ECB-ART-45083
Front Neurosci
2016 Dec 01;10:553. doi: 10.3389/fnins.2016.00553.
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Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens.
Mayorova TD, Tian S, Cai W, Semmens DC, Odekunle EA, Zandawala M, Badi Y, Rowe ML, Egertová M, Elphick MR.
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Neuropeptides are an ancient class of neuronal signaling molecules that regulate a variety of physiological and behavioral processes in animals. The life cycle of many animals includes a larval stage(s) that precedes metamorphic transition to a reproductively active adult stage but, with the exception of Drosophila melanogaster and other insects, research on neuropeptide signaling has hitherto largely focused on adult animals. However, recent advances in genome/transcriptome sequencing have facilitated investigation of neuropeptide expression/function in the larvae of protostomian (e.g., the annelid Platynereis dumerilii) and deuterostomian (e.g., the urochordate Ciona intestinalis) invertebrates. Accordingly, here we report the first multi-gene investigation of larval neuropeptide precursor expression in a species belonging to the phylum Echinodermata-the starfish Asterias rubens. Whole-mount mRNA in situ hybridization was used to visualize in bipinnaria and brachiolaria stage larvae the expression of eight neuropeptide precursors: L-type SALMFamide (S1), F-type SALMFamide (S2), vasopressin/oxytocin-type, NGFFYamide, thyrotropin-releasing hormone-type, gonadotropin-releasing hormone-type, calcitonin-type and corticotropin-releasing hormone-type. Expression of only three of the precursors (S1, S2, NGFFYamide) was observed in bipinnaria larvae but by the brachiolaria stage expression of all eight precursors was detected. An evolutionarily conserved feature of larval nervous systems is the apical organ and in starfish larvae this comprises the bilaterally symmetrical lateral ganglia, but only the S1 and S2 precursors were found to be expressed in these ganglia. A prominent feature of brachiolaria larvae is the attachment complex, comprising the brachia and adhesive disk, which mediates larval attachment to a substratum prior to metamorphosis. Interestingly, all of the neuropeptide precursors examined here are expressed in the attachment complex, with distinctive patterns of expression suggesting potential roles for neuropeptides in the attachment process. Lastly, expression of several neuropeptide precursors is associated with ciliary bands, suggesting potential roles for the neuropeptides derived from these precursors in control of larval locomotion and/or feeding. In conclusion, our findings provide novel perspectives on the evolution and development of neuropeptide signaling systems and neuroanatomical insights into neuropeptide function in echinoderm larvae.
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Species referenced: Echinodermata
Genes referenced: LOC115918707
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Figure 1. Schematic diagrams of the general anatomy of starfish (Asterias rubens) larvae (modified after, Murabe et al., 2008) (top half) and main neuronal aggregations of the nervous system (bottom half). In all diagrams anterior is uppermost with the overall body structure shown in yellow and the digestive system shown in orange. (A) bipinnaria larva; dorsal view. (B–D) brachiolaria larva. (B) dorsal view. (C) frontal (ventral) view. (D) left lateral view with ventral side on the left and dorsal on the right. (E) bipinnaria larva; dorsal view. (F) bipinnaria larva; ventral view. (G–I) brachiolaria larva. (G) dorsal view. (H) frontal (ventral) view. (I) left lateral view with ventral side on the left and dorsal on the right. The areas of main neuronal aggregations are highlighted in red in (E–I). The lateral ganglia start to develop at the bipinnaria stage and are located at the base of the anterior projection (solid black arrow labels the left lateral ganglion and dotted black arrow labels the right lateral ganglion; Moss et al., 1994; Elia et al., 2009). Neurons are also concentrated in several regions along ciliary bands, especially in the preoral ciliary band near the mouth (small black arrowhead; Moss et al., 1994; Byrne et al., 2007). In addition to these regions, the brachiolaria stage develops neuronal aggregations in the brachia tips (black arrowheads) and stems (white arrowheads), in the adhesive disk (double arrow), and in the basi-epithelial nerve plexus underlying the disk (white arrow; Barker, 1978; Murabe et al., 2008; Elia et al., 2009). a, anus; abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; m, mouth; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach. |
