Dopaminergic innervation and inhibition of ciliary movement in the ciliated epithelium of frog palatine mucosa

Maruyama, I; Yamamoto, Toshiharu; Ochi, Junzo; Nakai, Yasumitsu; Yamada, Shigeo

doi:10.1016/0014-2999(83)90553-8

Cited by 10 publications

(5 citation statements)

References 10 publications

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“…Although no immunohistochemical observation of a close localization between the DA/DA receptor and the basal body of cilia in organisms other than the present sea urchin embryos and larvae has been made to date, such sub-cellular localization and previously identified morphological and functional relationships may provide the morphological basis of DA involvement in the regulation of the beating of cilia through DA receptors (Catapane et al, 1979;Soliman, 1983b;Maruyama et al, 1983;Braubach et al, 2006;Martin et al, 2008).…”

Section: Morphological Basis Of the Preneural Dopaminergic System Formentioning

confidence: 88%

“…Thus, the decreased swimming activity of larvae treated with carbidopa is due to the decreased synthesis of DA. DA and serotonin have been thought to have counteracting functions in the beating of cilia and/or the regulation of swimming activity (Braubach et al, 2006;Martin et al, 2008), because DA was shown to suppress the beating of cilia in the gill of the mollusk Mytilus edulis (Catapane et al, 1979) as well as that in the palatine mucosa of frog (Maruyama et al, 1983). However, in sea urchin larvae (Soliman, 1983b), as well as in the motile cilia that line the foot of the mollusk Tritonia diomedea (Woodward and Willows, 2006), both serotonin and DA have been shown to stimulate the beating of cilia.…”

Section: Morphological Basis Of the Preneural Dopaminergic System Formentioning

confidence: 99%

“…The beating of cilia is known to be regulated by catecholamines, in particular dopamine (DA) in invertebrates (Soliman, 1983b;Voronezhskaya et al, 1999;Martin et al, 2008) and vertebrates (Maruyama et al, 1983;Tomé et al, 2007). To date, expression of catecholamines has been demonstrated in basic deuterostomes, including asteroidae (Huet and Fraquinet, 1981), brittlestars (De Bremaeker et al, 2000) and holothurian species (Inoue et al, 2002), but not in hemichordates.…”

Section: Introductionmentioning

confidence: 99%

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Development of a dopaminergic system in sea urchin embryos and larvae

Katow

Suyemitsu

Ooka

et al. 2010

Journal of Experimental Biology

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SUMMARYThe mechanisms that regulate the organized swimming movements of sea urchin blastulae are largely unknown. Using immunohistochemistry, we found that dopamine (DA) and the Hemicentrotus pulcherrimus homolog of the dopamine receptor D1 (Hp-DRD1) were strongly co-localized in 1-2m diameter granules (DA/DRD1 granules). Furthermore, these granules were arranged across the entire surface of blastulae as they developed locomotory cilia before hatching, and remained evident until metamorphosis. DA/DRD1 granules were associated with the basal bodies of cilia, and were densely packed in the ciliary band by the eight-arm pluteus stage. The transcription of Hp-DRD1 was detected from the unfertilized egg stage throughout the period of larval development. Treatment with S-(-)-carbidopa, an inhibitor of aromatic-L-amino acid decarboxylase, for 20-24h (i) from soon after insemination until the 20h post-fertilization (20hpf) early gastrula stage and (ii) from the 24hpf prism larva stage until the 48hpf pluteus stage, inhibited the formation of DA granules and decreased the swimming activity of blastulae and larvae in a dose-dependent manner. Exogenous DA rescued these deprivations. The formation of DRD1 granules was not affected. However, in 48hpf plutei, the serotonergic nervous system (5HT-NS) developed normally. Morpholino antisense oligonucleotides directed against Hp-DRD1 inhibited the formation of DRD1 granules and the swimming of larvae, but did not disturb the formation of DA granules. Thus, the formation of DRD1 granules and DA granules occurs chronologically closely but mechanically independently and the swimming of blastulae is regulated by the dopaminergic system. In plutei, the 5HT-NS closely surrounded the ciliary bands, suggesting the functional collaboration with the dopaminergic system in larvae. Supplementary material available online at

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Section: Morphological Basis Of the Preneural Dopaminergic System Formentioning

confidence: 88%

Section: Morphological Basis Of the Preneural Dopaminergic System Formentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Development of a dopaminergic system in sea urchin embryos and larvae

