Hormonal control of the crustacean molting gland: Insights from transcriptomics and proteomics

Mykles, Donald L.; Chang, Ernest S.

doi:10.1016/j.ygcen.2020.113493

Cited by 57 publications

(80 citation statements)

References 135 publications

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“…Static factors, such as dILP8, prothoracicostatic peptides, Bommo-myosuppressin, and FMRFamide-related peptide, inhibit ecdysteroidogenesis (97,98,105). By contrast, the neuropeptides MIH and CHH are the only known ligands identified for YOs in crustaceans (2,50,55,189,190). Transcriptomic analysis has revealed that the YO expresses receptors for ILPs, growth factors, biogenic amines, and neuropeptides (Tables 2, 3) (25,29).…”

Section: Conclusion and Future Researchmentioning

confidence: 99%

“…In the intermolt stage (stage C 4 ), inhibitory neuropeptides produced in the X-organ/ sinus gland complex, such as molt-inhibiting hormone (MIH) and crustacean hyperglycemic hormone (CHH), maintain the YO in the basal state (Figure 1). A proposed model for MIH signaling couples a cAMP/Ca 2+ -dependent triggering phase with a NO/cGMP-dependent summation phase [reviewed in (2)]. The prolonged activation of a calmodulin-dependent NO synthase and NO-dependent guanylyl cyclase (GC-I) represses ecdysteroidogenesis between MIH pulses (2,(6)(7)(8)(9).…”

Section: Introductionmentioning

confidence: 99%

“…A proposed model for MIH signaling couples a cAMP/Ca 2+ -dependent triggering phase with a NO/cGMP-dependent summation phase [reviewed in (2)]. The prolonged activation of a calmodulin-dependent NO synthase and NO-dependent guanylyl cyclase (GC-I) represses ecdysteroidogenesis between MIH pulses (2,(6)(7)(8)(9). The decision to molt, or enter premolt, is determined by integration of environmental and physiological cues by the central nervous system that are not completely understood (10).…”

Section: Introductionmentioning

confidence: 99%

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Signaling Pathways That Regulate the Crustacean Molting Gland

Mykles

2021

Front. Endocrinol.

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A pair of Y-organs (YOs) are the molting glands of decapod crustaceans. They synthesize and secrete steroid molting hormones (ecdysteroids) and their activity is controlled by external and internal signals. The YO transitions through four physiological states over the molt cycle, which are mediated by molt-inhibiting hormone (MIH; basal state), mechanistic Target of Rapamycin Complex 1 (mTORC1; activated state), Transforming Growth Factor-β (TGFβ)/Activin (committed state), and ecdysteroid (repressed state) signaling pathways. MIH, produced in the eyestalk X-organ/sinus gland complex, inhibits the synthesis of ecdysteroids. A model for MIH signaling is organized into a cAMP/Ca2+-dependent triggering phase and a nitric oxide/cGMP-dependent summation phase, which maintains the YO in the basal state during intermolt. A reduction in MIH release triggers YO activation, which requires mTORC1-dependent protein synthesis, followed by mTORC1-dependent gene expression. TGFβ/Activin signaling is required for YO commitment in mid-premolt. The YO transcriptome has 878 unique contigs assigned to 23 KEGG signaling pathways, 478 of which are differentially expressed over the molt cycle. Ninety-nine contigs encode G protein-coupled receptors (GPCRs), 65 of which bind a variety of neuropeptides and biogenic amines. Among these are putative receptors for MIH/crustacean hyperglycemic hormone neuropeptides, corazonin, relaxin, serotonin, octopamine, dopamine, allatostatins, Bursicon, ecdysis-triggering hormone (ETH), CCHamide, FMRFamide, and proctolin. Contigs encoding receptor tyrosine kinase insulin-like receptor, epidermal growth factor (EGF) receptor, and fibroblast growth factor (FGF) receptor and ligands EGF and FGF suggest that the YO is positively regulated by insulin-like peptides and growth factors. Future research should focus on the interactions of signaling pathways that integrate physiological status with environmental cues for molt control.

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Section: Conclusion and Future Researchmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Signaling Pathways That Regulate the Crustacean Molting Gland

Mykles

2021

Front. Endocrinol.

