Developmental lead exposure causes startle response deficits in zebrafish

Aquatic Toxicology

Volumn 105, Issue 3-4, 2011, Pages 600-608

  Rice, Clinton ^a,c   Ghorai, Jugal K ^b   Zalewski, Kathryn ^b   Weber, Daniel N ^b  

^a AMERICAN UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Behavior; Lead; Mechanosensory; Startle response; Visual; Zebrafish

Indexed keywords

LEAD;

BEHAVIORAL RESPONSE; BIOINDICATOR; BIOMONITORING; CONCENTRATION (COMPOSITION); FISH; LEAD; LIGHT EFFECT; PHYSIOLOGICAL RESPONSE; POLLUTION EXPOSURE; SENSORY SYSTEM;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; ESCAPE BEHAVIOR; FERTILIZATION; LARVA; LATENT PERIOD; LEAD POISONING; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; STARTLE REFLEX; STIMULUS RESPONSE; VISUAL STIMULATION; ZEBRA FISH;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; ESCAPE REACTION; LARVA; LEAD; STARTLE REACTION; TIME FACTORS; TOXICITY TESTS, ACUTE; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

DANIO RERIO;

EID: 80053367762     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2011.08.014     Document Type: Article

References (66)

1. Basha R., Reddy G.R. Developmental exposure to lead and late life abnormalities of nervous system. Indian J. Exp. Biol. 2010, 48:636-641.
2. Buekers J., Redeker E.S., Smolders E. Lead toxicity to wildlife: derivation of a critical blood concentration for wildlife monitoring based on literature data. Sci. Total Environ. 2009, 15:3431-3438.
3. Bunn T.L., Parsons P.J., Kao E., Dietert R.R. Exposure to lead during critical windows of embryonic development: differential immunotoxic outcome based on stage of exposure and gender. Toxicol. Sci. 2001, 64:57-66.
4. Burgess H.A., Johnson S.L., Granato M. Unidirectional startle responses and disrupted left-right co-ordination of motor behaviors in robo3 mutant zebrafish. Genes Brain Behav. 2009, 8:500-511.
5. Carvan M.J., Loucks E., Weber D.N., Williams F.E. Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol. Teratol. 2004, 26:757-768.
6. Cory-Slechta D.A. Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions. Annu. Rev. Pharmacol. Toxicol. 1995, 35:391-415.
7. Cory-Slechta D.A., Pokora M.J. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology 1995, 16:337-347.
8. Costa L.G., Aschner M., Vitalone A., Syversen T., Soldin O.P. Developmental neuropathology of environmental agents. Annu. Rev. Pharmacol. Toxicol. 2004, 44:87-110.
9. Dearth R.K., Hiney J.K., Srivastava V., Dees L.W., Bratton G.R. Low level lead (Pb) exposure during gestation and lactation: assessment of effects on pubertal development in Fisher 344 and Sprague-Dawley female rats. Life Sci. 2004, 74:1139-1148.
10. Dearth R.K., Hiney J.K., Srivastava V., Burdick S.B., Bratton G.R., Dees W.L. Effects of lead (Pb) exposure during gestation and lactation on female pubertal development in the rat. Reprod. Toxicol. 2002, 16:343-352.
11. Devoto P., Flore G., Ibba A., Fratta W., Pani L. Lead intoxication during intrauterine life and lactation but not during adulthood reduces nucleus accumbens dopamine release as studied by brain microdialysis. Toxicol. Lett. 2001, 121:199-206.
12. Diamond J. The activation and distribution of GABA and l-glutamate receptors on goldfish Mauthner neurons: an analysis of dendritic remote inhibition. J. Physiol. 1968, 194:669-723.
13. Dietrich K.N., Krafft K.M., Pearson D.T., Bornschein R.L., Hammond P.B., Succop P.A. Postnatal lead exposure and early sensorimotor development. Environ. Res. 1985, 38:130-136.