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Figure 2. Localization of L-type SALMFamide (S1) precursor transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A–E) bipinnaria larva; (F,G) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (A) dorsal view showing paired groups of 2–3 stained cells on the left (solid arrow) and right (dashed arrow) sides of the anterior projection. (B) detail of the anterior projection (boxed region in A) showing stained cells on the left and right sides (solid and dashed arrows, respectively). (C) left lateral view showing three stained cells at the base of the anterior projection (solid arrow). (D) detail of the anterior projection (boxed region in C) showing stained cells at the base of the anterior projection (solid arrows). (E) dorsal view of the anterior projection showing absence of staining in a larva incubated with sense probes. (F) left lateral view showing expression in solitary cells of the brachia (black and white arrowheads) and around the adhesive disk (white arrow), and in a group of tightly packed cells in the dorsal region of the larva (black solid arrow). (G) detail of the attachment complex, showing stained cells present in both the tip (black arrowheads) and the stem (white arrowheads) of a lateral brachium. In addition to a group of cells under the adhesive disk (white arrow), there are also scattered solitary stained cells (small black arrowheads) that appear to be located along the ciliary bands of the preoral lobe and a group of stained cells in the dorsal region of the larva (black solid arrows). Inset shows the attachment complex of a brachiolaria larva incubated with sense probe control. abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach; st, stem of brachium; t, tip of brachium. Scale bars: 200 μm (A,C,F, inset of G), 50 μm (B,D,E,G). |
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Figure 3. Localization of F-type SALMFamide (S2) precursor transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A–G) bipinnaria larva; (H,I) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (A) early bipinnaria, dorsal view showing stained cells on the left (solid arrow) and right (dashed arrow) sides of the anterior projection. (B) detail of the anterior projection (boxed region in A) showing stained cells on the left and right sides (solid and dashed arrows, respectively). (C) later bipinnaria, left lateral view showing two symmetrical groups of cells along the left (solid arrow) and right (dashed arrow) sides of anterior projection. (D) detail of the anterior projection (boxed region in C) showing stained cells on the left and right sides (solid and dashed arrows, respectively). (E) later bipinnaria, dorsal view showing stained cells along the margin of the anterior projection, with solid and dashed arrows highlighting cells on the left and right side, respectively. (F) detail of the anterior projection (boxed region in E) showing stained cells on the left and right sides (solid and dashed arrows, respectively). (G) left lateral view of anterior projection showing absence of staining in a larva incubated with sense probes. (H) left lateral view, showing expression in brachia (white arrowheads), near the adhesive disk (white arrow), and in a ganglion on the dorsal side (black arrow). Inset shows the attachment complex of a brachiolaria larva incubated with sense probe control. (I) detail of the attachment complex (boxed region in H), showing expression in separate cells along the brachium stems (white arrowheads) and arms (small black arrowhead). Groups of stained cells are located close to the adhesive disk (white arrows) and on the dorsal side (black arrow) of the larva. abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; lbr, lateral brachium; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A,C,E,H, inset of H), 100 μm (B,D,F,G,I). |
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Figure 4. Localization of asterotocin precursor transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A,B) bipinnaria larvae, showing no detectable expression of asterotocin precursor transcripts (A, left lateral view; B, frontal view). (C–E) brachiolaria larva. The schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (C) left lateral view, showing expression in the tips of the brachia (black arrowheads) and near the adhesive disk (white arrow). (D) detail of the attachment complex (boxed region in C) showing stained cells in the brachium tips (black arrowheads), the adhesive disk (double arrow), and adjacent to the adhesive disk (white arrow). (E) detail of the attachment complex showing absence of staining in a larva incubated with sense probes. abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; m, mouth; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A–C), 100 μm (D,E). |
