Acute Restraint Stress in Zebrafish: Behavioral Parameters and Purinergic Signaling

Despite the extensive knowledge about the effects of acute restraint stress (ARS) in rodents, zebrafish research is still elementary in this field, and the consequences of stress on purinergic system are unclear. Therefore, we evaluated the effects of ARS on behavior, biochemical, and molecular parameters in zebrafish brain. Animals were submitted to a 90 min ARS protocol and tested for anxiety levels, exploratory behavior, and memory performance. Furthermore, we analyzed ectonucleotidase and adenosine deaminase activities and their gene expression profile, as well as transcription of adenosine receptors. ARS increased anxiety, but did not impair locomotion or cognition. ARS significantly increased ATP hydrolysis, decreased cytosolic ADA activity, and changed the entpd and adora gene expression. In conclusion, ARS disturbed zebrafish behavior, and we hypothesize that the augmentation in adenosine-mediated signaling may be a strategy to reestablish homeostasis and normal behavior after a stressful event.

[1]  H. Barry,et al.  Stress responses of rats to acute body or neck restraint. , 1970, Physiology & behavior.

[2]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[3]  K. Chan,et al.  A direct colorimetric assay for Ca2+ -stimulated ATPase activity. , 1986, Analytical biochemistry.

[4]  J. Terborgh,et al.  Oddity and the ‘confusion effect’ in predation , 1986, Animal Behaviour.

[5]  T. Pitcher.  Functions of Shoaling Behaviour in Teleosts , 1986 .

[6]  T. Pitcher.  Behaviour of Teleost Fishes , 1986 .

[7]  S. Cabib,et al.  Different effects of acute and chronic stress on two dopamine-mediated behaviors in the mouse , 1988, Physiology & Behavior.

[8]  R. J. Smith,et al.  The influence of alarm substance and shoal size on the behaviour of zebra danios, Brachydanio rerio (Cyprinidae) , 1988 .

[9]  D. Diamond,et al.  Inverted‐U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation , 1992, Hippocampus.

[10]  J. Henley,et al.  Interaction of Guanine Nucleotides with [3H]Kainate and 6‐[3H]Cyano‐7‐Nitroquinoxaline‐2,3‐dione Binding in Goldfish Brain , 1993, Journal of neurochemistry.

[11]  T. Stone,et al.  Anxiolytic activity of adenosine receptor activation in mice , 1995, British journal of pharmacology.

[12]  W. Paré,et al.  Effect of Acute or Repeated Stress on Behavior and Brain Norepinephrine System in Wistar-Kyoto (WKY) Rats , 1997, Brain Research Bulletin.

[13]  C. Florio,et al.  Adenosine A1 receptors modulate anxiety in CD1 mice , 1998, Psychopharmacology.

[14]  M. Westerfield,et al.  Overview of the Zebrafish system. , 1999, Methods in cell biology.

[15]  J. McPherson,et al.  The syntenic relationship of the zebrafish and human genomes. , 2000, Genome research.

[16]  R. Gerlai,et al.  Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects , 2000, Pharmacology Biochemistry and Behavior.

[17]  B. Fredholm,et al.  International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. , 2001, Pharmacological reviews.

[18]  R. Cunha,et al.  Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors , 2001, Neurochemistry International.

[19]  Julio Collado-Vides,et al.  RegulonDB (version 3.2): transcriptional regulation and operon organization in Escherichia coli K-12 , 2001, Nucleic Acids Res..

[20]  G. Guidotti,et al.  Soluble apyrases release adp during ATP hydrolysis. , 2001, Biochemical and biophysical research communications.

[21]  H. Zimmermann.  Ectonucleotidases: Some recent developments and a note on nomenclature , 2001 .

[22]  S. Latini,et al.  Adenosine in the central nervous system: release mechanisms and extracellular concentrations , 2001, Journal of neurochemistry.

[23]  P. Silveira,et al.  Effect of chronic and acute stress on ectonucleotidase activities in spinal cord , 2002, Physiology & Behavior.

[24]  M. Bogo,et al.  ATP and ADP hydrolysis in brain membranes of zebrafish (Danio rerio). , 2003, Life sciences.

[25]  C. Dalmaz,et al.  The effect of stress upon hydrolysis adenine nucleotides in blood serum of rats , 2003, Pharmacology Biochemistry and Behavior.

[26]  Darrell R. Abernethy,et al.  International Union of Pharmacology: Approaches to the Nomenclature of Voltage-Gated Ion Channels , 2003, Pharmacological Reviews.

[27]  Robert Gerlai,et al.  Zebra Fish: An Uncharted Behavior Genetic Model , 2003, Behavior genetics.

[28]  C. Ryer,et al.  Agonistic behavior in a schooling fish: form, function and ontogeny , 1991, Environmental Biology of Fishes.

[29]  M. Bogo,et al.  Ecto-5'-nucleotidase activity in brain membranes of zebrafish (Danio rerio). , 2004, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[30]  R. Cunha,et al.  Presynaptic Modulation Controlling Neuronal Excitability and Epileptogenesis: Role of Kainate, Adenosine and Neuropeptide Y Receptors , 2003, Neurochemical Research.

[31]  C. Dalmaz,et al.  Acute and chronic stress alter ecto-nucleotidase activities in synaptosomes from the rat hippocampus , 2004, Pharmacology Biochemistry and Behavior.

