Advertisement

Perinatal Domoic Acid as a Neuroteratogen

  • Tracy A. Doucette
  • R. Andrew TaskerEmail author
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 29)

Abstract

In mammals, the period shortly before and shortly after birth is a time of massive brain growth, plasticity and maturation. It is also a time when the developing brain is exquisitely sensitive to insult, often with long-lasting consequences. Many of society’s most debilitating neurological diseases arise, at least in part, from trauma around the time of birth but go undetected until later in life. For the past 15 years, we have been studying the consequences of exposure to the AMPA/kainate agonist domoic acid (DOM) on brain development in the rat. Domoic acid is a naturally occurring excitotoxin that enters the food chain and is known to produce severe neurotoxicity in humans and other adult wildlife. Our work, and that of others, however, has demonstrated that DOM is also toxic to the perinatal brain and that toxicity occurs at doses much lower than those required in adults. This raises concern about the current regulatory limit for DOM contamination that is based on data in adult animals, but has also allowed creation of a novel model of neurological disease progression. Herein, we review briefly the toxicity of DOM in adults, including humans, and describe features of the developing nervous system relevant to enhanced risk. We then review the data on DOM as a prenatal neuroteratogen and describe in detail the work of our respective laboratories to characterize the long-term behavioural and neuropathological consequences of exposure to low-dose DOM in the newborn rat.

Keywords

Glutamate receptors Amnesic shellfish toxin Seizures Epilepsy Schizophrenia Social interaction Attentional processing Cognition 

Notes

Acknowledgements

Research attributed to the Doucette and Tasker laboratories was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canadian Institutes of Health Research (CIHR), Atlantic Innovation Fund (AIF), Springboard Atlantic and Innovation PEI. T.A. Doucette holds the Jeanne and J Louis Levesque Research Professorship and receives partial salary support from Neurodyn Life Sciences Inc.

