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Functional changes in the snail statocyst system elicited by microgravity.

Balaban PM, Malyshev AY, Ierusalimsky VN, Aseyev N, Korshunova TA, Bravarenko NI, Lemak MS, Roshchin M, Zakharov IS, Popova Y, Boyle R - PLoS ONE (2011)

Bottom Line: Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration.A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

View Article: PubMed Central - PubMed

Affiliation: Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia.

ABSTRACT

Background: The mollusk statocyst is a mechanosensing organ detecting the animal's orientation with respect to gravity. This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations.

Methodology/principal findings: In terrestrial gastropod snail we studied the impact of 16- (Foton M-2) and 12-day (Foton M-3) exposure to microgravity in unmanned orbital missions on: (i) the whole animal behavior (Helix lucorum L.), (ii) the statoreceptor responses to tilt in an isolated neural preparation (Helix lucorum L.), and (iii) the differential expression of the Helix pedal peptide (HPep) and the tetrapeptide FMRFamide genes in neural structures (Helix aspersa L.). Experiments were performed 13-42 hours after return to Earth. Latency of body re-orientation to sudden 90° head-down pitch was significantly reduced in postflight snails indicating an enhanced negative gravitaxis response. Statoreceptor responses to tilt in postflight snails were independent of motion direction, in contrast to a directional preference observed in control animals. Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration. A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.

Conclusions/significance: Upregulation of statocyst function in snails following microgravity exposure parallels that observed in vertebrates suggesting fundamental principles underlie gravi-sensing and the organism's ability to adapt to gravity changes. This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

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Localization of neurons expressing preproHPep gene in snail CNS and statocyst using in situ hybridization.Left panels (A, C, E, G) are images taken from control snails; right panels (B, D, F, I) are those taken from postflight snails. The staining in control and postflight snails was qualitatively similar in the CNS structures, but consistently different in the statocyst. A, B: cerebral ganglia; C, D: suboesophageal ganglia complex; E, F: pedal ganglia; G, I: statocysts. Note the labelled statocyst receptor cells in postflight snails in I (indicated by arrows) and lack of staining in control snails in G. H: for illustrative purposes the immunohistochemistry of HPep in a preflight snail shows the location of 3 receptors with respect to the statocyst nerve. Expression of this gene was observed only in these cells in all preparations. Calibration: A–F, 500 µm; G–I, 50 µm.
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pone-0017710-g005: Localization of neurons expressing preproHPep gene in snail CNS and statocyst using in situ hybridization.Left panels (A, C, E, G) are images taken from control snails; right panels (B, D, F, I) are those taken from postflight snails. The staining in control and postflight snails was qualitatively similar in the CNS structures, but consistently different in the statocyst. A, B: cerebral ganglia; C, D: suboesophageal ganglia complex; E, F: pedal ganglia; G, I: statocysts. Note the labelled statocyst receptor cells in postflight snails in I (indicated by arrows) and lack of staining in control snails in G. H: for illustrative purposes the immunohistochemistry of HPep in a preflight snail shows the location of 3 receptors with respect to the statocyst nerve. Expression of this gene was observed only in these cells in all preparations. Calibration: A–F, 500 µm; G–I, 50 µm.

Mentions: The expression pattern of the preproHPep gene was re-investigated in the postflight and control snails using ISH with mRNA following the Foton M-3 mission. The M-3 results qualitatively match those of the Foton M-2. Specifically stained cells were similarly observed in cerebral, subesophageal ganglia complex, and in pedal ganglia in all preparations. No systematic differences were observed between the postflight and control snails with respect to location and pattern of the stained ganglion neurons (Fig. 5, A–F). Once again a qualitative difference in staining of the statocyst neurons in postflight snails was observed (Fig. 5, G and I). In control animals (11 snails, 22 statocysts examined) the 3 specifically located neurons expressing preproHPep gene were found in 59% of cases, while in 16 postflight snails fixed 14 h after landing the expression was found in 96% of cases (Table 2). Since there are only 13 receptors in total in each statocyst, an up-regulation of gene expression in several of them represents possible changes in their function. This specific increase in gene expression in statocysts is indicative of the physiological load and may reflect the flight experience.