[32]  Jeffrey C. Raum,et al.  Effect of steady and oscillatory shear stress on F-actin content and distribution in neutrophils. , 2004, Biorheology.

[33]  Peter D. Karp,et al.  EcoCyc: a comprehensive database resource for Escherichia coli , 2004, Nucleic Acids Res..

[34]  R. Cunha,et al.  Neuroprotection by adenosine in the brain: From A1 receptor activation to A2A receptor blockade , 2005, Purinergic Signalling.

[35]  L. Zon,et al.  In vivo drug discovery in the zebrafish , 2005, Nature Reviews Drug Discovery.

[36]  D. Stainier,et al.  In vivo cell biology: following the zebrafish trend. , 2006, Trends in cell biology.

[37]  Kim Sneppen,et al.  Structure and function of negative feedback loops at the interface of genetic and metabolic networks , 2006, Nucleic acids research.

[38]  H. Zimmermann.  Ectonucleotidases in the nervous system. , 2008, Novartis Foundation symposium.

[39]  Á. Miklósi,et al.  The zebrafish as a model for behavioral studies. , 2006, Zebrafish.

[40]  Jens Krause,et al.  Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes , 2006, Nature Protocols.

[41]  M. Bogo,et al.  Methanol alters ecto-nucleotidases and acetylcholinesterase in zebrafish brain. , 2006, Neurotoxicology and teratology.

[42]  G. Burnstock,et al.  Purine and pyrimidine receptors , 2007, Cellular and Molecular Life Sciences.

[43]  Edward D. Levin,et al.  Anxiolytic effects of nicotine in zebrafish , 2007, Physiology & Behavior.

[44]  P. Currie,et al.  Animal models of human disease: zebrafish swim into view , 2007, Nature Reviews Genetics.

[45]  Noam Miller,et al.  Quantification of shoaling behaviour in zebrafish (Danio rerio) , 2007, Behavioural Brain Research.

[46]  D. Parichy,et al.  Zebrafish in the wild: a review of natural history and new notes from the field. , 2007, Zebrafish.

[47]  D. Souza,et al.  Adenosine deaminase-related genes: molecular identification, tissue expression pattern and truncated alternative splice isoform in adult zebrafish (Danio rerio). , 2007, Life sciences.

[48]  D. Souza,et al.  Kinetic characterization of adenosine deaminase activity in zebrafish (Danio rerio) brain. , 2008, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[49]  Allan I Pack,et al.  Molecular Mechanisms of Sleep and Wakefulness , 2008, Annals of the New York Academy of Sciences.

[50]  Cristina Saverino,et al.  The social zebrafish: Behavioral responses to conspecific, heterospecific, and computer animated fish , 2008, Behavioural Brain Research.

[51]  E. Levin,et al.  Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety , 2009, Pharmacology Biochemistry and Behavior.

[52]  O. Krishtal,et al.  P2X receptors and synaptic plasticity , 2009, Neuroscience.

[53]  R. Bunte,et al.  Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). , 2009, Journal of the American Association for Laboratory Animal Science : JAALAS.

[54]  D. Mostofsky,et al.  Restraint stress in biobehavioral research: Recent developments , 2009, Neuroscience & Biobehavioral Reviews.

[55]  Allan V. Kalueff,et al.  Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish , 2009, Behavioural Brain Research.

[56]  Geoffrey Burnstock,et al.  Purinergic signalling in the nervous system: an overview , 2009, Trends in Neurosciences.

[57]  G. Burnstock,et al.  Evolutionary origins of the purinergic signalling system , 2009, Acta physiologica.

[58]  M. Vianna,et al.  A one-trial inhibitory avoidance task to zebrafish: Rapid acquisition of an NMDA-dependent long-term memory , 2009, Neurobiology of Learning and Memory.

[59]  Ana M Sebastião,et al.  Adenosine receptors and the central nervous system. , 2009, Handbook of experimental pharmacology.

[60]  D. Souza,et al.  NTPDase family in zebrafish: Nucleotide hydrolysis, molecular identification and gene expression profiles in brain, liver and heart. , 2010, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[61]  Laure Bally-Cuif,et al.  Adult zebrafish as a model organism for behavioural genetics , 2010, BMC Neuroscience.

[62]  Robert Gerlai,et al.  High-Throughput Behavioral Screens: the First Step towards Finding Genes Involved in Vertebrate Brain Function Using Zebrafish , 2010, Molecules.

[63]  Michael K. Richardson,et al.  Translating rodent behavioral repertoire to zebrafish (Danio rerio): Relevance for stress research , 2010, Behavioural Brain Research.

[64]  Robert Gerlai,et al.  Zebrafish antipredatory responses: A future for translational research? , 2010, Behavioural Brain Research.

[65]  Diogo R. Lara,et al.  Effects of anxiolytics in zebrafish: Similarities and differences between benzodiazepines, buspirone and ethanol , 2011, Pharmacology Biochemistry and Behavior.

[66]  M. Calcagnotto,et al.  Differences in Spatio-Temporal Behavior of Zebrafish in the Open Tank Paradigm after a Short-Period Confinement into Dark and Bright Environments , 2011, PloS one.

[67]  M. Bogo,et al.  Unpredictable chronic stress model in zebrafish (Danio rerio): Behavioral and physiological responses , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.