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Myoinhibitory peptide regulates feeding in the marine annelid Platynereis.

Williams EA, Conzelmann M, Jékely G - Front. Zool. (2015)

Bottom Line: In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis.Our results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae.The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Developmental Biology, Spemannstrasse 35, Tübingen, 72076 Germany.

ABSTRACT

Background: During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown.

Results: Here, we explore the contribution of MIP to the regulation of feeding behavior in settled Platynereis postlarvae. We find that in addition to expression in the brain, MIP is expressed in the gut of developing larvae in sensory neurons that densely innervate the hindgut, the foregut, and the midgut. Activating MIP signaling by synthetic neuropeptide addition causes increased gut peristalsis and more frequent pharynx extensions leading to increased food intake. Conversely, morpholino-mediated knockdown of MIP expression inhibits feeding. In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis.

Conclusions: Our results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae. MIP is expressed in enteroendocrine cells of the digestive system suggesting that following larval settlement, feeding may be initiated by a direct sensory-neurosecretory mechanism. This is similar to the mechanism by which MIP induces larval settlement. The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.

No MeSH data available.


Related in: MedlinePlus

Co-staining of MIP and phalloidin in 1 month post fertilization (mpf)Platynereis.(A-K) Immunostaining of 1mpf Platynereis with an antibody raised against Platynereis MIP7 (red), counterstained with phalloidin. (A) Full body ventral view. White boxes indicate areas examined in cross-section in (B-D). Yellow arrowheads in (A-D) indicate cell bodies of MIP-expressing neurons. (B-D) Apical views of 10 μM cross-sections of the foregut (B), foregut-midgut boundary (C) and hindgut (D). (E) Ventral view of mid- and hindgut with ventral nerve cord region removed to expose digestive system. White box indicates area examined in cross-section in (F). Yellow arrowheads in (E-H, J) indicate cell bodies of MIP-expressing neurons in the midgut. Orange and purple arrowheads in (E, G, H) mark cell bodies of MIP-expressing neurons in the hindgut. (F) Apical view of 10 μM cross-section in the midgut. Dashed white line marks the boundary between the gut lumen and epithelial cell layer. (G, H) Lateral layers of (E) indicating the MIP-expressing cell bodies of the midgut and hindgut that sit in the gut epithelium, just underlying the gut musculature. (I-K) Close-up ventral view of the mid- and hindgut. (I) Phalloidin staining shows the circular and longitudinal smooth muscle fibres of the gut. (J) MIP immunostaining. (K) Overlay of MIP immunostaining and phalloidin staining. The axons of MIP-expressing neurons run parallel to the muscle fibres of the gut. Scale bars in (A, E, G-K): 50 μM, in (B-D, F): 20 μM. Abbreviations: fg, foregut; mg, midgut; hg, hindgut; VNC, ventral nerve cord; DIC, differential interference contrast; cm, circular muscle fibre; lm, longitudinal muscle fibre.
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Fig2: Co-staining of MIP and phalloidin in 1 month post fertilization (mpf)Platynereis.(A-K) Immunostaining of 1mpf Platynereis with an antibody raised against Platynereis MIP7 (red), counterstained with phalloidin. (A) Full body ventral view. White boxes indicate areas examined in cross-section in (B-D). Yellow arrowheads in (A-D) indicate cell bodies of MIP-expressing neurons. (B-D) Apical views of 10 μM cross-sections of the foregut (B), foregut-midgut boundary (C) and hindgut (D). (E) Ventral view of mid- and hindgut with ventral nerve cord region removed to expose digestive system. White box indicates area examined in cross-section in (F). Yellow arrowheads in (E-H, J) indicate cell bodies of MIP-expressing neurons in the midgut. Orange and purple arrowheads in (E, G, H) mark cell bodies of MIP-expressing neurons in the hindgut. (F) Apical view of 10 μM cross-section in the midgut. Dashed white line marks the boundary between the gut lumen and epithelial cell layer. (G, H) Lateral layers of (E) indicating the MIP-expressing cell bodies of the midgut and hindgut that sit in the gut epithelium, just underlying the gut musculature. (I-K) Close-up ventral view of the mid- and hindgut. (I) Phalloidin staining shows the circular and longitudinal smooth muscle fibres of the gut. (J) MIP immunostaining. (K) Overlay of MIP immunostaining and phalloidin staining. The axons of MIP-expressing neurons run parallel to the muscle fibres of the gut. Scale bars in (A, E, G-K): 50 μM, in (B-D, F): 20 μM. Abbreviations: fg, foregut; mg, midgut; hg, hindgut; VNC, ventral nerve cord; DIC, differential interference contrast; cm, circular muscle fibre; lm, longitudinal muscle fibre.

Mentions: By combining phalloidin staining and MIP immunostaining in Platynereis 1 month post fertilization (1 mpf), we could assess the location of MIP-expressing neurons in the gut in relation to the digestive system musculature. In the foregut and in the sphincter muscle that separates foregut from hindgut, MIP-expressing neurons are intermingled with the muscle tissue of the pharynx and sphincter (Figure 2A-C). In the mid- and hindgut, MIP-expressing neurons sit in the inner epithelial cell layer underlying the smooth muscles of the gut (Figure 2D-K). The axons of the MIP-expressing cells in the mid- and hind-gut of 1 month post fertilization (mpf) Platynereis run parallel to and just beneath the muscle fibers of both circular and longitudinal smooth muscles (Figure 2I-K). The spatial expression patterns of Platynereis MIP and MIP peptide suggest a potential role for MIP signaling in feeding and digestion during larval and early juvenile stages of the life cycle.Figure 2


Myoinhibitory peptide regulates feeding in the marine annelid Platynereis.