Katow

Suyemitsu

Ooka

et al. 2010

Journal of Experimental Biology

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“…We found, in addition to 5-HT (Aiello, 1990;Goldberg et al, 1994;Christopher et al, 1996;Christopher et al, 1999;Willows et al, 1997) and TPep-NLS (Willows et al, 1997;Popescu and Willows, 1999), that dopamine also produces significant increases in the CBF of CPE cells. All previous reports of dopamine action on cilia beating in molluscs (Catapane et al, 1978;Aiello, 1990), marine invertebrates (Wada et al, 1997) and even vertebrates (Maruyama et al, 1983) found that dopamine inhibits CBF, often acting in opposition to an excitatory 5-HT pathway (Catapane et al, 1978). Tritonia appears to be the first example where dopamine excites ciliary beating.…”

Section: Discussionmentioning

confidence: 94%

Dopamine modulation of Ca2+ dependent Cl- current regulates ciliary beat frequency controlling locomotion inTritonia diomedea

Woodward

Willows

2006

Journal of Experimental Biology

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SUMMARY The physiological mechanisms controlling ciliary beating remain largely unknown. Evidence exists supporting both hormonal control of ciliary beating and control via direct innervation. In the present study we investigated nervous control of cilia based locomotion in the nudibranch mollusc, Tritonia diomedea. Ciliated pedal epithelial (CPE) cells acting as locomotory effectors may be electrically excitable. To explore this possibility we characterized the cells' electrical properties, and found that CPE cells have large voltage dependent whole cell currents with two components. First, there is a fast activating outward Cl- current that is both voltage and Ca2+ influx dependent(ICl(Ca)). ICl(Ca) is sensitive to DIDS and 9-AC, and resembles currents of Ca2+-activated Cl- channels (CaCC). Ca2+ dependence also suggests the presence of voltage-gated Ca2+ channels; however, we were unable to detect these currents. The second current, a voltage dependent proton current(IH), activates very slowly and is sensitive to both Zn2+ and changes in pH. In addition we identify a new cilio-excitatory substance in Tritonia, viz., dopamine. Dopamine, in the 10 μmol l-1-1 mmol l-1 range, significantly increases ciliary beat frequency (CBF). We also found dopamine and Tritonia Pedal Peptide(TPep-NLS) selectively suppress ICl(Ca) in CPE cells,demonstrating a link between CBF excitation and ICl(Ca). It appears that dopamine and TPep-NLS inhibit ICl(Ca) not through changing [Ca2+]in, but directly by an unknown mechanism. Coupling of ICl(Ca) and CBF is further supported by our finding that DIDS and zero [Cl-]outboth increase CBF, mimicking dopamine and TPep-NLS excitation. These results suggest that dopamine and TPep-NLS act to inhibit ICl(Ca),initiating and prolonging Ca2+ influx, and activating CBF excitation.

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“…These observations suggest that the autonomic nervous system plays an important role in regulating ciliary movement. Recently, it was reported that cells containing elongated dopaminergic granules exist in the ciliated epithelium of frog palatine mucosae and play a role in suppressing ciliary movement [Maruyama et al, 1983]. We sup posed the possibility that ciliary movement is normally regulated by dopamine-containing cells as well as serotonin-containing cells when these cells receive each its specific exogenous stimulus.…”

Section: Discussionmentioning

confidence: 97%

Immunocytochemical Localization of Serotonin-Like Immunoreactivities in the Ciliated Epithelium of the Frog Palatine Mucosa

Maruyama

Shioda

Nakai

1984

Cells Tissues Organs

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Immunocytochemical localization of serotonin (5-HT)-like immunoreactivities was studies in the ciliated epithelium of the frog palatine mucosa by the peroxidase anti-peroxidase (PAP) method. 5-HT-like immunoreactivity was found only in the small granular vesicles (100–150 nm in diameter) and not in any mature large secretory granules or in other cell organellae in the goblet cells. No 5-HT-like immunoreactivities were found in any other epithelial and secretory cells in the palatine epithelium. It appears therefore that 5-HT-like immunoreactive granular vesicles have certain physiological effects on the ciliary movement of the ciliated cells or in the goblet cells.

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Dopaminergic innervation and inhibition of ciliary movement in the ciliated epithelium of frog palatine mucosa

Cited by 10 publications

References 10 publications

Development of a dopaminergic system in sea urchin embryos and larvae

Development of a dopaminergic system in sea urchin embryos and larvae

Dopamine modulation of Ca2+ dependent Cl- current regulates ciliary beat frequency controlling locomotion inTritonia diomedea

Immunocytochemical Localization of Serotonin-Like Immunoreactivities in the Ciliated Epithelium of the Frog Palatine Mucosa

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