TY - JOUR

T1 - Pigment dispersing factors and their cognate receptors in a crustacean model, with new insights into distinct neurons and their functions

AU - Alexander, Jodi

AU - Wilcockson, David

AU - Brendler-Spaeth, Timothy

AU - Oliphant, Andrew

AU - Dircksen, Heinrich

AU - Webster, Simon

N1 - Copyright © 2020 Alexander, Oliphant, Wilcockson, Brendler-Spaeth, Dircksen and Webster.

PY - 2020/10/29

Y1 - 2020/10/29

N2 - Pigment dispersing factors (PDFs, or PDHs in crustaceans) form a structurallyrelated group of neuropeptides found throughout the Ecdysozoa and were firstdiscovered as pigmentary effector hormones in crustaceans. In insects PDFs fulfill crucial neuromodulatory roles, most notably as output regulators of the circadian system, underscoring their central position in physiological and behavioral organization of arthropods. Intriguingly, decapod crustaceans express multiple isoforms of PDH originating from separate genes, yet their differential functions are still to be determined. Here, we functionally define two PDH receptors in the crab Carcinus maenas and show them to be selectively activated by four PDH isoforms: PDHR 43673 was activated byPDH-1 and PDH-2 at low nanomolar doses whilst PDHR 41189 was activated by PDH-3and an extended 20 residue e-PDH. Detailed examination of the anatomical distribution of all four peptides and their cognate receptors indicate that they likely perform different functions as secreted hormones and/or neuromodulators, with PDH-1 and its receptor 43673 implicated in an authentic hormonal axis. PDH-2, PDH-3, and e-PDH were limited to non-neurohemal interneuronal sites in the CNS; PDHR 41189 was largely restricted to the nervous system suggesting a neuromodulatory function. Notably PDH-3 and e-PDH were without chromatophore dispersing activity. This is the first report which functionally defines a PDHR in an endocrine system in a crustacean and to indicate this and other putative roles of this physiologically pivotal peptide group in these organisms. Thus, our findings present opportunities to further examine the endocrine and circadian machinery in this important arthropod phylum.

AB - Pigment dispersing factors (PDFs, or PDHs in crustaceans) form a structurallyrelated group of neuropeptides found throughout the Ecdysozoa and were firstdiscovered as pigmentary effector hormones in crustaceans. In insects PDFs fulfill crucial neuromodulatory roles, most notably as output regulators of the circadian system, underscoring their central position in physiological and behavioral organization of arthropods. Intriguingly, decapod crustaceans express multiple isoforms of PDH originating from separate genes, yet their differential functions are still to be determined. Here, we functionally define two PDH receptors in the crab Carcinus maenas and show them to be selectively activated by four PDH isoforms: PDHR 43673 was activated byPDH-1 and PDH-2 at low nanomolar doses whilst PDHR 41189 was activated by PDH-3and an extended 20 residue e-PDH. Detailed examination of the anatomical distribution of all four peptides and their cognate receptors indicate that they likely perform different functions as secreted hormones and/or neuromodulators, with PDH-1 and its receptor 43673 implicated in an authentic hormonal axis. PDH-2, PDH-3, and e-PDH were limited to non-neurohemal interneuronal sites in the CNS; PDHR 41189 was largely restricted to the nervous system suggesting a neuromodulatory function. Notably PDH-3 and e-PDH were without chromatophore dispersing activity. This is the first report which functionally defines a PDHR in an endocrine system in a crustacean and to indicate this and other putative roles of this physiologically pivotal peptide group in these organisms. Thus, our findings present opportunities to further examine the endocrine and circadian machinery in this important arthropod phylum.

KW - Pigment dispersing hormone, G protein-coupled receptor deorphaning, neuroanatomy, gene expression, functions

U2 - 10.3389/fnins.2020.595648

DO - 10.3389/fnins.2020.595648

M3 - Article

C2 - 33192283

VL - 14

SP - 1

EP - 16

JO - Frontiers in Neuroscience

JF - Frontiers in Neuroscience

SN - 1662-453X

M1 - 595648

ER -