Changes in dopamine uptake and developmental effects of dopamine receptor inactivation in the sea urchin

Carginale, Vincenzo; Borrelli, Lucia; Capasso, Antonio; Parisi, Elio

doi:10.1002/mrd.1080400315

Cited by 9 publications

(13 citation statements)

References 32 publications

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“…It also appears that, at least in some species, neurotransmitters may be required for egg cleavage (29,31). We now show that there are two embryologically unrelated cell types able to produce catecholamines in the mammalian ovary: neuronal cells located in the interstitial gland and oocytes.…”

Section: Discussionmentioning

confidence: 59%

“…In fact, the expression of neurotransmitters in ova and early embryos appears to be a highly conserved feature in evolution, as monoaminesincluding DA, NE, and serotonin-have been detected not only in fertilized eggs of vertebrates, such as teleosts, toads, and frogs (29), but also in invertebrates, such as molluscs, polychetes, and echinoderms (30). Studies in sea urchins demonstrated the ability of both unfertilized and fertilized eggs to take up DA and showed that the uptake is more prominent before fertilization (31). That the mammalian egg is also capable of incorporating and͞or synthesizing catecholamines was suggested by the earlier experiments of Burden and Lawrence (32), who, using a fluorescence method, detected catecholamine-like activity in rat ova, zygotes and 2-4 cell embryos.…”

Section: Discussionmentioning

confidence: 99%

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Oocytes are a source of catecholamines in the primate ovary: Evidence for a cell–cell regulatory loop

Mayerhofer

Smith

Danilchik

et al. 1998

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

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Catecholamines, thought to derive from the extrinsic innervation of the ovary, participate in the regulation of ovarian development and mature gonadal function. Recently, intraovarian neurons containing tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine biosynthesis, were described in the ovary of nonhuman primates. We now show that the primate ovary expresses both the genes encoding TH and dopamine ␤-hydroxylase (DBH), the key enzymes in norepinephrine (NE) biosynthesis. Ovarian neurons were identified as a site of TH and DBH gene expression, and surprisingly, oocytes were identified as an exclusive site of DBH synthesis. Oocytes contain neither TH mRNA nor protein, indicating that they are unable to synthesize dopamine (DA). They did, however, express a DA transporter gene identical to that found in human brain. The physiological relevance of this transporter system and DBH in oocytes was indicated by the ability of isolated oocytes to metabolize exogenous DA into NE. Isolated follicles containing oocytes-but not those from which the oocytes had been removed-responded to DA with an elevation in cAMP levels; this elevation was prevented by propranolol, a ␤-adrenoreceptor antagonist. The results suggest that oocytes and somatic cells are linked by a neuroendocrine loop consisting of NE synthesized in oocytes from actively transported DA and cAMP produced by somatic follicular cells in response to NE-induced ␤-adrenoreceptor activation.All three major catecholamines used as transmitters by sympathetic neurons of the peripheral nervous system are present in the mammalian ovary (1, 2). Among them, norepinephrine (NE) is the most abundant (1, 3, 4). A variety of experimental approaches have demonstrated that NE, recognized by specific receptors of the ␤ 2 -adrenergic subtype, stimulates ovarian steroidogenesis on its own and facilitates the stimulatory effect of gonadotropins on steroid production (5-7). NE also promotes follicular development (8-10). In contrast to this body of information, very little is known about the potential contribution(s) of dopamine (DA) to ovarian physiology. In one of the few studies on the subject (11), a stimulatory effect of DA on human granulosa cell steroidogenesis was blocked by propranolol, a ␤-adrenoreceptor antagonist, indicating that the effect of the catecholamine was indirect and most likely mediated by NE.It is commonly assumed that catecholamines reach the ovary exclusively via its extrinsic sympathetic innervation (12). However, ovarian denervation reduces, but does not eliminate, the content of NE in the gland (13), implying the existence of an additional source of catecholamine synthesis. That this source may be intrinsic to the ovary has been suggested by the identification of neuronal cell bodies containing immunoreactive tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine biosynthesis, in the ovary of nonhuman primates (14). Whether this is the only, or the more important, intragonadal source of catecholamines in the primate ...

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Section: Discussionmentioning

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Oocytes are a source of catecholamines in the primate ovary: Evidence for a cell–cell regulatory loop

Mayerhofer

Smith

Danilchik

et al. 1998

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

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“…This suggests that DA functions during early development in this species (Sea Urchin Genome Project, http://www.spbase.org/SpBase/search/anno_search_result.php). Despite previous biochemical observations that suggest a role for DA in sea urchin embryogenesis (Gustafson and Toneby, 1970;Toneby, 1980;Capasso et al, 1987;Carginale et al, 1995;AnitoleMisleh and Brown, 2004) and embryonic swimming activity (Soliman, 1983a), few morphological studies exist to support this. Therefore, in this study we investigated the localization of DA and its receptor Hp-DRD1, a D1 homolog found in the sea urchin species Hemicentrotus pulcherrimus (Suyemitsu, 2007) (Hp-DRD1; accession number AB510005, see supplementary material Fig.S1), from the pre-hatched blastula stage to metamorphosis using wholemount immunohistochemistry.…”

Section: Introductionmentioning

confidence: 92%

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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“…This function of acetylcholine is mediated by M-cholinoceptors located on the surfaces of the mature egg and linked with Ca 2+ channels [13,41,105]. Judging from resuits obtained in experiments on sea urchins and mollusks, fertilization and the blockade of polyspermy also involve biogenic monoamines [29,54,70,75].…”

Section: Pre-nervous Neurotransmitters As Mediators Of Regulatory Promentioning

confidence: 98%

“…In sea urchins, neurotransmitter receptors located on the cell surface are involved in regulating cytoplasmic calcium ion levels, in early intercellular interactions [5,26,86,88], and in controlling the transmembrane transport of biogenic monoamines [29] and various other membrane processes which occur immediately after fertilization [75]. Among these receptors, studies have identified, with varying levels of significance, serotonin receptors [4,5,23,26,86], cholinoceptors (muscarinic and nicotinic) [13,22,41], dopamine receptors [29], and adrenoceptors [75].…”

Section: Pre-nervous Neurotransmitters As Regulators Ofmentioning

confidence: 99%

Changes in the physiological roles of neurotransmitters during individual development

Buznikov

Shmukler

Lauder

1999

Neurosci Behav Physiol

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The classical neurotransmitters (acetylcholine and biogenic monoamines) are multifunctional substances involved in intra- and intercellular signaling at all stages of ontogenesis in multicellular animals. A cyclical scheme is proposed to describe age-related changes in neurotransmitter functions at different stages of development from oocyte maturation to neuron formation. This may reflect not only the temporospatial organization of neurotransmitter processes, but also the origin of the functions of acetylcholine and biogenic monoamines from the protosynapses of the cleaved embryo to neuronal synapses.

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Changes in dopamine uptake and developmental effects of dopamine receptor inactivation in the sea urchin

Cited by 9 publications

References 32 publications

Oocytes are a source of catecholamines in the primate ovary: Evidence for a cell–cell regulatory loop

Oocytes are a source of catecholamines in the primate ovary: Evidence for a cell–cell regulatory loop

Development of a dopaminergic system in sea urchin embryos and larvae

Changes in the physiological roles of neurotransmitters during individual development

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