfunction. Toxicol. Appl. Pharmacol. 130 (1995), 108–120.