References

  1. Adams AL, Doucette TA, Ryan CL (2008) Altered pre-pulse inhibition in adult rats treated neonatally with domoic acid. Amino Acids 35:157–160CrossRefGoogle Scholar
  2. Adams AL, Doucette TA, James R, Ryan CL (2009) Persistent changes in learning and memory in rats following neonatal treatment with domoic acid. Physiol Behav 96:505–512CrossRefGoogle Scholar
  3. Bates SS, Horner RA (1998) Bloom dynamics and physiology of domoic-acid-producing Pseudo-nitzschia species. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Heidelberg, pp 267–292Google Scholar
  4. Bates SS, Trainer VL (2006) The ecology of harmful diatoms. In: Granéli E, Turner J (eds) Ecology of harmful algae. Ecological studies, vol 189. Springer, Heidelberg, pp 81–93Google Scholar
  5. Bernard PB, MacDonald DS, Gill DA, Ryan CL, Tasker RA (2007) Hippocampal mossy fiber sprouting and elevated trkB receptor expression following systemic administration of low dose domoic acid during neonatal development. Hippocampus 17:1121–1133CrossRefGoogle Scholar
  6. Brodie EC, Gulland FMD, Greig DJ, Hunter M, Jaakola J, Leger J, Leighfield TA, Van Dolan FM (2006) Domoic acid causes reproductive failure in California sea lions (Zalophus californianus). Mar Mammal Sci 22(3):700–707CrossRefGoogle Scholar
  7. Burt MA, Ryan CL, Doucette TA (2008a) Altered responses to novelty and drug reinforcement in adult rats treated neonatally with domoic acid. Physiol Behav 93:327–336CrossRefGoogle Scholar
  8. Burt MA, Ryan CL, Doucette TA (2008b) Low dose domoic acid in neonatal rats abolishes nicotine induced conditioned place preference during late adolescence. Amino Acids 35:247–249CrossRefGoogle Scholar
  9. Can Dis Wkly Rep (1990) Proceedings of a symposium on domoic acid. Can Dis Wkly Rep 16:Suppl. 1EGoogle Scholar
  10. Cendes F, Andermann F, Carpenter S et al (1995) Temporal lobe epilepsy caused by domoic acid intoxication: evidence for glutamate receptor-mediated excitotoxicity in humans. Ann Neurol 37:123–126CrossRefGoogle Scholar
  11. Clancy B, Finlay BL, Darlington RB, Anand KJS (2007) Extrapolating brain development from experimental species to humans. Neurotoxicol 28(5):931–937CrossRefGoogle Scholar
  12. Colombo J (1982) The critical period concept: research, methodology, and theoretical issues. Psychol Bull 91(2):260–275CrossRefGoogle Scholar
  13. Dakshinamurti K, Sharma SK, Sundaram M, Watanabe T (1993) Hippocampal changes in developing postnatal mice following intrauterine exposure to domoic acid. J Neurosci 13(10):4486–4495CrossRefGoogle Scholar
  14. Dobbing J (1976) Vulnerable periods in brain growth and somatic growth. In: Roberts DF, Thomson AM (eds) The biology of human fetal growth. Taylor & Francis, London, pp 137–147Google Scholar
  15. Dobbing J, Sands J (1979) Comparative aspects of the brain growth spurt. Early Hum Dev 3:79–83CrossRefGoogle Scholar
  16. Dobbing J, Smart JL (1974) Vulnerability of developing brain and behaviour. Br Med Bull 30:164–168CrossRefGoogle Scholar
  17. Doucette TA, Tasker RA (2008) Domoic acid: detection methods, pharmacology and toxicology. In: Botana LM (ed) Seafood and freshwater toxins. Pharmacology, physiology and detection (2nd edn). CRC Press, Taylor Francis Group, New York, pp 398–429Google Scholar
  18. Doucette TA, Strain SM, Allen GV, Ryan CL, Tasker RAR (2000) Comparative behavioural toxicity of domoic acid and kainic acid in neonatal rats. Neurotox Teratol 22:863–869CrossRefGoogle Scholar
  19. Doucette TA, Bernard PB, Yuill PC, Tasker RA, Ryan CL (2003) Low doses of non-NMDA glutamate receptor agonists alter neurobehavioral development in the rat. Neurotoxicol Teratol 25:473–479CrossRefGoogle Scholar
  20. Doucette TA, Bernard PB, Husum H, Perry MA, Ryan CL, Tasker RA (2004) Low doses of domoic acid during postnatal development produce permanent changes in rat behaviour and hippocampal morphology. Neurotox Res 6(7, 8):555–563CrossRefGoogle Scholar
  21. Doucette TA, Ryan CL, Tasker RA (2007) Gender-based changes in cognition and emotionality in a new rat model of epilepsy. Amino Acids 32:317–322CrossRefGoogle Scholar
  22. Gill DA, Bastlund JF, Anderson NJ, Tasker RA (2009) Reductions in paradoxical sleep time in adult rats treated neonatally with low dose domoic acid. Behav Brain Res 205:564–567CrossRefGoogle Scholar
  23. Gill DA, Bastlund JF, Watson WP, Ryan CL, Reynolds DS, Tasker RA (2010a) Neonatal exposure to low-dose domoic acid lowers seizure threshold in adult rats. Neuroscience 169:1789–1799CrossRefGoogle Scholar
  24. Gill DA, Ramsay R, Tasker RA (2010b) Selective reductions in subpopulations of GABAergic neurons in a developmental rat model of epilepsy. Brain Res 1331:114–123CrossRefGoogle Scholar
