Zebrafish locomotor capacity and brain acetylcholinesterase activity is altered by aphanizomenon flos-aquae DC-1 aphantoxins

Aquatic Toxicology

Volumn 138-139, Issue , 2013, Pages 139-149

  Zhang, De Lu ^a,b   Hu, Chun Xiang ^b   Li, Dun Hai ^b   Liu, Yong Ding ^b  

^a WUHAN UNIVERSITY OF TECHNOLOGY   (China)

^b INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Acetylcholinesterase; Aphantoxins; Brain; Locomotor abnormality; Mechanosensory change; Zebrafish

Indexed keywords

ACETYLCHOLINESTERASE; APHANTOXIN; GONYAUTOXIN; GONYAUTOXIN 1; GONYAUTOXIN 5; NEOSAXITOXIN; SHELLFISH TOXIN; UNCLASSIFIED DRUG;

BEHAVIORAL RESPONSE; BRAIN; DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; FISH; NEUROLOGY; POLLUTION EFFECT; POLLUTION EXPOSURE; SWIMMING BEHAVIOR; TIME DEPENDENT BEHAVIOR; TOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APHANIZOMENON; APHANIZOMENON FLOS-AQUAE; ARTICLE; CHOLINERGIC SYSTEM; CONCENTRATION RESPONSE; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LOCOMOTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; TOUCH; TOXIN ANALYSIS; ZEBRA FISH;

ACETYLCHOLINESTERASE; ANALYSIS OF VARIANCE; ANIMALS; APHANIZOMENON; BACTERIAL TOXINS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENCE; HEAD; INJECTIONS, INTRAPERITONEAL; MARINE TOXINS; MOTOR ACTIVITY; TAIL; TOUCH; ZEBRAFISH;

APHANIZOMENON FLOS-AQUAE; DANIO RERIO;

EID: 84879458348     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.04.016     Document Type: Article

References (142)

1. Airhart M.J., Lee D.H., Wilson T.D., Miller B.E., Miller M.N., Skalko R.G. Movement disorders and neurochemical changes in zebrafish larvae after bath exposure to fluoxetine (PROZAC). Neurotoxicology and Teratology 2007, 29:652-664.
2. Alsop D., Vijayan M.M. Development of the corticosteroid stress axis and receptor expression in zebrafish. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2008, 294:R711-R719.
3. Altringham D., Ellerby D.J. Fish swimming: patterns in muscle function. Journal of Experimental Biology 1999, 202:3397-3403.
4. Anderson D.M., Glibert P.M., Burkholder J.M. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 2002, 25(4b):704-726.
5. Anglister L., Etlin A., Finkel E., Durrant A.R., Lev-Tov A. Cholinesterases in development and disease. Chemico-Biological Interactions 2008, 175:92-100.
6. Aráoz R., Molgó J., de Marsac N.T. Neurotoxic cyanobacterial toxins. Toxicon 2010, 56(5):813-828.
7. Baganz D., Staaks G., Steinberg C. Impact of the cyanobacteria toxin, microcystin-LR on Behaviour of zebrafish, Danio rerio. Water Research 1998, 32(3):948-952.
8. Baganz D., Staaks G., Pflugmacher S., Steinberg C.E.W. Comparative Study of Microcystin-LR-Induced Behavioral Changes of Two Fish Species. Danio rerio and Leucaspius delineatus Environmental Toxicology 2004, 19(6):564-570.
9. Bakke M.J., Hustoft H.K., Horsberg T.E. Subclinical effects of saxitoxin and domoic acid on aggressive behaviour and monoaminergic turnover in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 2010, 99:1-9.
10. Ballesteros M.L., Durando P.E., Nores M.L., Díaz M.P., Bistoni M.A., Wunderlin D.A. Endosulfan induces changes in spontaneous swimming activity and acetylcholinesterase activity of Jenynsia multidentata (Anablepidae Cyprinodontiformes). Environmental Pollution 2009, 157:1573-1580.
11. Ballot A., Fastner J., Wiedner C. Paralytic shellfish poisoning toxin-producing cyanobacterium Aphanizomenon gracile in Northeast Germany. Applied and Environment Microbiology 2010, 76(4):1173-1180.
12. Banker R., Carmeli S., Hadas O., Teltsch B., Porat R., Sukenik A. Identification of cylindrospermopsin in aphanizomenon obalisporum (cyanophyceae) isolated from lake kinneret, Israel. Journal of Phycology 1997, 33:613-616.