14. Eaton R.C., Bombardieri R.A., Meyer D.L. The Mauthner-initiated startle response in teleost fish. J. Exp. Biol. 1977, 66:65-81.
15. Ebrahimi M., Taherianfard M. Concentration of four heavy metals (cadmium, lead, mercury, and arsenic) in organs of two cyprinid fish (Cyprinus carpio and Capoeta sp.) from the Kor River (Iran). Environ. Monit. Assess. 2010, 16:575-585.
16. Fitsanakis V.A., Aschner M. The importance of glutamate, glycine, and gamma-aminobutyric acid transport and regulation in manganese, mercury and lead neurotoxicity. Toxicol. Appl. Pharmacol. 2005, 204:343-354.
17. Fortune T., Lurie D.I. Chronic low-level lead exposure affects the monoaminergic system in the mouse superior olivary complex. J. Comp. Neurol. 2009, 513:542-558.
18. Fox D.A., Kala S.V., Hamilton W.R., Johnson J.E., O'Callaghan J.P. Low-level human equivalent gestational lead exposure produces supernormal scotopic electroretinograms, increased retinal neurogenesis, and decreased retinal dopamine utilization in rats. Environ. Health Perspect. 2008, 116:618-625. (Erratum in: Environ. Health Perspect. 2008, 116, A241).
19. Fox D.A., Katz L.M., Farber D.B. Low level developmental lead exposure decreases the sensitivity, amplitude and temporal resolution of rods. Neurotoxicology 1991, 12:641-654.
20. Fox D.A., Silman A.J. Heavy metals affect rod, but not cone, photoreceptors. Science 1979, 206:78-80.
21. Froehlicher M., Liedtke A., Groh K.J., Neuhauss S.C., Segner H., Eggen R.I. Zebrafish (Danio rerio) neuromast: promising biological endpoint linking developmental and toxicological studies. Aquat. Toxicol. 2009, 95:307-319.
22. Hatta K., Ankri N., Faber D.S., Korn H. Slow inhibitory potentials in the teleost Mauthner cell. Neuroscience 2001, 103:561-579.
23. Hinck J.E., Schmitt C.J., Blazer V.S., Denslow N.D., Bartish T.M., Anderson P.J., Coyle J.J., Gail M., Dethloff G.M., Tillitt D.E. Environmental contaminants and biomarker responses in fish from the Columbia River and its tributaries: spatial and temporal trends. Sci. Total Environ. 2006, 366:549-578.
24. Iavicoli I., Fontana L., Bergamaschi A. The effects of metals as endocrine disruptors. J. Toxicol. Environ. Health B Crit. Rev. 2009, 12:206-223.
25. Irons T.D., MacPhail R.C., Hunter D.L., Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol. Teratol. 2010, 32:84-90.
26. Jin M., Zhang Y., Ye J., Huang C., Zhao M., Liu W. Dual enantioselective effect of the insecticide bifenthrin on locomotor behavior and development in embryonic-larval zebrafish. Environ. Toxicol. Chem. 2010, 29:1561-1567.
27. Kuhlmann A.C., McGlothan J.L., Guilarte T.R. Developmental lead exposure causes spatial learning deficits in adult rats. Neurosci. Lett. 1997, 233:101-114.
28. Lahnsteiner F. The sensitivity and reproducibility of the zebrafish (Danio rerio) embryo test for the screening of wastewater quality and for testing the toxicity of chemicals. Altern. Lab. Anim. 2008, 36:299-311.
29. Leasure J.L., Giddabasappa A., Chaney S., Johnson J.E., Pothakos K., Lau Y.S., Fox D.A. Low-level human equivalent gestational lead exposure produces sex-specific motor and coordination abnormalities and late-onset obesity in year-old mice. Environ. Health Perspect. 2008, 116:355-361.
30. Levesque H.M., Dorval J., Hontela A., Van Der Kraak G.J., Campbell P.G. Hormonal, morphological, and physiological responses of yellow perch (Perca flavescens) to chronic environmental metal exposures. J. Toxicol. Environ. Health A 2003, 11:657-676.
