Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis

Pharmacological, behavioral, and ultrastructural studies

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16 Citations (Scopus)

Abstract

On the basis of the distribution of NADPH-diaphorase (NADPH-d) activity, we have previously suggested a role for nitric oxide (NO) in the development of Lymnaea stagnalis. In the present study, the long-term effects of NO donors (sodium nitroprusside, S-nitroso-N-acetyl-penicillamine) and nitric oxide synthase (NOS) inhibitors (nitro-L-arginine methyl-ester [L-NAME], NG-nitro-L-arginine [L-NOARG]) were tested on the survival, length of embryonic (intracapsular) life, locomotion (gliding), heartbeat activity and feeding behavior, as well as on the ultrastructure of the developing ganglia in the embryonic Lymnaea. No effect of any of the substances applied can be observed under 10-5 M concentration, whereas at 10-3 M concentration both kinds of treatment proved to be toxic. Between 10-5 M and 10-3 M concentrations the effects are reversible. At 10-4 M concentration, NO donors slightly increase the frequency of gliding and heartbeat of E70% embryos, and evoke a more than twofold enhancement of the feeding activity, i.e., the frequency of radula protrusions in the E90% embryonic stage. In contrast, NOS inhibitors at 10-4 M concentration strongly inhibit the locomotion and heartbeat of E70% embryos, and the feeding of E90% embryos. Under 10-3 M concentration, L-arginine diminishes the effect of NOARG, whereas the D-isomer of NAME has little or no significant effect. Neither type of treatment alters the course of gangliogenesis, and the light-microscopic appearance of neurons also remains unaffected. Ultrastructural analysis of the central nervous system of E90% embryos treated with 10-4 M NOS inhibitors revealed a significant reduction of the glycogen granule content and accumulation of lipid droplets in a number of the neuronal perikarya, as well as the occurrence of disintegrated mitochondria in axonal profiles. The effect of 10-4 M NO donors is mainly characterized by the increased number of lysosomes, disintegrated mitochondria and degenerating axonal profiles. The present findings suggest that NO is involved in the regulation of different behaviors and physiological functions, such as feeding activity, locomotion and heartbeat, during the embryonic development of Lymnaea. Changes observed in neuronal ultrastructure in ganglia seem to indicate NOergic regulatory processes at the central level.

Original languageEnglish
Pages (from-to)119-130
Number of pages12
JournalCell and Tissue Research
Volume310
Issue number1
DOIs
Publication statusPublished - 2002

Fingerprint

Lymnaea
Snails
Ponds
Embryonic Development
Nitric Oxide Donors
Nitric Oxide
Locomotion
Embryonic Structures
Nitric Oxide Synthase
Pharmacology
Mitochondria
Nitroarginine
Ganglia
NADPH Dehydrogenase
Arginine
Penicillamine
Poisons
NG-Nitroarginine Methyl Ester
Neurology
Nitroprusside

Keywords

  • Behavior
  • Embryonic development
  • Lymnaea stagnalis (Mollusca)
  • Nitric oxide
  • Ultrastructure

ASJC Scopus subject areas

  • Anatomy
  • Clinical Biochemistry
  • Cell Biology

Cite this

@article{541075095fdc46199cfee9ad8d44123d,
title = "Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis: Pharmacological, behavioral, and ultrastructural studies",
abstract = "On the basis of the distribution of NADPH-diaphorase (NADPH-d) activity, we have previously suggested a role for nitric oxide (NO) in the development of Lymnaea stagnalis. In the present study, the long-term effects of NO donors (sodium nitroprusside, S-nitroso-N-acetyl-penicillamine) and nitric oxide synthase (NOS) inhibitors (nitro-L-arginine methyl-ester [L-NAME], NG-nitro-L-arginine [L-NOARG]) were tested on the survival, length of embryonic (intracapsular) life, locomotion (gliding), heartbeat activity and feeding behavior, as well as on the ultrastructure of the developing ganglia in the embryonic Lymnaea. No effect of any of the substances applied can be observed under 10-5 M concentration, whereas at 10-3 M concentration both kinds of treatment proved to be toxic. Between 10-5 M and 10-3 M concentrations the effects are reversible. At 10-4 M concentration, NO donors slightly increase the frequency of gliding and heartbeat of E70{\%} embryos, and evoke a more than twofold enhancement of the feeding activity, i.e., the frequency of radula protrusions in the E90{\%} embryonic stage. In contrast, NOS inhibitors at 10-4 M concentration strongly inhibit the locomotion and heartbeat of E70{\%} embryos, and the feeding of E90{\%} embryos. Under 10-3 M concentration, L-arginine diminishes the effect of NOARG, whereas the D-isomer of NAME has little or no significant effect. Neither type of treatment alters the course of gangliogenesis, and the light-microscopic appearance of neurons also remains unaffected. Ultrastructural analysis of the central nervous system of E90{\%} embryos treated with 10-4 M NOS inhibitors revealed a significant reduction of the glycogen granule content and accumulation of lipid droplets in a number of the neuronal perikarya, as well as the occurrence of disintegrated mitochondria in axonal profiles. The effect of 10-4 M NO donors is mainly characterized by the increased number of lysosomes, disintegrated mitochondria and degenerating axonal profiles. The present findings suggest that NO is involved in the regulation of different behaviors and physiological functions, such as feeding activity, locomotion and heartbeat, during the embryonic development of Lymnaea. Changes observed in neuronal ultrastructure in ganglia seem to indicate NOergic regulatory processes at the central level.",
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author = "Z. Serfőző and K. Elekes",
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T1 - Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis

T2 - Pharmacological, behavioral, and ultrastructural studies

AU - Serfőző, Z.

