Gene expression profiles in zebrafish brain after acute exposure to domoic acid at symptomatic and asymptomatic doses

Toxicological Sciences

Volumn 107, Issue 1, 2009, Pages 65-77

  Lefebvre, Kathi A ^a   Tilton, Susan C ^b   Bammler, Theo K ^b   BeyerR P , Richard P ^b   Srinouanprachan, Sengkeo ^b   Stapleton, Patricia L ^b   Farin, Federico M ^b   Gallagher, Evan P ^b  

^a NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Domoic acid; Excitotoxicity; Microarray analysis; Zebrafish

Indexed keywords

BIOLOGICAL MARKER; DOMOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ACUTE TOXICITY; ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; EXCITOTOXICITY; FEMALE; GENE EXPRESSION PROFILING; ION TRANSPORT; MALE; MICROARRAY ANALYSIS; NEUROPATHY; NEUROTOXICITY; NONHUMAN; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SYMPTOMATOLOGY; ZEBRA FISH;

ANIMALS; BRAIN CHEMISTRY; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENES; KAINIC ACID; MUSCLE PROTEINS; NEUROTOXINS; UP-REGULATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; NITZSCHIA ALBA; PSEUDO-NITZSCHIA; VERTEBRATA;

EID: 58049204424     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn207     Document Type: Article

References (66)