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Figure 5. Localization of NGFFYamide precursor transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A–C) bipinnaria larva; (D–F) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (A) frontal view, showing solitary stained cells along the ciliary band of the preoral lobe (small arrowheads). (B) detail of the mouth region, showing expression in solitary cells (small arrowheads) along the ciliary bands of both preoral and postoral lobes. (C) detail of the mouth region showing absence of staining in a larva incubated with sense probes. (D) middle part of the body and the attachment complex, showing absence of staining with sense probes. (E) left lateral view, showing stained cells scattered throughout the larval body (small arrowheads) and under the adhesive disk (white arrows). (F) attachment complex and the middle part of the body, showing stained cells along the rims (small arrowheads) and under the adhesive disk (white arrows). abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; m, mouth; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach. Scale bars: 100 μm (A–D,F), 200 μm (E). |
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Figure 6. Localization of ArTRHP transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A) bipinnaria larva, frontal view showing no detectable expression of ArTRHP transcripts; (B–E) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (B) left lateral view, showing stained cells along the brachium stems (white arrowheads), near the adhesive disk (white arrows) and throughout the preoral lobe (small black arrowheads). (C) detail of a lateral brachium; note the presence of stained cells (white arrowheads) in the stem, but not in the tip of the brachium. (D) detail of the attachment complex; stained cells are present in the brachium stem (white arrowheads) and near the adhesive disk (white arrows). (E) attachment complex and the middle part of the body, showing no staining with sense probes. abr, anterior brachium; ad, adhesive disk; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; m, mouth; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A,B,E), 50 μm (C,D). |
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Figure 7. Localization of ArGnRHP transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A) bipinnaria larva, left lateral view, showing no detectable expression of ArGnRHP transcripts; (B–D) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (B) left lateral view, showing stained cells close to the adhesive disk (white arrow) (C) detail of the attachment complex (boxed region in B) showing two groups of stained cells near the adhesive disk (white arrows). (D) absence of staining in a brachiolaria larva incubated with sense probes. a, anus; abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; lbr, lateral brachium; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A,B,D), 100 μm (C). |
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Figure 8. Localization of ArCTP transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A) bipinnaria larva, frontal view, showing no detectable expression of ArCTP transcripts; (B–D) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (B) left lateral view, showing stained cells in the adhesive disk (double arrow) and adjacent to the adhesive disk (white arrows). (C) detail of the attachment complex; note stained cells within the adhesive disk (double arrows) and adjacent to it (white arrow). (D) absence of staining in a brachiolaria larva incubated with sense probes. abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; m, mouth; lbr, lateral brachium; pol, postoral lobe; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A,B,D), 100 μm (C). |
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Figure 9. Localization of ArCRHP transcripts in larvae of the starfish Asterias rubens using whole-mount in situ hybridization. (A) bipinnaria larva, frontal view, showing no detectable expression of ArCRHP transcripts; (B–D) brachiolaria larva; the schematic drawings illustrate the distribution of stained cells (see Figure 1 for labeling). (B) left lateral view, showing stained cells along the brachia (black and white arrowheads) and near the adhesive disk (white arrow). (C) detail of the attachment complex showing absence of staining in a larva incubated with sense probes. (D) detail of the attachment complex (boxed region in B) showing stained cells in tips (black arrowheads) and stems (white arrowheads) of brachia and close to the adhesive disk (white arrows). abr, anterior brachium; ad, adhesive disk; ap, anterior projection; ar, adult rudiment; ba, bipinnaria arms; e, esophagus; g, gut; m, mouth; lbr, lateral brachium; prl, preoral lobe; s, stomach; st, stem of a brachium; t, tip of a brachium. Scale bars: 200 μm (A,B), 100 μm (C,D). |
References [+] :
Barker,
DESCRIPTIONS OF THE LARVAE OF STICHASTER AUSTRALIS (VERRILL) AND COSCINASTERIAS CALAMARIA (GRAY) (ECHINODERMATA: ASTEROIDEA) FROM NEW ZEALAND, OBTAINED FROM LABORATORY CULTURE.