  25. Gill DA, Perry MA, McGuire EP, Perez-Gomez A, Tasker RA (2012) Low-dose neonatal domoic acid causes persistent changes in behavioural and molecular indicators of stress response in rats. Behav Brain Res 230:409–417CrossRefGoogle Scholar
  26. Goldstein T, Mazet JAK, Zabka TS et al (2008) Novel symptomatology and changing epidemiology of domoic acid toxicosis in California sea lions (Zalophus californianus): an increasing risk to marine mammal health. Proc R Soc B 275:267–276CrossRefGoogle Scholar
  27. Gulland FMD, Haulena M, Fauguier D et al (2002) Domoic acid toxicity in Californian sea lions (Zalophus californianus): clinical signs, treatment and survival. Vet Record 150:475–480CrossRefGoogle Scholar
  28. Holmes GL, Sarkisian M, Ben-Ari Y, Chevassus-Au-Louis N (1999) Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 22:537–553CrossRefGoogle Scholar
  29. Kaufmann W (2000) Developmental neurotoxicity. In: Krinke GJ (ed) The handbook of experimental animals: the laboratory rat. Academic Press, New York, pp 227–252CrossRefGoogle Scholar
  30. Levin ED, Pizarro K, Pang WG, Harrison J, Ramsdell JS (2005) Persisting behavioural consequences of prenatal domoic acid exposure in rats. Neurotox Teratol 27(5):719–725CrossRefGoogle Scholar
  31. Lujan R, Shigemoto R, Lopez-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580CrossRefGoogle Scholar
  32. Marriott AL, Ryan CL, Doucette TA (2012) Neonatal domoic acid treatment produces alterations to prepulse inhibition and latent inhibition in adult rats. Pharm Biochem Behav 103:338–344CrossRefGoogle Scholar
  33. Marriott AL, Tasker RA, Ryan CL, Doucette TA (2014) Neonatal domoic acid abolishes latent inhibition in male but not female rats and has differential interactions with social isolation. Neurosci Lett 578:22–26CrossRefGoogle Scholar
  34. Marriott AL, Tasker RA, Ryan CL, Doucette TA (2015) Alterations to prepulse inhibition magnitude and latency in adult rats following neonatal treatment with domoic acid and social isolation rearing. Behav Brain Res doi: 10.1016/j.bbr.2015.11.009 [Epub ahead of print]
  35. Maucher JM, Ramsdell JS (2007) Maternal-fetal transfer of domoic acid in rats at two gestational time points. Environ Health Perspect 115(12):1743–1746CrossRefGoogle Scholar
  36. Maucher-Fuquay J, Muha N, Wang Z, Ramsdell JS (2012) Elimination kinetics of domoic acid from the brain and cerebrospinal fluid of the pregnant rat. Chem Res Toxicol 25(12):2805–2809CrossRefGoogle Scholar
  37. McNamara RK, Skelton RW (1993) The neuropharmacological and neurochemical basis of place learning in the Morris Water Maze. Brain Res Brain Res Rev 18:33–49CrossRefGoogle Scholar
  38. Moshe SL, Alabala BJ, Ackermann RF, Engel J Jr (1983) Increased seizure susceptibility of the immature brain. Brain Res 283:81–85CrossRefGoogle Scholar
  39. Pérez-Gómez A, Tasker RA (2012) Enhanced neurogenesis in organotypic cultures of rat hippocampus after transient subfield-selective excitotoxic insult induced by domoic acid. Neuroscience 208:97–108CrossRefGoogle Scholar
  40. Pérez-Gómez A, Tasker RA (2013) Transient domoic acid excitotoxicity increases BDNF expression and activates both MEK- and PKA-dependent neurogenesis in organotypic hippocampal slices. BMC Neurosci 14(1):72 (13 pages online only)CrossRefGoogle Scholar
  41. Pérez-Gómez A, Tasker RA (2014a) Domoic acid as a neurotoxin. In: Kostrewza R (ed) Handbook of neurotoxicity. Springer, New York, pp 399–419Google Scholar
  42. Pérez-Gómez A, Tasker RA (2014b) Enhanced mossy fibre sprouting and synapse formation in organotypic hippocampal cultures following transient domoic acid excitotoxicity. Neurotox Res 25:402–410CrossRefGoogle Scholar
  43. Perl TM, Bedard L, Kosatsky T et al (1990) An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N Engl J Med 322:1775–1780CrossRefGoogle Scholar
  44. Perry MA, Ryan CL, Tasker RA (2009) Effects of low dose neonatal domoic acid administration on behavioural and physiological response to mild stress in adult rats. Physiol Behav 98:53–59CrossRefGoogle Scholar
  45. Pulido OM (2008) Domoic acid toxicologic pathology: a review. Mar Drugs 6:180–219CrossRefGoogle Scholar
  46. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281–294CrossRefGoogle Scholar
  47. Ramsdell JS, Zabka TS (2008) In utero domoic acid toxicity: a fetal basis to adult diseases in the California sea lion (Zalophus californianus). Mar Drugs 6(2):262–290CrossRefGoogle Scholar
  48. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(3):511–533PubMedPubMedCentralGoogle Scholar
  49. Ritter LM, Vazquez DM, Meador-Woodruff JH (2002) Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Dev Brain Res 139:227–236CrossRefGoogle Scholar