1. Ananth, C., Gopalakrishnakone, P., and Kaur, C. (2003). Induction of inducible nitric oxide synthase expression in activated microglia following domoic acid (DA)-induced neurotoxicity in the rat hippocampus. Neurosci. Lett. 338, 49-52.
2. Ananth, C., Thameem Dheen, S., Gopalakrishnakone, P., and Kaur, C. (2001). Domoic acid-induced neuronal damage in the rat hippocampus: Changes in apoptosis related genes (bcl-2, bax, caspase-3) and microglial response. J. Neurosci. Res. 66, 177-190.
3. Ball, M. J. (1977). Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. A quantitative study. Acta Neuropathol. 37, 111-118.
4. Bates, S. S., Garrison, D. L., and Horner, R. A. (1998). Bloom dynamics and physiology of domoic-acid-producing Pseudo-nitzschia species. In The Physiological Ecology of Harmful Algal Blooms-NATO Advanced Study Institute Series (D. M. Anderson, G. M. Hallegraeff, and A. D. Cembella, Eds.), pp. 267-292. Springer-Verlag, Heidelberg, Germany.
5. Behrens, A., Sibilia, M., and Wagner, E. F. (1999). Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21, 326-329.
6. Berman, F. W., LePage, K. T., and Murray, T. F. (2002). Domoic acid neurotoxicity in cultured cerebellar granule neurons is controlled preferentially by the NMDA receptor Ca(2+) influx pathway. Brain Res. 924, 20-29.
7. Berman, F. W., and Murray, T. F. (1997). Domoic acid neurotoxicity in cultured cerebellar granule neurons is mediated predominantly by NMDA receptors that are activated as a consequence of excitatory amino acid release. J. Neurochem. 69, 693-703.
8. Bondy, S. C., and Lee, D. K. (1993). Oxidative stress induced by glutamate receptor agonists. Brain Res. 610, 229-233.
9. Boyd, J. M., Malstrom, S., Subramanian, T., Venkatesh, L. K., Schaeper, U., Elangovan, B., D'Sa-Eipper, C., and Chinnadurai, G. (1994). Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79, 341-351.
10. Caivano, M., Gorgoni, B., Cohen, P., and Poli, V. (2001). The induction of cyclooxygenase-2 mRNA in macrophages is biphasic and requires both CCAAT enhancer-binding protein beta (C/EBP beta) and C/EBP delta transcription factors. J. Biol. Chem. 276, 48693-48701.
11. Camon, M., Magrane, D., Barrell, V., Lee, E., Dimmer, D., Binns, J., Maslen, N., Harte, N., Lopez, R., and Apweiler, R. (2004). The Gene Ontology annotation (GOA) database: Sharing knowledge in Uniprot with Gene Ontology. Nucleic Acids Res. 32, D262-D266.
12. Carafoli, E. (2004). The ambivalent nature of the calcium signal. J. Endocrinol. Invest. 27, 134-136.
13. Clayton, E. C., Peng, Y. G., Means, L. W., and Ramsdell, J. S. (1999). Working memory deficits induced by single but not repeated exposures to domoic acid. Toxicon 37, 1025-1039.
14. Coyle, J. T., and Puttfarcken, P. (1993). Oxidative stress, glutamate, and neurodegenerative disorders. Science. 262, 689-695.
15. Dakshinamurti, K., Sharma, S. K., and Sundaram, M. (1991). Domoic acid induced seizure activity in rats. Neurosci. Lett. 127, 193-197.
16. Dakshinamurti, K., Sharma, S. K., Sundaram, M., and Watanabe, T. (1993). Hippocampal changes in developing postnatal mice following intrauterine exposure to domoic acid. J. Neurosci. 13, 4486-4495.
17. Duchen, M. R. (1999). Contributions of mitochondria to animal physiology: From homeostatic sensor to calcium signalling and cell death. J. Physiol. 516, 1-17.
18. Edwards, J. G., and Michel, W. C. (2002). Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. J. Comp. Neurol. 454, 294-309.
19. Gallagher, E. P., Buetler, T. M., Stapleton, P. L., Wang, C. H., Stahl, D. L., and Eaton, D. L. (1995). The effects of diquat and ciprofibrate on mRNA expression and catalytic activities of hepatic xenobiotic metabolizing and antioxidant enzymes in rat liver. Toxicol. Appl. Pharmacol. 134, 81-91.
20. Gentleman, R. (2005). In Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, New York.
21. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004). Bioconductor: Open software development for computational biology and bioinformatics. Genome. Biol. 5, R80.
22. Green, D. R., and Reed, J. C. (1998). Mitochondria and apoptosis. Science 281, 1309-1312.