1978, Pubmed,
Echinobase
Barker, DESCRIPTIONS OF THE LARVAE OF STICHASTER AUSTRALIS (VERRILL) AND COSCINASTERIAS CALAMARIA (GRAY) (ECHINODERMATA: ASTEROIDEA) FROM NEW ZEALAND, OBTAINED FROM LABORATORY CULTURE. 1978, Pubmed , Echinobase
Barlow, Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abalone, Haliotis rufescens. 1992, Pubmed
Beer, Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris. 2001, Pubmed , Echinobase
Braubach, Neural control of the velum in larvae of the gastropod, Ilyanassa obsoleta. 2006, Pubmed
Burke, Development of the larval nervous system of the sand dollar, Dendraster excentricus. 1983, Pubmed , Echinobase
Burke, A genomic view of the sea urchin nervous system. 2006, Pubmed , Echinobase
Byrne, Development and distribution of the peptidergic system in larval and adult Patiriella: comparison of sea star bilateral and radial nervous systems. 2002, Pubmed , Echinobase
Byrne, Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. 2007, Pubmed , Echinobase
Byrne, Evolution of larval form in the sea star genus Patiriella: conservation and change in the larval nervous system. 2001, Pubmed , Echinobase
Byrne, Engrailed is expressed in larval development and in the radial nervous system of Patiriella sea stars. 2005, Pubmed , Echinobase
Conzelmann, Antibodies against conserved amidated neuropeptide epitopes enrich the comparative neurobiology toolbox. 2012, Pubmed
Conzelmann, Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. 2013, Pubmed
Conzelmann, Neuropeptides regulate swimming depth of Platynereis larvae. 2011, Pubmed
Croll, Early elements in gastropod neurogenesis. 1996, Pubmed
Cummins, Molecular analysis of two FMRFamide-encoding transcripts expressed during the development of the tropical abalone Haliotis asinina. 2011, Pubmed
Cummins, Expression of prohormone convertase 2 and the generation of neuropeptides in the developing nervous system of the gastropod Haliotis. 2009, Pubmed
Dehal, The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. 2002, Pubmed
Dickinson, Development of embryonic cells containing serotonin, catecholamines, and FMRFamide-related peptides in Aplysia californica. 2000, Pubmed
Dickinson, Development of the larval nervous system of the gastropod Ilyanassa obsoleta. 2003, Pubmed
Dyachuk, Development of the larval muscle system in the mussel Mytilus trossulus (Mollusca, Bivalvia). 2009, Pubmed
Elia, Nervous system development in feeding and nonfeeding asteroid larvae and the early juvenile. 2009, Pubmed , Echinobase
Elphick, SALMFamide salmagundi: the biology of a neuropeptide family in echinoderms. 2014, Pubmed , Echinobase
Elphick, Reconstructing SALMFamide Neuropeptide Precursor Evolution in the Phylum Echinodermata: Ophiuroid and Crinoid Sequence Data Provide New Insights. 2015, Pubmed , Echinobase
Elphick, The SALMFamides: a new family of neuropeptides isolated from an echinoderm. 1991, Pubmed , Echinobase
Erwin, The last common bilaterian ancestor. 2002, Pubmed
Furuya, Cockroach diuretic hormones: characterization of a calcitonin-like peptide in insects. 2000, Pubmed
Galliot, A two-step process in the emergence of neurogenesis. 2011, Pubmed
Gröger, Larval development in Cnidaria: a connection to Bilateria? 2001, Pubmed
Hamada, Expression of neuropeptide- and hormone-encoding genes in the Ciona intestinalis larval brain. 2011, Pubmed
Hewes, Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. 2001, Pubmed
Jékely, Global view of the evolution and diversity of metazoan neuropeptide signaling. 2013, Pubmed
Jones, Identification of a neuropeptide precursor protein that gives rise to a "cocktail" of peptides that bind Cu(II) and generate metal-linked dimers. 2016, Pubmed , Echinobase
Kataoka, Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta. 1989, Pubmed
Katsukura, Inhibition of metamorphosis by RFamide neuropeptides in planula larvae of Hydractinia echinata. 2003, Pubmed
Katsukura, Control of planula migration by LWamide and RFamide neuropeptides in Hydractinia echinata. 2004, Pubmed