31. Levin E.D., Swain H.A., Donerly S., Linney E. Developmental chlorpyrifos effects on hatchling zebrafish swimming behavior. Neurotoxicol. Teratol. 2004, 26:719-723.
32. Li L., Dowling J.E. Zebrafish visual sensitivity is regulated by a circadian clock. Vis. Neurosci. 1998, 15:851-857.
33. Li L., Dowling J.E. A dominant form of inherited retinal degeneration caused by non-photoreceptor cell-specific mutation. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:11645-11650.
34. McLean D.L., Fetcho J.R. Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish. J. Comp. Neurol. 2004, 480:57-71.
35. Moreira E.G., Vassilieff I., Vassilieff V.S. Developmental lead exposure: behavioral alterations in the short and long term. Neurotoxicol. Teratol. 2001, 23:489-495.
36. Morgan R.E., Garavan H., Smith E.G., Driscoll L.L., Levitsky D.A., Strupp B.J. Early lead exposure produces lasting changes in sustained attention, response initiation, and reactivity to errors. Neurotoxicol. Teratol. 2001, 23:519-531.
37. Mueller, K.A., Snyder-Conn, E., Bertram, M., 2011. Water Quality and Metal and Metalloid Contaminants in Sediments and Fish of Koyukuk, Nowitna, and the Northern Unit of Innoko National Wildlife Refuges, Alaska, 1991. Natl Tech Info Serv.
38. Nawrocki L., BreMiller R., Streisinger G., Kaplan M. Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vis. Res. 1985, 25:1569-1576.
39. Neal A.P., Worley P.F., Guilarte T.R. Lead exposure during synaptogenesis alters NMDA receptor targeting via NMDA receptor inhibition. Neurotoxicology 2011, 32:281-289.
40. Oberto A., Marks N., Evans H.L., Guidotti A. Lead (Pb+2) promotes apoptosis in newborn rat cerebellar neurons: pathological implications. J. Pharmacol. Exp. Ther. 1996, 279:435-442.
41. Patten S.A., Ali D.W. AMPA receptors associated with zebrafish Mauthner cells switch subunits during development. J. Physiol. 2007, 581:1043-1056.
42. Powers C.M., Yen J., Linney E.A., Seidler F.J., Slotkin T.A. Silver exposure in developing zebrafish (Danio rerio): persistent effects on larval behavior and survival. Neurotoxicol. Teratol. 2010, 32:391-397.
43. Rademacher D.J., Steinpreis R.E., Weber D.N. Short-term exposure to dietary Pb and/or DMSA affects dopamine and dopamine metabolite levels in the medulla, optic tectum, and cerebellum of rainbow trout (Oncorhynchus mykiss). Pharmacol. Biochem. Behav. 2001, 70:199-207.
44. Reddy G.R., Devi B.C., Chetty C.S. Developmental lead neurotoxicity: alterations in brain cholinergic system. Neurotoxicology 2007, 28:402-407.
45. Reiter L.W., Anderson G.E., Laskey J.W., Cahill D.F. Developmental and behavioral changes in the rat during chronic exposure to lead. Environ. Health Perspect. 1975, 12:119-123.
46. Rigo J.M., Legendre P. Frequency-dependent modulation of glycine receptor activation recorded from the zebrafish larvae hindbrain. Neuroscience 2006, 140:389-402.
47. Rombough P.J. The influence of the zona radiata on the toxicities of zinc, lead, mercury, copper and silver ions to embryos of steelhead trout Salmo gairdneri. Comp. Biochem. Physiol. C 1985, 82:115-117.
48. Schmitt F.A., Dowling J.E. Early eye morphogenesis in the zebrafish, Brachydanio rerio. J. Comp. Neurol. 1994, 344:532-542.
49. Schmitt F.A., Dowling J.E. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J. Comp. Neurol. 1999, 404:515-536.