23. Grimmelt, B., Nijjar, M. S., Brown, J., Macnair, N., Wagner, S., Johnson, G. R., and Amend, J. F. (1990). Relationship between domoic acid levels in the blue mussel (Mytilus edulis) and toxicity in mice. Toxicon 28, 501-508.
24. Gulland, F. M., Haulena, M., Fauquier, D., Langlois, G., Lander, M. E., Zabka, T., and Duerr, R. (2002). Domoic acid toxicity in Californian sea lions (Zalophus californianus): Clinical signs, treatment and survival. Vet. Rec. 150, 475-480.
25. Hampson, D. R., and Manalo, J. L. (1998). The activation of glutamate receptors by kainic acid and domoic acid. Nat. Toxins 6, 153-158.
26. Hoppmann, V., Wu, J. J., Soviknes, A.M., Helvik, J.V., and Becker, T. S. (2008). Expression of the eight AMPA receptor subunit genes in the developing central nervous system and sensory organs of zebrafish. Dev. Dyn. 237, 788-799.
27. Horn, R., Ostertun, B., Fric, M., Solymosi, L., Steudel, A., and Moller, H. J. (1996). Atrophy of hippocampus in patients with Alzheimer's disease and other diseases with memory impairment. Dementia 7 182-186.
28. Hunsberger, J. G., Bennett, A. H., Selvanayagam, E., Duman, R. S., and Newton, S. S. (2005). Gene profiling the response to kainic acid induced seizures. Brain Res. Mol. Brain Res. 141, 95-112.
29. Iverson, F., Truelove, J., Tryphonas, L., and Nera, E. A. (1990). The toxicology of domoic acid administered systemically to rodents and primates. Can. Dis. Wkly. Rep 16(Suppl. 1E), 15-19.
30. Jin, W., Zhang, J., Lou, D., Chavkin, C., and Xu, M. (2002). C-fos-deficient mouse hippocampal CA3 pyramidal neurons exhibit both enhanced basal and kainic acid-induced excitability. Neurosci. Lett. 331, 151-154.
31. Kindy, M. S., and Verma, I. M. (1990). Developmental expression of the Xenopus laevis fos protooncogene. Cell Growth Differ. 1, 27-37.
32. Lefebvre, K. A., Dovel, S. L., and Silver, M. W. (2001). Tissue distribution and neurotoxic effects of domoic acid in a prominent vector species, the northern anchovy Engraulis mordax. Marine Biol. 138, 693-700.
33. Lefebvre, K. A., Noren, D. P., Schultz, I. R., Bogard, S. M., Wilson, J., and Eberhart, B. T. (2007). Uptake, tissue distribution and excretion of domoic acid after oral exposure in coho salmon (Oncorhynchus kisutch). Aquat. Toxicol. 81, 266-274.
34. Lefebvre, K. A., Powell, C. L., Busman, M., Doucette, G. J., Moeller, P. D. R., Silver, J. B., Miller, P. E., Hughes, M. P., Singaram, S., Silver, M. W., et al. (1999). Detection of domoic acid in northern anchovies and California Sea Lions associated with an unusual mortality event. Nat. Toxins 7, 85-92.
35. Lefebvre, K. A., Silver, M. W., Coale, S. L., and Tjeerdema, R. S. (2002). Domoic acid in planktivorous fish in relation to toxic Pseudo-nitzschia cell densities. Marine Biol. 140, 625-631.
36. Levitan, I. (1991). In The Neuron. Oxford University Press, New York.
37. Lyons, S., Shuea, B., Lei, L., Oates, A., Zon, L., and Liua, P. (2001). Molecular cloning, genetic mapping, and expression analysis of four zebrafish c/ebp genes. Gene 281, 43-51.
38. Ohki, T., Hongo, S., Nakada, N., Maeda, A., and Takeda, M. (2002). Inhibition of neurite outgrowth by reduced level of NDRG4 protein in antisense transfected PC12 cells. Brain Res. Dev. Brain Res. 135, 55-63.
39. Okuda, T., Kokame, K., and Miyata, T. (2008). Differential expression patterns of NDRG family proteins in the central nervous system. J. Histochem. Cytochem. 56, 175-182.
40. Peng, Y. G., and Ramsdell, J. S. (1996). Brain Fos induction is a sensitive biomarker for the lowest observed neuroexcitatory effects of domoic acid. Fundam. Appl. Toxicol. 31, 162-168.
41. Peng, Y. G., Taylor, T. B., Finch, R. E., Switzer, R. C., and Ramsdell, J. S. (1994). Neuroexcitatory and neurotoxic actions of the amnesic shellfish poison, domoic acid. Neuroreport. 5, 981-985.
42. Perl, T. M., Bedard, L., Kosatsky, T., Hockin, J. C., Todd, E. C., and Remis, R. S. (1990). An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N. Engl. J. Med. 322, 1775-1780.
43. Qiu, S., and Curras-Collazo, M. C. (2006). Histopathological and molecular changes produced by hippocampal microinjection of domoic acid. Neurotoxicol. Teratol. 28, 354-362.
