Neuropeptides in flatworms

Gustafsson, Margaretha K. S.; Halton, D W; Kreshchenko, N. D.; Movsessian, S. O.; Raikova, Olga I.; Reuter, Maria; Теренина, Н. Б.

doi:10.1016/s0196-9781(02)00193-6

Cited by 44 publications

(29 citation statements)

References 35 publications

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“…Members of this family are present in all eumetazoans, and their mature peptides can have diverse functions in the regulation of neuronal circuits (31,37,(41)(42)(43)(44). Many Platynereis neuropeptides have close relatives in other lophotrochozoan species (mollusks and annelids) and some also outside the lophotrochozoans (RYa, RFa, and L11).…”

Section: Resultsmentioning

confidence: 99%

Neuropeptides regulate swimming depth of Platynereis larvae

Conzelmann

Offenburger

Asadulina

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

118

180

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Cilia-based locomotion is the major form of locomotion for microscopic planktonic organisms in the ocean. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. The neuronal bases of depth regulation in ciliary swimmers are unknown. To gain insights into depth regulation we studied ciliary locomotor control in the planktonic larva of the marine annelid, Platynereis. We found several neuropeptides expressed in distinct sensory neurons that innervate locomotor cilia. Neuropeptides altered ciliary beat frequency and the rate of calcium-evoked ciliary arrests. These changes influenced larval orientation, vertical swimming, and sinking, resulting in upward or downward shifts in the steady-state vertical distribution of larvae. Our findings indicate that Platynereis larvae have depth-regulating peptidergic neurons that directly translate sensory inputs into locomotor output on effector cilia. We propose that the simple circuitry found in these ciliated larvae represents an ancestral state in nervous system evolution.neural circuit | zooplankton | sensory-motor neuron | FMRFamide-related peptides T wo different types of locomotor systems are present in animals, one muscle based and the other cilia based. The neuronal control of muscle-based motor systems is well understood from studies on terrestrial model organisms. In contrast, our knowledge of the neuronal control of ciliary locomotion is limited, even though cilia-driven locomotion is prominent in the majority of animal phyla (1).Ciliary swimming in open water is widespread among the larval stages of marine invertebrates, including sponges, cnidarians, and many protostomes and deuterostomes (2-5). Freely swimming ciliated larvae often spend days to months as part of the zooplankton (1, 6). The primary axis for ciliated plankton is vertical, and body orientation is maintained either by passive (buoyancy) or active (gravitaxis, phototaxis) mechanisms. When cilia beat, larvae swim upward, and when cilia cease beating, the negatively buoyant larvae sink. During swimming, the thrust exerted on the body is proportional to the beating frequency of cilia (7-9). The alternation of active upward swimming and passive sinking, together with swimming speed and sinking rate, is thought to determine vertical distribution in the water (8). Because several environmental parameters, including water temperature, light intensity, and phytoplankton abundance, change with depth, swimming depth will influence the speed of larval development, the magnitude of UV damage, and the success of larval feeding and settlement. To stay at an appropriate depth, planktonic swimmers must therefore sense environmental cues and regulate ciliary beating.The ciliated larvae of the marine annelid Platynereis dumerilii provide an accessible model for the study of ciliary swimming in marine plankton (10). Platynereis can be cultured in the laboratory, and thousands of synchronously developing larvae can be obtained daily year-round (11). Platynereis ha...

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Section: Resultsmentioning

confidence: 99%

Neuropeptides regulate swimming depth of Platynereis larvae

Conzelmann

Offenburger

Asadulina

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

118

180

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“…General aspects of flatworm brain structure, including the shape of neurons and synapses, the distribution of histochemically detectable neuronal cell types, and the overall pattern of nerves connecting the brain to the periphery, have been described for a number of species (Lentz 1967;Keenan et al 1981;Shaw 1981;Halton et al 1992;Reuter and Gustafsson 1995;Gustafsson et al 2002). All flatworms possess a relatively compact anterior brain organized in a way that resembles a typical invertebrate ganglion.…”