Functional changes in the snail statocyst system elicited by microgravity.

Balaban PM, Malyshev AY, Ierusalimsky VN, Aseyev N, Korshunova TA, Bravarenko NI, Lemak MS, Roshchin M, Zakharov IS, Popova Y, Boyle R - PLoS ONE (2011)

Localization of neurons expressing preproHPep gene in snail CNS and statocyst using in situ hybridization.Left panels (A, C, E, G) are images taken from control snails; right panels (B, D, F, I) are those taken from postflight snails. The staining in control and postflight snails was qualitatively similar in the CNS structures, but consistently different in the statocyst. A, B: cerebral ganglia; C, D: suboesophageal ganglia complex; E, F: pedal ganglia; G, I: statocysts. Note the labelled statocyst receptor cells in postflight snails in I (indicated by arrows) and lack of staining in control snails in G. H: for illustrative purposes the immunohistochemistry of HPep in a preflight snail shows the location of 3 receptors with respect to the statocyst nerve. Expression of this gene was observed only in these cells in all preparations. Calibration: A–F, 500 µm; G–I, 50 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3066201&req=5

pone-0017710-g005: Localization of neurons expressing preproHPep gene in snail CNS and statocyst using in situ hybridization.Left panels (A, C, E, G) are images taken from control snails; right panels (B, D, F, I) are those taken from postflight snails. The staining in control and postflight snails was qualitatively similar in the CNS structures, but consistently different in the statocyst. A, B: cerebral ganglia; C, D: suboesophageal ganglia complex; E, F: pedal ganglia; G, I: statocysts. Note the labelled statocyst receptor cells in postflight snails in I (indicated by arrows) and lack of staining in control snails in G. H: for illustrative purposes the immunohistochemistry of HPep in a preflight snail shows the location of 3 receptors with respect to the statocyst nerve. Expression of this gene was observed only in these cells in all preparations. Calibration: A–F, 500 µm; G–I, 50 µm.
Mentions: The expression pattern of the preproHPep gene was re-investigated in the postflight and control snails using ISH with mRNA following the Foton M-3 mission. The M-3 results qualitatively match those of the Foton M-2. Specifically stained cells were similarly observed in cerebral, subesophageal ganglia complex, and in pedal ganglia in all preparations. No systematic differences were observed between the postflight and control snails with respect to location and pattern of the stained ganglion neurons (Fig. 5, A–F). Once again a qualitative difference in staining of the statocyst neurons in postflight snails was observed (Fig. 5, G and I). In control animals (11 snails, 22 statocysts examined) the 3 specifically located neurons expressing preproHPep gene were found in 59% of cases, while in 16 postflight snails fixed 14 h after landing the expression was found in 96% of cases (Table 2). Since there are only 13 receptors in total in each statocyst, an up-regulation of gene expression in several of them represents possible changes in their function. This specific increase in gene expression in statocysts is indicative of the physiological load and may reflect the flight experience.

Bottom Line: Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration.A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

View Article: PubMed Central - PubMed

Affiliation: Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia.

ABSTRACT

Background: The mollusk statocyst is a mechanosensing organ detecting the animal's orientation with respect to gravity. This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations.

Methodology/principal findings: In terrestrial gastropod snail we studied the impact of 16- (Foton M-2) and 12-day (Foton M-3) exposure to microgravity in unmanned orbital missions on: (i) the whole animal behavior (Helix lucorum L.), (ii) the statoreceptor responses to tilt in an isolated neural preparation (Helix lucorum L.), and (iii) the differential expression of the Helix pedal peptide (HPep) and the tetrapeptide FMRFamide genes in neural structures (Helix aspersa L.). Experiments were performed 13-42 hours after return to Earth. Latency of body re-orientation to sudden 90° head-down pitch was significantly reduced in postflight snails indicating an enhanced negative gravitaxis response. Statoreceptor responses to tilt in postflight snails were independent of motion direction, in contrast to a directional preference observed in control animals. Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration. A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.

Conclusions/significance: Upregulation of statocyst function in snails following microgravity exposure parallels that observed in vertebrates suggesting fundamental principles underlie gravi-sensing and the organism's ability to adapt to gravity changes. This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

Show MeSH
Related in: MedlinePlus