13. Barbazuk W.B., Korf I., Kadavi C., Heyen J., Tate S., Wun E., et al. The syntenic relationship of the zebrafish and human genomes. Genome Research 2000, 10:1351-1358.
14. Bégout Anras M.L., Lagardére J.P. Measuring cultured fish swimming behaviour: first results on rainbow trout using acoustic telemetry in tanks. Aquaculture 2004, 240:175-186.
15. Bierman H.S., Schriefer J.E., Zottoli S.J., Hale M.E. The effects of head and tail stimulation on the withdrawal startle response of the rope fish (Erpetoichthys calabaricus). Journal of Experimental Biology 2004, 207:3985-3997.
16. Blaser R., Gerlai R. Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods. Behavior Research Methods 2006, 38(3):456-469.
17. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:218-254.
18. Brewer S.K., DeLonay A.J., Beauvais S.B., Little E.E., Jones S.B. The use of automated monitoring to assess behavioral toxicology in fish: linking behavior and physiology. Environmental toxicology and risk assessment vol. 8 ASTM STP 1364 1999, American Society for Testing and Materials, West Conshohocken, PA, pp 371-386. D.S. Henshel, M.C. Black, M.C. Harrass (Eds.).
19. Brewer S.K., Little E.E., DeLonay A.J., Beauvais S.L., Jones S.B., Ellersieck M.R. Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Archives of Environment Contamination and Toxicology 2001, 40:70-76.
20. Bricelj V.M., Connell L., Konoki K., Macquarrie S.P., Scheuer T., Catterall W.A., Trainer V.L. Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 2005, 434(7034):763-767.
21. Brittijn S.A., Duivesteijn S.J., Belmamoune M., Bertens L.F., Bitter W., de Bruijn J.D., Champagne D.L., Cuppen E., Flik G., Vandenbroucke-Grauls C.M., Janssen R.A., de Jong I.M., de Kloet E.R., Kros A., Meijer A.H., Metz J.R., van der Sar A.M., Schaaf M.J., Schulte-Merker S., Spaink H.P., Tak P.P., Verbeek F.J., Vervoordeldonk M.J., Vonk F.J., Witte F., Yuan H., Richardson M.K. Zebrafish development and regeneration: new tools for biomedical research. The International Journal of Developmental Biology 2009, 53:835-850.
22. Bruce R.D. An up-and-down procedure for acute toxicity testing. Fundamental and Applied Toxicology 1985, 5(1):151-157.
23. Carvan M.J., Loucks E., Weber D.N., Williams F.E. Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicology and Teratology 2004, 26:757-768.
24. Cazenave J., Nores M.L., Miceli M., Díaz M.P., Wunderlin D.A., Bistoni M.A. Changes in the swimming activity and the glutathione S-transferase activity of Jenynsia multidentata fed with microcystin-RR. Water Research 2008, 42:1299-1307.
25. Clemente Z., Busato R.H., Ribeiro C.A.O., Cestari M.M., Ramsdorf W.A., Magalhães V.F., Wosiack A.C., Assis H.C.S. Analyses of paralytic shellfish toxins and biomarkers in a southern Brazilian reservoir. Toxicon 2010, 55:396-406.
26. Costa I.A.S., Azevedo S.M.F.O., Senna P.A.C., Bernardo R.R., Costa S.M., Chellappa N.T. Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Brazilian Journal of Biology 2006, 66:211-219.
27. da Silva A.S., Monteiro S.G., Goncalves J.F., Spanevello R., Oliveira C.B., Costa M.M., Jaquesc J.A.S., Morschc V.M., Schetinger M.R.C., Mazzanti C.M., Lopes S.T.A. Acetylcholinesterase activity and lipid peroxidation in the brain and spinal cord of rats infected with Trypanosoma evansi. Veterinary Parasitology 2011, 175:237-244.
28. da Silva C.A., Oba E.T., Ramsdorf W.A., Magalhães V.F., Cestari M.M., Ribeiro C.A.O., Assis H.C.S. First report about saxitoxins in freshwater fish Hoplias malabaricus through trophic exposure. Toxicon 2011, 57:141-147.
29. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nature Reviews Neuroscience 2008, 9:46-56.
30. Damodaran S., Dlugos C.A., Wood T.D., Rabin R.A. Effects of chronic ethanol administration on brain protein levels: a proteomic investigation using 2-D DIGE system. European Journal of Pharmacology 2006, 547:75-82.