AU - Elekes, K.

PY - 2002

Y1 - 2002

N2 - On the basis of the distribution of NADPH-diaphorase (NADPH-d) activity, we have previously suggested a role for nitric oxide (NO) in the development of Lymnaea stagnalis. In the present study, the long-term effects of NO donors (sodium nitroprusside, S-nitroso-N-acetyl-penicillamine) and nitric oxide synthase (NOS) inhibitors (nitro-L-arginine methyl-ester [L-NAME], NG-nitro-L-arginine [L-NOARG]) were tested on the survival, length of embryonic (intracapsular) life, locomotion (gliding), heartbeat activity and feeding behavior, as well as on the ultrastructure of the developing ganglia in the embryonic Lymnaea. No effect of any of the substances applied can be observed under 10-5 M concentration, whereas at 10-3 M concentration both kinds of treatment proved to be toxic. Between 10-5 M and 10-3 M concentrations the effects are reversible. At 10-4 M concentration, NO donors slightly increase the frequency of gliding and heartbeat of E70% embryos, and evoke a more than twofold enhancement of the feeding activity, i.e., the frequency of radula protrusions in the E90% embryonic stage. In contrast, NOS inhibitors at 10-4 M concentration strongly inhibit the locomotion and heartbeat of E70% embryos, and the feeding of E90% embryos. Under 10-3 M concentration, L-arginine diminishes the effect of NOARG, whereas the D-isomer of NAME has little or no significant effect. Neither type of treatment alters the course of gangliogenesis, and the light-microscopic appearance of neurons also remains unaffected. Ultrastructural analysis of the central nervous system of E90% embryos treated with 10-4 M NOS inhibitors revealed a significant reduction of the glycogen granule content and accumulation of lipid droplets in a number of the neuronal perikarya, as well as the occurrence of disintegrated mitochondria in axonal profiles. The effect of 10-4 M NO donors is mainly characterized by the increased number of lysosomes, disintegrated mitochondria and degenerating axonal profiles. The present findings suggest that NO is involved in the regulation of different behaviors and physiological functions, such as feeding activity, locomotion and heartbeat, during the embryonic development of Lymnaea. Changes observed in neuronal ultrastructure in ganglia seem to indicate NOergic regulatory processes at the central level.

AB - On the basis of the distribution of NADPH-diaphorase (NADPH-d) activity, we have previously suggested a role for nitric oxide (NO) in the development of Lymnaea stagnalis. In the present study, the long-term effects of NO donors (sodium nitroprusside, S-nitroso-N-acetyl-penicillamine) and nitric oxide synthase (NOS) inhibitors (nitro-L-arginine methyl-ester [L-NAME], NG-nitro-L-arginine [L-NOARG]) were tested on the survival, length of embryonic (intracapsular) life, locomotion (gliding), heartbeat activity and feeding behavior, as well as on the ultrastructure of the developing ganglia in the embryonic Lymnaea. No effect of any of the substances applied can be observed under 10-5 M concentration, whereas at 10-3 M concentration both kinds of treatment proved to be toxic. Between 10-5 M and 10-3 M concentrations the effects are reversible. At 10-4 M concentration, NO donors slightly increase the frequency of gliding and heartbeat of E70% embryos, and evoke a more than twofold enhancement of the feeding activity, i.e., the frequency of radula protrusions in the E90% embryonic stage. In contrast, NOS inhibitors at 10-4 M concentration strongly inhibit the locomotion and heartbeat of E70% embryos, and the feeding of E90% embryos. Under 10-3 M concentration, L-arginine diminishes the effect of NOARG, whereas the D-isomer of NAME has little or no significant effect. Neither type of treatment alters the course of gangliogenesis, and the light-microscopic appearance of neurons also remains unaffected. Ultrastructural analysis of the central nervous system of E90% embryos treated with 10-4 M NOS inhibitors revealed a significant reduction of the glycogen granule content and accumulation of lipid droplets in a number of the neuronal perikarya, as well as the occurrence of disintegrated mitochondria in axonal profiles. The effect of 10-4 M NO donors is mainly characterized by the increased number of lysosomes, disintegrated mitochondria and degenerating axonal profiles. The present findings suggest that NO is involved in the regulation of different behaviors and physiological functions, such as feeding activity, locomotion and heartbeat, during the embryonic development of Lymnaea. Changes observed in neuronal ultrastructure in ganglia seem to indicate NOergic regulatory processes at the central level.

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KW - Nitric oxide

KW - Ultrastructure

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