Section: Introductionmentioning

confidence: 99%

Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile

et al. 2007

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We have analyzed brain structure in Macrostomum lignano, a representative of the basal platyhelminth taxon Macrostomida. Using confocal microscopy and digital 3D modeling software on specimens labeled with general markers for neurons (tyrTub), muscles (phalloidin), and nuclei (Sytox), an atlas and digital model of the juvenile Macrostomum brain was generated. The brain forms a ganglion with a central neuropile surrounded by a cortex of neuronal cell bodies. The neuropile contains a stereotypical array of compact axon bundles, as well as branched terminal axons and dendrites. Muscle fibers penetrate the flatworm brain horizontally and vertically at invariant positions. Beside the invariant pattern of neurite bundles, these "cerebral muscles" represent a convenient system of landmarks that help define discrete compartments in the juvenile brain. Commissural axon bundles define a dorsal and ventro-medial neuropile compartment, respectively. Longitudinal axons that enter the neuropile through an invariant set of anterior and posterior nerve roots define a ventro-basal and a central medial compartment in the neuropile. Flanking these "fibrous" compartments are neuropile domains that lack thick axon bundles and are composed of short collaterals and terminal arborizations of neurites. Two populations of neurons, visualized by antibodies against FMRFamide and serotonin, respectively, were mapped relative to compartment boundaries. This study will aid in the documentation and interpretation of patterns of gene expression, as well as functional studies, in the developing Macrostomum brain.

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“…This debate is mainly due to the fact that sufficient ultrastructural information has so far been lacking about the nervous system of the platyhelminths, especially of OV (Leksomboon et al, 2012a), in spite that there have been ample numbers of immuno-fluorescence microscopic studies of the peripheral and central nervous systems in the platyhelminths in which numerous neuron somata are clearly demonstrated in the immuno-light microscopy (Barton et al, 1993;Gustafsson et al, 2001Gustafsson et al, , 2002Leksomboon et al, 2012b). The lack thereof, seems to be understandable because it is technically impossible to examine at the electron microscopic level the immuno-labeled neurons.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, such knowledge may provide alternative drug targets for anthelminthics. The nervous system of the platyhelminths including the OV has been studied in immunofluorescence histochemistry at light microscopic levels with antibodies against several neurotransmitters and neuromodulators, whose functions are known to work largely in the motor nervous system (Gustafsson et al, 2001(Gustafsson et al, , 2002. However, there has so far, been neither ultrastructural knowledge of moter neurons of these parasites nor light and electron microscopic information of their peripheral sensory neurons (Leksomboon et al, 2012a).…”

Section: Introductionmentioning

confidence: 99%

Identification in Immuno-Electron Microscopy of Solitary Multi-Polar Peripheral Neurons of Adult Opisthorchis viverrini by Antibody Against Rat Diacylglycerol Kinaseζ

et al. 2016

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SUMMARY:By utilizing the antibody for rat DGKζ a substantial number of immunopositive cells were found in the OV (Opisthorchis viverrini). The immunopositive cells appeared solitarily and they were distributed rather symmetrically to the longitudinal axis of the OV. Some of them were located in close proximity to internal organs such as uterus, ovary, testes, vitelline glands and guts. The immunostained cells extended tapering processes horizontally or obliquely to the OV longitudinal axis. In immuno-electron microscopy, the immunopositive cells were characterized by intensely immunostained mitochondria and weakly immunostained cytoplasm and immunonegative chromatin-poor nucleus. Vacuoles of various sizes without the immunoreactivity were also contained in the cells. Thin cellular processes without the immunoreactivity were found to enclose thinly the entire surfaces of the immunostained cells and processes, and they were in continuity with the interstitial partition-like processes which contained nuclei and aggregation of microfibrils at some distance from the cytoplasmic envelopes. The present finding suggests the possibility that the immunostained cells were peripheral neurons enveloped by peripheral glia and that the glia are of mesenchymal origin because of their cytoplasmic continuity to the interstitial partition-like processes. The motor or sensory nature of the neurons remains to be elucidated.

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Neuropeptides in flatworms

Cited by 44 publications

References 35 publications

Neuropeptides regulate swimming depth of Platynereis larvae

Neuropeptides regulate swimming depth of Platynereis larvae

Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile

Identification in Immuno-Electron Microscopy of Solitary Multi-Polar Peripheral Neurons of Adult Opisthorchis viverrini by Antibody Against Rat Diacylglycerol Kinaseζ

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Neuropeptides in flatworms

Cited by 44 publications

References 35 publications

Neuropeptides regulate swimming depth of Platynereis larvae

Neuropeptides regulate swimming depth of Platynereis larvae

Neurobiology of the basal platyhelminth Macrostomum lignano: map and digital 3D model of the juvenile brain neuropile

Identification in Immuno-Electron Microscopy of Solitary Multi-Polar Peripheral Neurons of Adult Opisthorchis viverrini by Antibody Against Rat Diacylglycerol Kinase&#950;

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Identification in Immuno-Electron Microscopy of Solitary Multi-Polar Peripheral Neurons of Adult Opisthorchis viverrini by Antibody Against Rat Diacylglycerol Kinaseζ