31. Da Silva A.S., Spanevello R., Stefanello N., Wolkmer P., Costa M.M., Zanette R.A., Lopes S.T.A., Santurio J.M., Schetinger M.R.C., Monteiro S.G. Influence of Trypanosoma evansi in blood, plasma, and brain cholinesterase of experimentally infected cats. Research in Veterinary Science 2010, 88:281-284.
32. D'aoÛt K., Aerts P. A kinematic comparison of forward and backward swimming in the eel Anguilla anguilla. Journal of Experimental Biology 1999, 202:1511-1521.
33. Diener M., Erler K., Hiller S., Christian B., Luckas B. Determination of paralytic shellfish poisoning (PSP) toxins in dietary supplements by application of a new HPLC/FD method. European Food Research and Technology 2006, 224:147-151.
34. Domenici P., Blake R. The kinematics and performance of fish fast-start swimming. Journal of Experimental Biology 1997, 200:1165-1178.
35. Egan R.J., Bergner C.L., Hart P.C., Cachat J.M., Canavello P.R., Elegante M.F., Elkhayat S.I., Bartels B.K., Tien A.K., Tien D.H., Mohnot S., Beeson E., Glasgow E., Amri H., Zukowska Z., Kalueff A.V. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behavioural Brain Research 2009, 205:38-44.
36. Eissa B.L., Ossana N.A., Ferrari L., Salibiàn A. Quantitative behavioral parameters as toxicity biomarkers: fish responses to waterborne cadmium. Archives of Environment Contamination and Toxicology 2010, 58:1032-1039.
37. Faber S. Saxitoxin and the induction of paralytic shellfish poisoning. Journal of Young Investigators 2012, 23(1):1-7.
38. Ferrão-Filho A.S., Kozlowsky-Suzuk B. Cyanotoxins: bioaccumulation and effects on aquatic animals. Marine Drugs 2011, 9:2729-2772.
39. Ferrão-Filho A.S., Cunha R., Magalhães V.F., Soares M.C.S., Baptista D.F. Evaluation of Sub-lethal Toxicity of Cyanobacteria on the Swimming Activity of Aquatic Organisms by Image Analysis. Journal of the Brazilian Society of Ecotoxicology 2007, 2(2):1-8.
40. Ferreira F.M.B., Franco J.M., Fidalgo M.L., Fernandez-Vila P. PSP toxins from Aphanizomenon flos-aquae (cyanobacteria) collected in the Crestuma-Lever reservoir (Douro river, Northern Portugal). Toxicon 2001, 39:757-761.
41. Festa-Bianchet M., Apollonio M. Animal Behaviour and Wildlife Conservation 2003, Island Press, Washington, DC.
42. Foreman M.B., Eaton R.C. The direction change concept for reticulospinal control of goldfish escape. Journal of Neuroscience 1993, 13:4101-4133.
43. Garcia C., del Carmen Bravo M., Lagos M., Lagos N. Paralytic shellfish poisoning: Post-mortem analysis of tissue and body fluid samples from human victims in the Patagonia fjords. Toxicon 2004, 43:149-158.
44. Genovese R.F., Benton B.J., Lee E.H., Shippee S.J., Jakubowski E.M. Behavioral and biochemical evaluation of sub-lethal inhalation exposure to VX in rats. Toxicology 2007, 232:109-118.
45. Gerlai R., Lahav M., Guo S., Rosenthal A. Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacology Biochemistry and Behavior 2000, 67:773-782.
46. Gerlai R., Lee V., Blaser R. Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio). Pharmacology Biochemistry and Behavior 2006, 85:752-761.
47. Gerlai R. Zebrafish: an uncharted behavior genetic model. Behavior Genetics 2003, 33:461-468.
48. Gerlai R., Ahmad F., Prajapati S. Differences in acute alcohol-induced behavioral responses among zebrafish populations. Alcoholism: Clinical and Experimental Research 2008, 32(10):1763-1773.
49. Granato M., van Eeden F.J.M., Schach U., Trowe T., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., Nüsslein-Volhard C. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 1996, 123:399-413.
50. Grossman L., Utterback U., Stewart A., Gaikwad S., Wong K., Elegante M., Elkhayat S., Tan J., Gilder T., Wu N., Dileo J., Cachat J., Kalueff A.V. Characterization of behavioral and endocrine effects of LSD on zebrafish. Behavioural Brain Research 2010, 214:277-284.
