Behavioural and neural deficits induced by rotenone in the pond snail Lymnaea stagnalis. A possible model for Parkinson's disease in an invertebrate

Agnes Vehovszky; Henriette Szabo; Laszlo Hiripi; Christopher J. H. Elliott; Laszlo Hernadi

doi:10.1111/j.1460-9568.2007.05467.x

Behavioural and neural deficits induced by rotenone in the pond snail Lymnaea stagnalis. A possible model for Parkinson's disease in an invertebrate

Agnes Vehovszky, Henriette Szabo, Laszlo Hiripi, Christopher J. H. Elliott, Laszlo Hernadi

Biology

Research output: Contribution to journal › Article › peer-review

Abstract

Parkinson's disease is a neurodegenerative disorder, related to the loss of dopamine (DA)-containing neurons in the substantia nigra. In experimental animals, both vertebrates and invertebrates, rotenone, a commercially available organic pesticide, induces symptoms of Parkinson's disease. We found that that rotenone is toxic to the pond snail Lymnaea stagnalis (4-day LC50 0.8 mu M). Rotenone, at concentrations from 0.1 to 5 mu M, caused progressive and irreversible behavioural deficits in both acute and chronic exposure. Chronic exposure to 0.5 mu M rotenone led to a progressive decrease in spontaneous locomotion and in feeding, reaching almost 100% inhibition of both behaviours by the 7th day of rotenone treatment. In the central nervous system preparation made on the 7th day of treatment the postsynaptic potentials evoked by the identified dopaminergic RPeD1 neuron disappeared whereas the synaptic inputs received by the RPeD1 from a peptidergic neuron (VD4) were still functional. Immunostaining revealed that the tyrosine hydroxylase immunoreactivity decreased below the detectable level in both the RPeD1 cell body and its axonal processes. Finally, HPLC assay showed a significant (25%) decrease in DA level in the CNS by the 7th day of rotenone treatment. We conclude that, as in vertebrates, rotenone disrupts feeding and locomotion of the model mollusc Lymnaea stagnalis. One possible target of rotenone is the dopaminergic neurons in the CNS. We therefore suggest that Lymnaea stagnalis is a suitable invertebrate model for the study of Parkinson's disease, allowing direct analysis of the response of dopaminergic systems to rotenone at behavioural, cellular and neuronal levels.

Original language	English
Pages (from-to)	2123-2130
Number of pages	8
Journal	The European Journal of Neuroscience
Volume	25
Issue number	7
DOIs	https://doi.org/10.1111/j.1460-9568.2007.05467.x
Publication status	Published - Apr 2007

Keywords

dopamine
feeding
locomotion
neurodegeneration
snail
DOPAMINE-IMMUNOREACTIVE NEURONS
CENTRAL PATTERN GENERATOR
CENTRAL-NERVOUS-SYSTEM
ALPHA-SYNUCLEIN
RESPIRATORY BEHAVIOR
FEEDING SYSTEM
HELIX-POMATIA
EXPOSURE
RATS
6-HYDROXYDOPAMINE

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10.1111/j.1460-9568.2007.05467.x

Cite this

@article{46efda5fb30e42288c2a8a59bcdaeb5a,

title = "Behavioural and neural deficits induced by rotenone in the pond snail Lymnaea stagnalis. A possible model for Parkinson's disease in an invertebrate",

abstract = "Parkinson's disease is a neurodegenerative disorder, related to the loss of dopamine (DA)-containing neurons in the substantia nigra. In experimental animals, both vertebrates and invertebrates, rotenone, a commercially available organic pesticide, induces symptoms of Parkinson's disease. We found that that rotenone is toxic to the pond snail Lymnaea stagnalis (4-day LC50 0.8 mu M). Rotenone, at concentrations from 0.1 to 5 mu M, caused progressive and irreversible behavioural deficits in both acute and chronic exposure. Chronic exposure to 0.5 mu M rotenone led to a progressive decrease in spontaneous locomotion and in feeding, reaching almost 100% inhibition of both behaviours by the 7th day of rotenone treatment. In the central nervous system preparation made on the 7th day of treatment the postsynaptic potentials evoked by the identified dopaminergic RPeD1 neuron disappeared whereas the synaptic inputs received by the RPeD1 from a peptidergic neuron (VD4) were still functional. Immunostaining revealed that the tyrosine hydroxylase immunoreactivity decreased below the detectable level in both the RPeD1 cell body and its axonal processes. Finally, HPLC assay showed a significant (25%) decrease in DA level in the CNS by the 7th day of rotenone treatment. We conclude that, as in vertebrates, rotenone disrupts feeding and locomotion of the model mollusc Lymnaea stagnalis. One possible target of rotenone is the dopaminergic neurons in the CNS. We therefore suggest that Lymnaea stagnalis is a suitable invertebrate model for the study of Parkinson's disease, allowing direct analysis of the response of dopaminergic systems to rotenone at behavioural, cellular and neuronal levels.",