Kempf, A simple neuronal system characterized by a monoclonal antibody to SCP neuropeptides in embryos and larvae of Tritonia diomedea (Gastropoda, Nudibranchia). 1987, Pubmed
Leitz, Metamorphosin A: a novel peptide controlling development of the lower metazoan Hydractinia echinata (Coelenterata, Hydrozoa). 1994, Pubmed
Marlow, Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. 2009, Pubmed
Mayorova, FMRF-amide immunoreactivity pattern in the planula and colony of the hydroid Gonothyraea loveni. 2013, Pubmed
Middleton, Modulation by cellular cholesterol of gene transcription via the cyclic AMP response element. 2001, Pubmed
Mirabeau, Molecular evolution of peptidergic signaling systems in bilaterians. 2013, Pubmed
Murabe, Neural architecture of the brachiolaria larva of the starfish, Asterina pectinifera. 2008, Pubmed , Echinobase
Murabe, Adhesive papillae on the brachiolar arms of brachiolaria larvae in two starfishes, Asterina pectinifera and Asterias amurensis, are sensors for metamorphic inducing factor(s). 2007, Pubmed , Echinobase
Murphy, Preferential expression of antioxidant response element mediated gene expression in astrocytes. 2001, Pubmed
Nakajima, Divergent patterns of neural development in larval echinoids and asteroids. 2004, Pubmed , Echinobase
Nässel, Drosophila neuropeptides in regulation of physiology and behavior. 2010, Pubmed
Nikitin, Bioinformatic prediction of Trichoplax adhaerens regulatory peptides. 2015, Pubmed
Oguro, Development and metamorphosis of the sea-star, Astropecten scoparius Valenciennes. 1976, Pubmed , Echinobase
Okon, Localisation of gonadotropin-releasing and thyrotropin-releasing hormones in human brain by radioimmunoassay. 1976, Pubmed
Perillo, Characterization of insulin-like peptides (ILPs) in the sea urchin Strongylocentrotus purpuratus: insights on the evolution of the insulin family. 2014, Pubmed , Echinobase
Piraino, Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria). 2011, Pubmed
Pisani, Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships. 2012, Pubmed , Echinobase
Rowe, The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus. 2012, Pubmed , Echinobase
Sawchenko, Corticotropin-releasing factor: co-expression within distinct subsets of oxytocin-, vasopressin-, and neurotensin-immunoreactive neurons in the hypothalamus of the male rat. 1984, Pubmed
Semmens, Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution. 2016, Pubmed , Echinobase
Semmens, Discovery of sea urchin NGFFFamide receptor unites a bilaterian neuropeptide family. 2015, Pubmed , Echinobase
Semmens, Discovery of a novel neurophysin-associated neuropeptide that triggers cardiac stomach contraction and retraction in starfish. 2013, Pubmed , Echinobase
Shifrin, Enterocyte microvillus-derived vesicles detoxify bacterial products and regulate epithelial-microbial interactions. 2012, Pubmed
Simakov, Hemichordate genomes and deuterostome origins. 2015, Pubmed , Echinobase
Sodergren, The genome of the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Sossin, Cellular and molecular biology of neuropeptide processing and packaging. 1989, Pubmed
Thisse, High-resolution in situ hybridization to whole-mount zebrafish embryos. 2008, Pubmed
Tian, Urbilaterian origin of paralogous GnRH and corazonin neuropeptide signalling pathways. 2016, Pubmed , Echinobase
Veenstra, Neurohormones and neuropeptides encoded by the genome of Lottia gigantea, with reference to other mollusks and insects. 2010, Pubmed
Veenstra, Neuropeptide evolution: neurohormones and neuropeptides predicted from the genomes of Capitella teleta and Helobdella robusta. 2011, Pubmed
Voronezhskaya, Adult-to-embryo chemical signaling in the regulation of larval development in trochophore animals: cellular and molecular mechanisms. 2008, Pubmed
Williams, Myoinhibitory peptide regulates feeding in the marine annelid Platynereis. 2015, Pubmed
Yu, Immunohistochemical analysis of ZnT1, 4, 5, 6, and 7 in the mouse gastrointestinal tract. 2007, Pubmed
Yuan, Embryonic development and metamorphosis of the scyphozoan Aurelia. 2008, Pubmed
Zhou, Proteolytic processing in the secretory pathway. 1999, Pubmed