51. Hackett J.D., Wisecaver J.H., Brosnahan M.L., Kulis D.M., Anderson D.M., Bhattacharya D., Plumley F.G., Erdner D.L. Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Molecular Biology and Evolution 2012, 0(0):1-9. 10.1093/molbev/mss142.
52. Hale M.E. Locomotor mechanics during early life history: effects of size and ontogeny on fast-start performance of salmonid fishes. Journal of Experimental Biology 1999, 202:1465-1479.
53. Hale M.E. S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. Journal of Experimental Biology 2002, 205:2005-2016.
54. Hallegraeff G.M. Harmful algal blooms: a global overview. Manual on Harmful Marine Microalgae 2005, 25-49. Imprimerie Landais, France. D.M. Anderson, A.D. Cembella, G.M. Hallegraeff (Eds.).
55. Hallegraeff G.M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology 2010, 46:220-235.
56. Irons T.D., MacPhail R.C., Hunter D.L., Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicology and Teratology 2010, 32:84-90.
57. Jackim E., Gentile J. Toxins of a blue-green alga: similarity to saxitoxin. Science 1968, 162:915-916.
58. Jansen K.L., Cole T.B., Park S.S., Furlong C.E., Costa L.G. Paraoxonase 1 (PON1) modulates the toxicity of mixed organophosphorus compounds. Toxicology and Applied Pharmacology 2009, 236:142-153.
59. Jellett J.F., Stewart J.E., Laycock M.V. Toxicological evaluation of saxitoxin, neosaxitoxin, gonyautoxin II, gonyautoxin II plus III and decarbamoylsaxitoxin with the mouse neuroblastoma cell bioassay. Toxicology in Vitro 1995, 9(1):57-65.
60. Jiang T.J., Wang D.Z., Niu T., Xu Y.X. Trophic transfer of paralytic shellfish toxins from the cladoceran (Moina mongolica) to larvae of the fish (Sciaenops ocellatus). Toxicon 2007, 50:639-645.
61. Kanoshina I., Lips U., Leppänen J.M. The influence of weather conditions (temperature and wind) on cyanobacterial bloom development in the Gulf of Finland (Baltic Sea). Harmful Algae 2003, 2:29-41.
62. Kist L.W., Piato A.L., da Rosa J.G.S., Koakoski G., Gil Barcellos L.J., Yunes J.S., Bonan C.D., Bogo M.R. Acute exposure to microcystin-producing cyanobacterium microcystis aeruginosa alters adult zebrafish (Danio rerio) swimming performance parameters. Journal of Toxicology 2011, 1155:280-304.
63. Kily L.J., Cowe Y.C., Hussain O., Patel S., McElwaine S., Cotter F.E., et al. Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways. The Journal of Experimental Biology 2008, 211:1623-1634.
64. Kistler C., Hegglin D., Würbel H., Köig B. Preference for structured environment in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis). Applied Animal Behaviour Science 2011, 135:318-327.
65. Kotaki Y. Screening of bacteria which convert gonyautoxin 2,3 to saxitoxin. Nippon Suisan Gakk. 1989, 55:1293.
66. Kotaki Y., Oshima Y., Yasumoto T. Bacterial transformation of paralytic shellfish toxins in coral reef crabs and a marine snail. Nippon Suisan Gakkaishi 1985, 51:1009-1013.
67. Kwong R.W.M., Wang W.X., Lam P.K.S., Yu P.K.N. The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquatic Toxicology 2006, 80:82-91.
68. Lassen N., Estey T., Tanguay R.L., Pappa A., Reimers M.J., Vasiliou V. Molecular cloning, baculovirus expression, and tissue distribution of the zebrafish aldehyde dehydrogenase 2. Drug Metabolism and Disposition 2005, 33:649-656.
69. Ledreux A., Thomazeau S., Catherine A., Duval C., Yéprémian C., Marie A., Bernard C. Evidence for saxitoxins production by the cyanobacterium Aphanizomenon gracile in a French recreational water body. Harmful Algae 2010, 10:88-97.
70. Lefebvre K.A., Elder N.E., Hershberger P.K., Trainer V.L., Stehr C.M., Scholz N.L. Dissolved saxitoxin causes transient inhibition of sensorimotor function in larval Pacific herring (Clupea harengus pallasi). Marine Biology 2005, 147:1393-1402.