keywords = "dopamine, feeding, locomotion, neurodegeneration, snail, DOPAMINE-IMMUNOREACTIVE NEURONS, CENTRAL PATTERN GENERATOR, CENTRAL-NERVOUS-SYSTEM, ALPHA-SYNUCLEIN, RESPIRATORY BEHAVIOR, FEEDING SYSTEM, HELIX-POMATIA, EXPOSURE, RATS, 6-HYDROXYDOPAMINE",

author = "Agnes Vehovszky and Henriette Szabo and Laszlo Hiripi and Elliott, {Christopher J. H.} and Laszlo Hernadi",

year = "2007",

month = apr,

doi = "10.1111/j.1460-9568.2007.05467.x",

language = "English",

volume = "25",

pages = "2123--2130",

journal = "The European Journal of Neuroscience",

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TY - JOUR

T1 - Behavioural and neural deficits induced by rotenone in the pond snail Lymnaea stagnalis. A possible model for Parkinson's disease in an invertebrate

AU - Vehovszky, Agnes

AU - Szabo, Henriette

AU - Hiripi, Laszlo

AU - Elliott, Christopher J. H.

AU - Hernadi, Laszlo

PY - 2007/4

Y1 - 2007/4

N2 - Parkinson's disease is a neurodegenerative disorder, related to the loss of dopamine (DA)-containing neurons in the substantia nigra. In experimental animals, both vertebrates and invertebrates, rotenone, a commercially available organic pesticide, induces symptoms of Parkinson's disease. We found that that rotenone is toxic to the pond snail Lymnaea stagnalis (4-day LC50 0.8 mu M). Rotenone, at concentrations from 0.1 to 5 mu M, caused progressive and irreversible behavioural deficits in both acute and chronic exposure. Chronic exposure to 0.5 mu M rotenone led to a progressive decrease in spontaneous locomotion and in feeding, reaching almost 100% inhibition of both behaviours by the 7th day of rotenone treatment. In the central nervous system preparation made on the 7th day of treatment the postsynaptic potentials evoked by the identified dopaminergic RPeD1 neuron disappeared whereas the synaptic inputs received by the RPeD1 from a peptidergic neuron (VD4) were still functional. Immunostaining revealed that the tyrosine hydroxylase immunoreactivity decreased below the detectable level in both the RPeD1 cell body and its axonal processes. Finally, HPLC assay showed a significant (25%) decrease in DA level in the CNS by the 7th day of rotenone treatment. We conclude that, as in vertebrates, rotenone disrupts feeding and locomotion of the model mollusc Lymnaea stagnalis. One possible target of rotenone is the dopaminergic neurons in the CNS. We therefore suggest that Lymnaea stagnalis is a suitable invertebrate model for the study of Parkinson's disease, allowing direct analysis of the response of dopaminergic systems to rotenone at behavioural, cellular and neuronal levels.

AB - Parkinson's disease is a neurodegenerative disorder, related to the loss of dopamine (DA)-containing neurons in the substantia nigra. In experimental animals, both vertebrates and invertebrates, rotenone, a commercially available organic pesticide, induces symptoms of Parkinson's disease. We found that that rotenone is toxic to the pond snail Lymnaea stagnalis (4-day LC50 0.8 mu M). Rotenone, at concentrations from 0.1 to 5 mu M, caused progressive and irreversible behavioural deficits in both acute and chronic exposure. Chronic exposure to 0.5 mu M rotenone led to a progressive decrease in spontaneous locomotion and in feeding, reaching almost 100% inhibition of both behaviours by the 7th day of rotenone treatment. In the central nervous system preparation made on the 7th day of treatment the postsynaptic potentials evoked by the identified dopaminergic RPeD1 neuron disappeared whereas the synaptic inputs received by the RPeD1 from a peptidergic neuron (VD4) were still functional. Immunostaining revealed that the tyrosine hydroxylase immunoreactivity decreased below the detectable level in both the RPeD1 cell body and its axonal processes. Finally, HPLC assay showed a significant (25%) decrease in DA level in the CNS by the 7th day of rotenone treatment. We conclude that, as in vertebrates, rotenone disrupts feeding and locomotion of the model mollusc Lymnaea stagnalis. One possible target of rotenone is the dopaminergic neurons in the CNS. We therefore suggest that Lymnaea stagnalis is a suitable invertebrate model for the study of Parkinson's disease, allowing direct analysis of the response of dopaminergic systems to rotenone at behavioural, cellular and neuronal levels.

KW - dopamine

KW - feeding

KW - locomotion

KW - neurodegeneration

KW - snail

KW - DOPAMINE-IMMUNOREACTIVE NEURONS

KW - CENTRAL PATTERN GENERATOR

KW - CENTRAL-NERVOUS-SYSTEM

KW - ALPHA-SYNUCLEIN

KW - RESPIRATORY BEHAVIOR

KW - FEEDING SYSTEM

KW - HELIX-POMATIA

KW - EXPOSURE

KW - RATS

KW - 6-HYDROXYDOPAMINE

U2 - 10.1111/j.1460-9568.2007.05467.x

DO - 10.1111/j.1460-9568.2007.05467.x

M3 - Article

SN - 0953-816X

VL - 25

SP - 2123

EP - 2130

JO - The European Journal of Neuroscience

JF - The European Journal of Neuroscience

IS - 7

ER -