50. Schmitt C.J., Brumbaugh W.G., Linder G.L., Hinck J.E. A screening-level assessment of lead, cadmium, and zinc in fish and crayfish from Northeastern Oklahoma, USA. Environ. Geochem. Health 2006, 28:445-471.
51. Spieler R.E., Russo A.C., Weber D.N. Waterborne lead affects circadian variations of brain neurotransmitters in fathead minnows. Bull. Environ. Contam. Toxicol. 1995, 55:412-418.
52. Strickler-Shaw S., Taylor D.H. Lead inhibits acquisition and retention learning in bullfrog tadpoles. Neurotoxicol. Teratol. 1991, 13:167-173.
53. Sun L., Zhao Z.Y., Hu J., Zhou X.L. Potential association of lead exposure during early development of mice with alteration of hippocampus nitric oxide levels and learning memory. Biomed. Environ. Sci. 2005, 18:375-378.
54. Thomas L.T., Welsh L., Galvez F., Svoboda K.R. Acute nicotine exposure and modulation of a spinal motor circuit in embryonic zebrafish. Toxicol. Appl. Pharmacol. 2009, 239:1-12.
55. Triller A., Rostaing P., Korn H., Legendre P. Morphofunctional evidence for mature synaptic contacts on the Mauthner cell of 52-hour-old zebrafish larvae. Neuroscience 1997, 80:133-145.
56. Weber D.N., Russo A., Seale D.B., Spieler R.E. Waterborne lead affects feeding abilities and neurotransmitter levels of juvenile fathead minnows (Pimephales promelas). Aquat. Toxicol. 1991, 21:71-80.
57. Weber D.N. Exposure to sublethal levels of waterborne lead alters reproductive behavior patterns in fathead minnows (Pimephales promelas). Neurotoxicology 1993, 14:347-358.
58. Weber D.N., Dingel W.M., Panos J.J., Steinpreis R.E. Alterations in neurobehavioral responses in fishes exposed to lead and lead-chelating agents. Amer. Zool. 1997, 37:354-362.
59. Weber D.N. Dose-dependent effects of developmental mercury exposure on C-start escape responses of larval zebrafish Danio rerio. J. Fish Biol. 2006, 69:75-94.
60. Weber D.N., Connaughton V.P., Dellinger J.A., Klemer D., Udvadia A., Carvan M.J. Selenomethionine reduces visual deficits due to developmental methylmercury exposures. Physiol. Behav. 2008, 93:250-260.
61. Weber D.N., Spieler R.E. Behavioral mechanisms of metal toxicity in fishes. Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspectives 1994, 421-467. Lewis Publishers, Boca Raton, FL. D.C. Malins, G.K. Ostrander (Eds.).
62. Winter M.J., Redfern W.S., Hayfield A.J., Owen S.F., Valentin J.P., Hutchinson T.H. Validation of a larval zebrafish locomotor assay for assessing the seizure liability of early-stage development drugs. J. Pharmacol. Toxicol. Methods 2008, 57:176-187.
63. Xing X.J., Rui Q., Du M., Wang D.Y. Exposure to lead and mercury in young larvae induces more severe deficits in neuronal survival and synaptic function than in adult nematodes. Arch. Environ. Contam. Toxicol. 2009, 56:732-741.
64. Yang Y., Ma Y., Ni L., Zhao S., Li L., Zhang J., Fan M., Liang C., Cao J., Xu L. Lead exposure through gestation-only caused long-term learning/memory deficits in young adult offspring. Exp. Neurol. 2003, 184:489-495.
65. Zacharová D., Hencek M., Pavelková J., Lipská E. The effect of Pb2+ ions on calcium currents and contractility in single muscle fibres of the crayfish. Gen. Physiol. Biophys. 1993, 12:183-198.
66. Zhang, J., Peterson, S.M., Weber, G.J., Zhu, X., Zheng, W., Freeman J.L. Decreased axonal density and altered expression profiles of axonal guidance genes underlying lead (Pb) neurodevelopmental toxicity at early embryonic stages in the zebrafish. Neurotoxicol. Teratol., doi:10.1016/j.ntt.2011.07.010.