71. Lefebvre K.A., Trainer V.L., Scholz N.L. Morphological abnormalities and sensorimotor deficits in larval fish exposed to dissolved saxitoxin. Aquatic Toxicology 2004, 66:159-170.
72. Levin E.D., Bencan Z., Cerutti D.T. Anxiolytic effects of nicotine in zebrafish. Physiology and Behavior 2007, 90:54-58.
73. Lieschke G.J., Currie P.D. Animal models of human disease: zebra!sh swim into view. Nature Reviews Genetics 2007, 8:353-367.
74. Liu Y.M., Chen W., Li D.H., Shen Y.W., Li G.B., Liu Y.D. First report of aphantoxins in China-waterblooms of toxigenic Aphanizomenon flos-aquae in Lake Dianchi. Ecotoxicology and Environmental Safety 2006, 65:84-92.
75. Liu Y.M., Chen W., Li D.H., Shen Y.W., Liu Y.D., Song L.R. Analysis of Paralytic Shellfish Toxins in Aphanizomenon DC-1 from Lake Dianchi, China. Environmental Toxicology 2006, 21:289-295.
76. Llewellyn L., Negri A., Quilliam M. High affinity for the rat brain sodium channel of newly discovered hydroxybenzoate saxitoxin analogues from the dinoflagellate Gymnodinium catenatum. Toxicon 2004, 43:101-104.
77. Lu Z., Tomchik S.M. Effects of a red-tide toxin on fish hearing. Journal of Comparative Physiology A 2002, 188:807-813.
78. Macêdo D.S., de Lucena D.F., Queiroz A.I.G., Cordeiro R.C., Araújo M.M., Sousa F.C., Vasconcelos S.M., Hyphantis T.N., Quevedo J., McIntyre R.S., Carvalho A.F. Effects of lithium on oxidative stress and behavioral alterations induced by lisdexamfetamine dimesylate: relevance as an animal model of mania. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2013, 43:230-237.
79. MacPhail R.C., Brooks J., Hunter D.L., Padnos B., Irons T.D., Padilla S. Locomotion in larval zebrafish: influence of time of day, lighting and ethanol. Neurotoxicology 2009, 30:52-58.
80. Magalhães D.P., Cunha R.A., Santos J.A.A., Buss D.F., Baptista D.F. Behavioral response of Zebrafish Danio rerio Hamilton 1822 to sublethal stress by sodium hypochlorite: ecotoxicological assay using an image analysis biomonitoring system. Ecotoxicology 2007, 16:417-422.
81. Mahmood N.A., Carmichael W.W. Paralytic shellfish poisons produced bythe freshwater cyanobacterium Aphanizomenon flos-aquae NH-5. Toxicon 1986, 24:175-186.
82. Martins-Silva C., De Jaeger X., Guzman M.S., Lima R.D., Santos M.S., Kushmerick C., Gomez M.V., Caron M.G., Prado M.A., Prado V.F. Novel strains of mice deficient for the vesicular acetylcholine transporter: insights on transcriptional regulation and control of locomotor behavior. PLoS ONE 2011, 6(3):e17611. 10.1371/journal.pone.0017611.
83. Matsuda K., Kang K.S., Sakashita A., Yahashi S., Vaudry H. Behavioral effect of neuropeptides related to feeding regulation in fish. Annals of the New York Academy of Sciences 2011, 1220:117-126.
84. Michaud S., Levasseur M., Doucette G., Cantin G. Particle size fractionation of paralytic shellfish toxins (PSTs):seasonal distribution and bacterial production in the St Lawrence estuary, Canada. Toxicon 2002, 40:1451-1462.
85. Miller A.H. Mechanisms of cytokine-induced behavioral changes: psychoneuroimmunology at the translational interface. Brain, Behavior, and Immunity 2009, 23:149-158.
86. Mueller T., Vernier P., Wullimann M.F. The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Research 2004, 1011:156-169.
87. Müller U.K., Van Leeuwen J.L. Undulatory fish swimming: from muscles to flow. Fish and Fisheries 2006, 7:84-103.
88. Nimkerdphol K., Nakagaw M. Effect of sodium hypochlorite on zebrafish swimming behavior estimated by fractal dimension analysis. Journal of Bioscience and Bioengineering 2008, 105(5):486-492.