Williams EA, Conzelmann M, Jékely G - Front. Zool. (2015)

Co-staining of MIP and phalloidin in 1 month post fertilization (mpf)Platynereis.(A-K) Immunostaining of 1mpf Platynereis with an antibody raised against Platynereis MIP7 (red), counterstained with phalloidin. (A) Full body ventral view. White boxes indicate areas examined in cross-section in (B-D). Yellow arrowheads in (A-D) indicate cell bodies of MIP-expressing neurons. (B-D) Apical views of 10 μM cross-sections of the foregut (B), foregut-midgut boundary (C) and hindgut (D). (E) Ventral view of mid- and hindgut with ventral nerve cord region removed to expose digestive system. White box indicates area examined in cross-section in (F). Yellow arrowheads in (E-H, J) indicate cell bodies of MIP-expressing neurons in the midgut. Orange and purple arrowheads in (E, G, H) mark cell bodies of MIP-expressing neurons in the hindgut. (F) Apical view of 10 μM cross-section in the midgut. Dashed white line marks the boundary between the gut lumen and epithelial cell layer. (G, H) Lateral layers of (E) indicating the MIP-expressing cell bodies of the midgut and hindgut that sit in the gut epithelium, just underlying the gut musculature. (I-K) Close-up ventral view of the mid- and hindgut. (I) Phalloidin staining shows the circular and longitudinal smooth muscle fibres of the gut. (J) MIP immunostaining. (K) Overlay of MIP immunostaining and phalloidin staining. The axons of MIP-expressing neurons run parallel to the muscle fibres of the gut. Scale bars in (A, E, G-K): 50 μM, in (B-D, F): 20 μM. Abbreviations: fg, foregut; mg, midgut; hg, hindgut; VNC, ventral nerve cord; DIC, differential interference contrast; cm, circular muscle fibre; lm, longitudinal muscle fibre.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4307165&req=5

Fig2: Co-staining of MIP and phalloidin in 1 month post fertilization (mpf)Platynereis.(A-K) Immunostaining of 1mpf Platynereis with an antibody raised against Platynereis MIP7 (red), counterstained with phalloidin. (A) Full body ventral view. White boxes indicate areas examined in cross-section in (B-D). Yellow arrowheads in (A-D) indicate cell bodies of MIP-expressing neurons. (B-D) Apical views of 10 μM cross-sections of the foregut (B), foregut-midgut boundary (C) and hindgut (D). (E) Ventral view of mid- and hindgut with ventral nerve cord region removed to expose digestive system. White box indicates area examined in cross-section in (F). Yellow arrowheads in (E-H, J) indicate cell bodies of MIP-expressing neurons in the midgut. Orange and purple arrowheads in (E, G, H) mark cell bodies of MIP-expressing neurons in the hindgut. (F) Apical view of 10 μM cross-section in the midgut. Dashed white line marks the boundary between the gut lumen and epithelial cell layer. (G, H) Lateral layers of (E) indicating the MIP-expressing cell bodies of the midgut and hindgut that sit in the gut epithelium, just underlying the gut musculature. (I-K) Close-up ventral view of the mid- and hindgut. (I) Phalloidin staining shows the circular and longitudinal smooth muscle fibres of the gut. (J) MIP immunostaining. (K) Overlay of MIP immunostaining and phalloidin staining. The axons of MIP-expressing neurons run parallel to the muscle fibres of the gut. Scale bars in (A, E, G-K): 50 μM, in (B-D, F): 20 μM. Abbreviations: fg, foregut; mg, midgut; hg, hindgut; VNC, ventral nerve cord; DIC, differential interference contrast; cm, circular muscle fibre; lm, longitudinal muscle fibre.
Mentions: By combining phalloidin staining and MIP immunostaining in Platynereis 1 month post fertilization (1 mpf), we could assess the location of MIP-expressing neurons in the gut in relation to the digestive system musculature. In the foregut and in the sphincter muscle that separates foregut from hindgut, MIP-expressing neurons are intermingled with the muscle tissue of the pharynx and sphincter (Figure 2A-C). In the mid- and hindgut, MIP-expressing neurons sit in the inner epithelial cell layer underlying the smooth muscles of the gut (Figure 2D-K). The axons of the MIP-expressing cells in the mid- and hind-gut of 1 month post fertilization (mpf) Platynereis run parallel to and just beneath the muscle fibers of both circular and longitudinal smooth muscles (Figure 2I-K). The spatial expression patterns of Platynereis MIP and MIP peptide suggest a potential role for MIP signaling in feeding and digestion during larval and early juvenile stages of the life cycle.Figure 2

Bottom Line: In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis.Our results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae.The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute for Developmental Biology, Spemannstrasse 35, Tübingen, 72076 Germany.

ABSTRACT

Background: During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown.

Results: Here, we explore the contribution of MIP to the regulation of feeding behavior in settled Platynereis postlarvae. We find that in addition to expression in the brain, MIP is expressed in the gut of developing larvae in sensory neurons that densely innervate the hindgut, the foregut, and the midgut. Activating MIP signaling by synthetic neuropeptide addition causes increased gut peristalsis and more frequent pharynx extensions leading to increased food intake. Conversely, morpholino-mediated knockdown of MIP expression inhibits feeding. In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis.

Conclusions: Our results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae. MIP is expressed in enteroendocrine cells of the digestive system suggesting that following larval settlement, feeding may be initiated by a direct sensory-neurosecretory mechanism. This is similar to the mechanism by which MIP induces larval settlement. The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.

No MeSH data available.


Related in: MedlinePlus