44. Quilliam, M. A., Sim, P. G., McCulloch, A. W., and McInnes, A. G. (1989). High-performance liquid-chromatography of domoic acid, a marine neurotoxin, with application to shellfish and plankton. Int. J. Environ. Anal. Chem. 36, 139-154.
45. Ramji, D. P., and Foka, P. (2002). CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365, 561-575.
46. Ryan, J. C., Morey, J. S., Ramsdell, J. S., and Van Dolah, F. M. (2005). Acute phase gene expression in mice exposed to the marine neurotoxin domoic acid. Neuroscience 136, 1121-1132.
47. Salierno, J. D., Snyder, N. S., Murphy, A. Z., Poli, M., Hall, S., Baden, D., and Kane, A. S. (2006). Harmful algal bloom toxins alter c-Fos protein expression in the brain of killifish, Fundulus heteroclitus. Aquat. Toxicol. 78, 350-357.
48. Schimanski, L. A., and Nguyen, P. V. (2005). Impaired fear memories are correlated with subregion-specific deficits in hippocampal and amygdalar LTP. Behav. Neurosci. 119, 38-54.
49. Scholin, C. A., Gulland, F., Doucette, G. J., Benson, S., Busman, M., Chavez, F. P., Cordaro, J., DeLong, R., De Vogelaere, A., Harvey, J., et al. (2000). Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 403, 80-84.
50. Sierra-Beltran, A. P., Palafox-Uribe, M., Grajales-Montiel, J., Cruz-Villacorta, A., and Ochoa, J. L. (1997). Sea bird mortality at Cabo San Lucas, Mexico: Evidence that toxic diatom blooms are spreading. Toxicon 35, 447-453.
51. Silvagni, P. A., Lowenstine, L. J., Spraker, T., Lipscomb, T. P., and Gulland, F. M. D. (2005). Pathology of domoic acid toxicity in California sea lions (Zalophus californianus). Veterinary pathology 42, 184-191.
52. Smyth, G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
53. Strain, S. M., and Tasker, R. A. (1991). Hippocampal damage produced by systemic injections of domoic acid in mice. Neuroscience 44, 343-352.
54. Sutherland, R. J., Hoesing, J. M., and Whishaw, I. Q. (1990). Domoic acid, an environmental toxin, produces hippocampal damage and severe memory impairment. Neurosci. Lett. 120, 221-223.
55. Tasker, R. A., Connell, B. J., and Strain, S. M. (1991). Pharmacology of systemically administered domoic acid in mice. Can. J. Physiol. Pharmacol. 69, 378-382.
56. Taubenfeld, S., Wiig, K., Monti, B., Dolan, B., Pollonini, G., and Alberini, C. (2001). Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein b and d co localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J. Neuroscience. 21, 84-91.
57. Tiedeken, J. A., Ramsdell, J. S., and Ramsdell, A. F. (2005). Developmental toxicity of domoic acid in zebrafish (Danio rerio). Neurotoxicol. Teratol. 27, 711-717.
58. Tryphonas, L., Truelove, J., and Iverson, F. (1990a). Acute parenteral neurotoxicity of domoic acid in cynomolgus monkeys (M. fascicularis). Toxicol. Pathol. 18, 297-303.
59. Tryphonas, L., Truelove, J., Nera, E., and Iverson, F. (1990b). Acute neurotoxicity of domoic acid in the rat. Toxicol. Pathol. 18 1-9.
60. Tusher, V. G., Tibshirani, R., and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U S A. 98, 5116-5121.
61. Wekell, J. C., Gauglitz, E. J., Jr., Barnett, H. J., Hatfield, C. L., Simons, D., and Ayres, D. (1994). Occurrence of domoic acid in Washington state razor clams (Siliqua patula) during 1991-1993. Nat. Toxins 2, 197-205.
62. Westerfield, M. (1995). In The Zebrafish Book. University of Oregon Press, Oregon.
63. Work, T. M., Barr, B., Beale, A. M., Fritz, L., Quilliam, M. A., and Wright, J. L. C. (1993). Epidemiology of domoic acid poisoning in brown pelicans (Pelicanus occidentalis) and Brandt's cormorants ( Phalacrocorax penicillatus) in California. J. Zoo Wild. Med. 24, 54-62.
64. Wright, J. L. C., Boyd, R. K., Freitas, A., Falk, M., Foxall, R. A., Jamieson, W. D., Laycock, M. V., McCulloch, A. W., McInnes, A. G., et al. (1989). Identification of domoic acid, a neuroexcitatory amino acid, in toxic mussels from eastern Prince Edward Island. Can. J. Chem. 67, 481-490.
65. Zhang, J., Zhang, D., McQuade, J. S., Behbehani, M., Tsien, J. Z., and Xu, M. (2002). c-fos regulates neuronal excitability and survival. Nat. Genet. 30, 416-420.
66. Zhou, R. H., Kokame, K., Tsukamoto, Y., Yutani, C., Kato, H., and Miyata, T. (2001). Characterization of the human NDRG gene family: A newly identified member, NDRG4, is specifically expressed in brain and heart. Genomics 73, 86-97.