89. Nogueira I.C., Pereira P., Dias E., Pflugmacher S., Wiegand C., Franca S., Vasconcelos V.M. Accumulation of paralytic shellfish toxins (PST) from the cyanobacterium Aphanizomenon issatschenkoi by the cladoceran Daphnia magna. Toxicon 2004, 44(7):773-780.
90. Norton W., Bally-Cuif L. Adult zebrafish as a model organism for behavioural genetics. BMC Neuroscience 2010, 11:90.
91. Oberemm A., Becker J., Codd G.A., Steinberg C. Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians. Environmental Toxicology 1999, 14:77-88.
92. Olli K., Heiskanen A.S. Seasonal stages of phytoplankton community structure and sinking loss in the Gulf of Riga. Journal of Marine Systems 1999, 23:165-184.
93. Oshima Y. Chemical and enzymatic transformation of paralytic shellfish toxins in marine organisms. Harmful Marine Algal Blooms 1995, Lavoisier, Paris, France. P. Lassus, G. Arzul, E. Erard, P. Gentien, C. Marcaillou (Eds.).
94. Oshima Y. Postcolumn derivatization liquid-chromatography method for paralytic shellfish toxins. Journal of AOAC International 1995, 78:528-532.
95. Paerl H.W., Huisman J. Blooms like it hot. Science 2008, 320:57-58.
96. Panula P., Sallinen V., Sundvik M., Kolehmainen J., Torkko V., Tiittula A., Moshnyakov M., Podlasz P. Modulatory neurotransmitter systems and behavior: towards zebrafish models of neurodegenerative diseases. Zebrafish 2006, 3:235-247.
97. Pereira P., Dias E., Franca S., Pereira E., Carolino M., Vasconcelos V. Accumulation and depuration of cyanobacterial paralytic shellfish toxins by the freshwater mussel Anodonta cygnea. Aquatic Toxicology 2004, 68:339-350.
98. Pereira P., Onodera H., Andrinolo D., Franca S., Araujo F., Lagos N., Oshima Y. Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flos aquae, isolated from Montargil reservoir, Portugal. Toxicon 2000, 38:1689-1702.
99. Pereira V.M., Bortolotto J.W., Kist L.W., de Azevedo M.B., Fritsch R.S., Oliveira R.L., Pereira T.C.B., Bonan C.D., Vianna Mo.R., Bogo M.R. Endosulfan exposure inhibits brain AChE activity and impairs swimming performance in adult zebrafish (Danio rerio). Neurotoxicology 2012, 33:469-475.
100. Perreault F., Matias M.S., Melegari S.P., Carvalho-Pinto C.R.S., Creppy E.E., Popovic R., Matias W.G. Investigation of animal and algal bioassays for reliable saxitoxin ecotoxicity and cytotoxicity risk evaluation. Ecotoxicology and Environment Safety 2011, 74:1021-1026.
101. Prol M.J., Guisande C., Barreiro A., Míguez B., de la Iglesia P., Villar A., Gago-Martínez A., Combarro M.P. Evaluation of the production of paralytic shellfish poisoning toxins by extracellular bacteria isolated from the toxic dinoflagellate Alexandrium minutum. Canadian Journal of Microbiology 2009, 55:943-954.
102. Rao J.V., Begum G., Pallela R., Usman P.K., Rao N.R. Changes in behavior and brain acetylcholinesterase activity in mosquito fish Gambusia affinis in response to the sub-lethal exposure to Chlorpyrifos. International Journal of Environmental Research and Public Health 2005, 2:478-483.
103. Rao J.V., Begum G., Sridhar V., Chakra Reddy N. Sublethal effects of monocrotophos on locomotor behavior and gill architecture of the mosquito fish Gambusia affinis. Journal of Environmental Science and Health, Part B 2005, 40:813-825.
104. Reimers M.J., Hahn M.E., Tanguay R.L. Two zebrafish alcohol dehydrogenases share common ancestry with mammalian class I, II, IV, and V alcohol dehydrogenase genes but have distinct functional characteristics. Journal of Biological Chemistry 2004, 279:38303-38312.
105. Richetti S.K., Rosemberg D.B., Ventura-Lima J., Monserrat J.M., Bogo M.R., Bonan C.D. Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology 2011, 32:116-122.
106. Rico E.P., Rosemberg D.B., Senger M.R., Arizi M., de B., Bernardi G.F., Dias R.D., Bogo M.R., Bonan C.D. Methanol alters ecto-nucleotidases and acetylcholinesterase in zebrafish brain. Neurotoxicology and Teratology 2006, 28:489-496.