  50. Robbins MA, Ryan CL, Marriott AL, Doucette TA (2013) Temporal memory dysfunction and alterations in tyrosine hydroxylase immunoreactivity in adult rats following neonatal exposure to domoic acid. Neurosci Med 4:29–35CrossRefGoogle Scholar
  51. Ryan CL, Robbins MA, Smith MT, Gallant IC, Adams-Marriott AL, Doucette TA (2011) Altered social interaction in adult rats following neonatal treatment with domoic acid. Physiol Behav 102:291–295CrossRefGoogle Scholar
  52. Scholin CA, Gulland F, Doucette GJ et al (2000) Mortality of sea lions among the central California coast linked to a toxic diatom bloom. Nature 403:80–84CrossRefGoogle Scholar
  53. Schulz JB, Falkenburger BH (2004) Neuronal pathology in Parkinson’s disease. Cell Tissue Res 318:135–137CrossRefGoogle Scholar
  54. Shaw CA, Hoglinger GU (2008) Neurodegenerative diseases: neurotoxins as sufficient etiological agents? Neuromolecular Med 10:1–9CrossRefGoogle Scholar
  55. Sierra-Beltran A, Palafox-Uribe M, Grajales-Montiel J et al (1997) Sea bird mortality at Cabo San Lucas, Mexico: evidence that toxic diatom blooms are spreading. Toxicon 35:447–453CrossRefGoogle Scholar
  56. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Meth 37:173–182CrossRefGoogle Scholar
  57. Suzuki CAM, Hierlihy SL (1993) Renal clearance of domoic acid in the rat. Food Chem Toxicol 31(10):701–706CrossRefGoogle Scholar
  58. Tanemura K, Igarashi K, Matsugami TR, Aisaki K-I, Kitajima S, Kanno J (2009) Intrauterine environment-genome interaction and Children’s development (2): brain structure impairment and behavioural disturbance induced in male mice offspring by a single intraperitoneal administration of domoic acid (DA) to their dams. J Toxicol Sci 34:SP279–SP286CrossRefGoogle Scholar
  59. Tasker RA (2015) Domoic acid and other amnesic toxins: toxicological profile. Mar Freshw Toxins 1–16Google Scholar
  60. Tasker RA, Connell BJ, Strain SM (1991) Pharmacology of systemically administered domoic acid in mice. Can J Physiol Pharmacol 69:378–382CrossRefGoogle Scholar
  61. Tasker RA, Strain SM, Drejer J (1996) Selective reduction in domoic acid toxicity in vivo by a novel non-N-methyl-D-aspartate receptor antagonist. Can J Physiol Pharmacol 74:1047–1054CrossRefGoogle Scholar
  62. Tasker RAR, Perry MA, Doucette TA, Ryan CL (2005) NMDA receptor involvement in the effects of low dose domoic acid in neonatal rats. Amino Acids 28:193–196CrossRefGoogle Scholar
  63. Tasker RAR, Kuiper-Goodman T, Pulido O, Lawrence JF (2011) Domoic acid. In: Lawrence J, Loreal H, Toyofuku H, Karunasagar I, Ababouch L (eds) Assessment and management of biotoxin risks in bivalve molluscs. FAO Fisheries and Aquaculture Technical Paper No. 551. Rome, FAOGoogle Scholar
  64. Teitelbaum J, Zatorre R, Carpenter S et al (1990) Neurological sequelae of domoic acid intoxication due to ingestion of contaminated mussels. N Engl J Med 322:1781–1787CrossRefGoogle Scholar
  65. Tiedeken JA, Ramsdell JS (2007) Embryonic exposure to domoic acid increases the susceptibility of zebrafish larvae to the chemical convulsant pentylenetetrazole. Environ Health Perspect 115(11):1547–1552CrossRefGoogle Scholar
  66. Tiedeken JA, Ramsdell JS, Ramsdell AF (2005) Developmental toxicity of domoic acid in zebrafish (Danio rerio). Neurotoxicol Teratol 27(5):711–717CrossRefGoogle Scholar
  67. Tryphonas L, Truelove J, Nera E, Iverson F (1990) Acute neurotoxicity of domoic acid in the rat. Toxicol Pathol 18:1–9CrossRefGoogle Scholar
  68. Verdoorn TA, Johansen TH, Drejer J, Nielsen EO (1994) Selective block of recombinant GluR6 receptors by NS-102, a novel non-NMDA receptor antagonist. Eur J Pharmacol 269:43–49CrossRefGoogle Scholar
  69. Vernadakis A, Woodbury DM (1969) The developing animal as a model. Epilepsia 10:163–178CrossRefGoogle Scholar
  70. Vorhees CV (1986) Principles of behavioral teratology. In: Riley EP, Vorhees CV (eds) Handbook of behavioral teratology. Plenum Press, New York, pp 23–48CrossRefGoogle Scholar
  71. Work TM, Barr B, Beal AM, Fritz L, Quilliam MA, Wright JLC (1993) Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus occidentalis) and Brant’s cormorants (Phalacrocorax penicillatus) in California. J Zoo Wildl Med 24(1):54–62Google Scholar
  72. World Health Organization (2006) Neurology and public health. http://www.who.int/mental_health/neurology/en
  73. Wright JLC, Bird CJ, deFreitas ASW, Hampson D, McDonald J, Quilliam MA (1990) Chemistry, biology, and toxicology of domoic acid and its isomers. Can Dis Wkly Rep 16(Suppl. 1E):15–18Google Scholar
  74. Xi D, Peng YG, Ramsdell JS (1997) Domoic acid is a potent neurotoxin to neonatal rats. Nat Toxins 5:74–79CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of Prince Edward IslandCharlottetownCanada
  2. 2.Department of Biomedical SciencesUniversity of Prince Edward IslandCharlottetownCanada

Personalised recommendations