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“…Alternatively, a model hypothesizing that the MIH receptor is a G protein-coupled receptor (GPCR) was proposed ( 230 ) based on data obtained mainly from the crab Gecarcinus lateralis ( 240 – 243 ). In combination with previous related studies ( 230 , 243 ) and the transcriptomic analysis, the G. lateralis Y-organ was proposed to go through a four-stage transition (basal, activated, committed, and repressed stages) from inter-molt (stage C 4 ), early pre-molt (stage D 0 ), middle pre-molt (stage D 1 , D 2 ) and late pre-molt stage (stage D 4 ), respectively ( 244 , 245 ). The MIH signaling pathway plays a dominant role in the inter-molt and early pre-molt stage to suppress ecdysteroid production.…”

Section: Peptide Structure Signal Transduction Pathways and Receptomentioning

confidence: 99%

“…Advancements in the functional front are expected if more research efforts are to be made. A persuasive example is a sophisticated model for the regulation of steroidogenesis in the Y-organ built mainly based upon functional genomics data [see ( 245 )]. Additional genetic resources enjoyed by the study of insects, especially those working in the fruit fly D. melanogaster , as exemplified by a study of ITP ( 174 ), would probably render a faster development for the study of insect member peptides.…”

Section: Conclusion and Prospective Developmentsmentioning

confidence: 99%

The Crustacean Hyperglycemic Hormone Superfamily: Progress Made in the Past Decade

2020

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Early studies recognizing the importance of the decapod eyestalk in the endocrine regulation of crustacean physiology—molting, metabolism, reproduction, osmotic balance, etc.—helped found the field of crustacean endocrinology. Characterization of putative factors in the eyestalk using distinct functional bioassays ultimately led to the discovery of a group of structurally related and functionally diverse neuropeptides, crustacean hyperglycemic hormone (CHH), molt-inhibiting hormone (MIH), gonad-inhibiting hormone (GIH) or vitellogenesis-inhibiting hormone (VIH), and mandibular organ-inhibiting hormone (MOIH). These peptides, along with the first insect member (ion transport peptide, ITP), constitute the original arthropod members of the crustacean hyperglycemic hormone (CHH) superfamily. The presence of genes encoding the CHH-superfamily peptides across representative ecdysozoan taxa has been established. The objective of this review is to, aside from providing a general framework, highlight the progress made during the past decade or so. The progress includes the widespread identification of the CHH-superfamily peptides, in particular in non-crustaceans, which has reshaped the phylogenetic profile of the superfamily. Novel functions have been attributed to some of the newly identified members, providing exceptional opportunities for understanding the structure-function relationships of these peptides. Functional studies are challenging, especially for the peptides of crustacean and insect species, where they are widely expressed in various tissues and usually pleiotropic. Progress has been made in deciphering the roles of CHH, ITP, and their alternatively spliced counterparts (CHH-L, ITP-L) in the regulation of metabolism and ionic/osmotic hemostasis under (eco)physiological, developmental, or pathological contexts, and of MIH in the stimulation of ovarian maturation, which implicates it as a regulator for coordinating growth (molt) and reproduction. In addition, experimental elucidation of the steric structure and structure-function relationships have given better understanding of the structural basis of the functional diversification and overlapping among these peptides. Finally, an important finding was the first-ever identification of the receptors for this superfamily of peptides, specifically the receptors for ITPs of the silkworm, which will surely give great impetus to the functional study of these peptides for years to come. Studies regarding recent progress are presented and synthesized, and prospective developments remarked upon.

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Biological insights into the rapid tissue regeneration of freshwater crayfish and crustaceans

Feleke

Bennett

Chen

et al. 2021

Cell Biochemistry & Function

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The freshwater crayfish is capable of regenerating limbs, following autotomy, injury and predation. In arthropod species, regeneration and moulting are two processes linked and strongly regulated by ecdysone. The regeneration of crayfish limbs is divided into wound healing, blastema formation, cellular reprogramming and tissue patterning. Limb blastema cells undergo proliferation, dedifferentiation and redifferentiation. A limb bud, containing folded segments of the regenerating limb, is encased within a cuticular sheath. The functional limb regenerates, in proecdysis, in two to three consecutive moults. Rapid tissue growth is regulated by hormones, limb nerves and local cells. The TGF‐β/activin signalling pathway has been determined in the crayfish, P. fallax f. virginalis, and is suggested as a potential regulator of tissue regeneration. In this review article, we discuss current understanding of tissue regeneration in the crayfish and various crustaceans. A thorough understanding of the cellular, genetic and molecular pathways of these biological processes is promising for the development of therapeutic applications for a wide array of diseases in regenerative medicine.

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Hormonal control of the crustacean molting gland: Insights from transcriptomics and proteomics

Cited by 57 publications

References 135 publications

Signaling Pathways That Regulate the Crustacean Molting Gland

Signaling Pathways That Regulate the Crustacean Molting Gland

The Crustacean Hyperglycemic Hormone Superfamily: Progress Made in the Past Decade

Biological insights into the rapid tissue regeneration of freshwater crayfish and crustaceans

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