107. Rico E.P., Rosemberg D.B., Dias R.D., Bogo M.R., Bonan C.D. Ethanol alters acetylcholinesterase activity and gene expression in zebrafish brain. Toxicology Letters 2007, 174:25-30.
108. Rodrigues A., Fighera R.A., Souza T.M., Schild A.L., Barros C.S. Neuropathology of naturally occurring Trypanosoma evansi infection in horses. Veterinary Pathology 2009, 46:251-258.
109. Rodrigues S.M., de Carvalho M., Mestre T., Ferreira J.J., Coelho M., Peralta R., Vale P. Paralytic shellfish poisoning due to ingestion of Gymnodinium catenatum contaminated cockles - Application of the AOAC HPLC Official Method. Toxicon 2012, 59:558-566.
110. Rosemberg D.B., Braga M.M., Rico E.P., Loss C.M., Córdova S.D., Mussulini B.H.M., Blaser R.E., Leite C.E., Campos M.M., Dias R.D., Calcagnotto M.E., de Oliveira D.L., Souza D.O. Behavioral effects of taurine pretreatment in zebrafish acutely exposed to ethanol. Neuropharmacology 2012, 63:613-623.
111. Rosemberg D.B., da Rocha R.F., Rico E.P., Zanotto-Filho A., Dias R.D., Bogo M.R., Bonan C.D., Moreir J.C.F., Klamt F., Souza D.O. Taurine prevents enhancement of acetylcholinesterase activity induced by acute ethanol exposure and decreases the level of markers of oxidative stress in zebrafish brain. Neuroscience 2010, 171:683-692.
112. Samson J.C., Shumway S.E., Weis J.S. Effects of the toxic dinoflagellate, Alexandrium fundyense on three species of larval fish: a food-chain approach. Journal of Fish Biology 2008, 72:168-188.
113. Santi A., Menezes C., Duarte M.M.F., Leitemperger J., Lópes T., Loro V.L. Oxidative stress biomarkers and acetylcholinesterase activity in human erythrocytes exposed to clomazone (in vitro). Interdisciplinary Toxicology 2011, 4(3):149-153.
114. Savio L.E.B., Vuaden F.C., Piato A.L., Bonan C.D., Wyse A.T.S. Behavioral changes induced by long-term proline exposure are reversed by antipsychotics in zebrafish. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2012, 36:258-263.
115. Schreck C.B., Olla B.L., Davis M.W. Behavioral responses to stress. Fish Stress and Health in Aquaculture 1997, 145-170. Cambridge University Press, Cambridge. G.K. Iwama, A.D. Pickering, J.P. Sumpter, C.B. Schreck (Eds.).
116. Scott G.R., Sloman K.A. The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquatic Toxicology 2004, 68:369-392.
117. Shimizu Y., Yoshioka M. Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. Science 1981, 212:547-549.
118. Shin J.T., Fishman M.C. From zebrafish to human: modular medical models. Annual Review of Genomics and Human Genetics 2002, 3:311-340.
119. Sison M., Cawker J., Buske C., Gerlai R. Fishing for genes of vertebrate behavior: zebra fish as an upcoming model system. Lab Animal 2006, 35:33-39.
120. Sison M., Gerlai R. Behavioral performance altering effects of MK-801 in zebrafish (Danio rerio). Behavioural Brain Research 2011, 220:331-337.
121. Spence R., Fatema M.K., Reichard M., Huqk K.A., Wahab M.A., Ahmed Z.F., Smith C. The distribution and habitat preferences of the zebrafish in Bangladesh. Journal of Fish Biology 2006, 69:1435-1448.
122. Sugawara A., Imamura T., Aso S., Ebitani K. Change of paralytic shellfish poison by the marine bacteria living in the intestine of the Japanese surf clam, Pseudocardium sybillae, and the brown sole, Pleuronectes herensteini. Scientific Reports of the Hokkaido Fisheries Experiment Station 1997, 50:35-42.
123. Sullivan J.J., Iwaoka W.T., Liston J. Enzymatic transformation of PSP toxins in the littleneck clam (Protothaca staminea). Biochemical and Biophysical Research Communications 1983, 114:465-472.
124. Sutherland W.J. The effect of local change in habitat quality on populations of migratory species. Journal of Applied Ecology 1998, 35:418-421.
125. Tiedeken J.A., Ramsdell J.S. DDT exposure of zebrafish embryos enhances seizure susceptibility: relationship to fetal p,p'-DDE burden and domoic acid exposure of California Sea Lions. Environmental Health Perspectives 2009, 117(1):68-73.
126. Tierney K.B. Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochimica et Biophysica Acta 2011, 1812:381-389.
127. Trainer V.L., Bill B.D. Characterization of a domoic acid binding site from Pacific razor clam. Aquatic Toxicology 2004, 69:125-132.
128. Tropepe V., Sive H.L. Can zebrafish be used as a model to study the neurodevelopmental causes of autism?. Genes, Brain and Behavior 2003, 2(5):268-281.
129. Usup G., Leaw C.P., Cheah M.Y., Ahmad A., Ng B.K. Analysis of paralytic shellfish poisoning toxin congeners by a sodium channel receptor binding assay. Toxicon 2004, 44:37-43.
130. van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 2003, 13:57-149.
131. Vogl C., Grillitsch B., Wytek R., Spieser O.H., Scholz W. Qualification of spontaneous undirected locomotor behaviour of fish for sublethal toxicity testing. Part I. Variability of measurement parameters under general test conditions. Environmental Toxicology and Chemistry 1999, 18:2736-2742.
132. Wardle C., Videler J., Altringham J. Tuning in to fish swimming waves: body form, swimming mode and muscle function. Journal of Experimental Biology 1995, 198:1629-1636.
133. Wiese M., D'Agostino P.M., Mihali T.K., Moffitt M.C., Neilan B.A. Neurotoxic alkaloids: saxitoxin and its analogs. Marine Drugs 2010, 8:2185-2211.
134. Wörmer L., Cirés S., Agha R., Verdugo M., de Hoyos C., Quesada A. First detection of cyanobacterial PSP (paralytic shellfish poisoning) toxins in Spanish freshwaters. Toxicon 2011, 57:918-921.
135. Wu S.M., Tsai P.R., Yan C.J. Maternal cadmium exposure induces mt2 and smtB mRNA expression in zebrafish (Danio rerio) females and their offspring. Comparative Biochemistry and Physiology Part C 2012, 156:1-6.
136. Wu W.J., Li G.B., Li D.H., Liu Y.D. Temperature may be the dominating factor on the alternant succession of Aphanizomenon flos-aquae and Microcystis aeruginosa in Dianchi Lake. Fresenius Environment Bulletin 2010, 19:846-853.
137. Xing W., Huang W.M., Liu Y.D., Li D.H., Shen Y.W., Li G.B. Environmental mechanism of change in cyanobacterial species composition in the northeastern part of Lake Dianchi (China). Fresenius Environment Bulletin 2007, 17:82-90.
138. Yokoo H., Shiraishi S., Kobayashi H., Yanagita T., Minami S.I., Yamamoto R., Wada A. Short-and long-term differential effects of neuroprotective drug NS-7 on voltage-dependent sodium channels in adrenal chromaffin cells. British Journal of Pharmacology 2000, 131:779-787.
139. Zaccaroni A., Scaravelli D. Toxicity of sea algal toxins to humans and animals. NATO Security through Science Series C: Environmental Security: Algal Toxins: Nature, Occurrence, Effect and Detection 2008, 91-158. Springer, Netherlands. V. Evangelista, L. Barsanti, A.M. Frassanito, P. Passarelli, P. Gualtieri (Eds.).
140. Zhang D.L., Hu C.X., Wang G.H., Li D.H., Li G.B., Liu Y.D. Zebrafish neurotoxicity from aphantoxins-cyanobacterial Paralytic Shellfish Poisons (PSPs) from Aphanizomenon flos-aquae DC-1. Environmental Toxicology 2011, 0(0):1-16. 10.1002/tox.20714.
141. Zhang D.L., Hu C.X., Wang G.H., Liu Y.D., Li D.H., Li G.B., Shen Y.W. Response of apoptotic genes to aphantoxin-paralytic shellfish poison in freshwater extracted from the Aphanizomenon flos-aquae DC-1 in cells of brain on zebrafish. Acta Hydrobiologica Sinica 2011, 35(2):238-245.
142. Zhang H.Y., Ludsin S.A., Mason D.M., Adamack A.T., Brandt S.B., Zhang X.S., Kimmel D.G., Roman M.R., Boicourt W.C. Hypoxia-driven changes in the behavior and spatial distribution of pelagic fish and mesozooplankton in the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 2009, 381:S80-S91.