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Pigment-dispersing hormone in Daphnia interneurons, one type homologous to insect clock neurons displaying circadian rhythmicity

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Abstract

We report identification of a beta-type pigment-dispersing hormone (PDH) identical in two water flea species, Daphnia magna and Daphnia pulex. It has been identified by cloning of precursors, chromatographic isolation from tissue extracts followed by immunoassays and de novo-mass spectrometric sequencing. The peptide is restricted to a complex system of distinct interneurons in the brain and visual ganglia, but does not occur in neurosecretory cells projecting to neurohemal organs as in decapod crustaceans. Thirteen neuron types individually identified and reconstructed by immunohistochemistry were almost identical in terms of positions and projection patterns in both species. Several neurons invade and form plexuses in visual ganglia and major brain neuropils including the central body. Five neuron types show contralateral pathways and form plexuses in the lateral, dorsal, or postlateral brain neuropils. Others are local interneurons, and a tritocerebral neuron connects the protocerebrum with the neuropil of the locomotory second antenna. Two visual ganglia neuron types lateral to the medulla closely resemble insect medulla lateral circadian clock neurons containing pigment-dispersing factor based upon positional and projectional criteria. Experiments under 12:12 h light/dark cycles and constant light or darkness conditions showed significant circadian changes in numbers and activities of one type of medulla lateral PDH neuron with an acrophase in the evening. This simple PDH system shows striking homologies to PDH systems in decapod crustaceans and well-known clock neurons in several insects, which suggests evolutionary conservation of an ancient peptidergic interneuronal system that is part of biological clocks.

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Abbreviations

a2n1 :

Second antenna nerve 1

BrOG:

Brain-optic ganglia complex

CCAP:

Crustacean cardioactive peptide

CEC:

Circumesophageal commissure

CHH:

Crustacean hyperglycemic hormone

CID:

Collision-induced dissociation

CB:

Central body

CN:

Central neuropil

CNS:

Central nervous system

CT:

Circadian time

DAPI:

4′,6′ Diamino-2-phenylindole-2 HCl

DD:

Constant darkness condition

DN:

Dorsal neuropil

DVM:

Diel vertical migration

ELISA:

Enzyme-linked immunosorbent assay

EPR:

Extra-retinal photoreceptor

EST:

Expressed sequence tag

HPLC:

High-pressure lipid chromatography

IEP:

Isoelectric point

IIF:

Indirect immunofluorescence

La:

Lamina

LD:

Light dark conditions

LL:

Constant light condition

l-LNvs:

Large ventral lateral neurons

LN:

Lateral neuropil

MALDI-TOF:

Matrix-assisted laser desorption/ionization-time of flight

Me:

Medulla

Mel:

Medulla lateral neurons

MLL:

Levator labri muscle

NE:

Nauplius eye

ORF:

Open-reading frame

PAP:

Peroxidase anti-peroxidase

PB:

Protocerebral bridge

PCN:

Precentral neuropil

PDF:

Pigment-dispersing factor

PDH:

Pigment-dispersing hormone

pec:

Post-esophageal commissure

PER:

Period gene product

PLN:

Postlateral neuropils

PPRP:

PDH-precursor-related peptide

RACE:

Rapid amplification of cDNA ends

RPCH:

Red pigment-concentrating hormone

RT:

Room temperature

RT-PCR:

Reverse transcription-polymerase chain reaction

s-LNvs:

Small lateral ventral neurons

SP:

Signal peptide

VNC:

Ventral nerve cord

ZT:

Zeitgeber time

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Acknowledgments

The Carl Tryggers Foundation, Stockholm, Sweden (to J.S. and H.D.), the Faculty of Sciences, Stockholm University (to H.D.), the Federal ministry for research and technology, Germany (BMFT, to Q.Z.), and postdoctoral research grants from the Fund for Scientific Research—Flanders, Belgium (F.W.O.-Vlaanderen, to P.V., J.H., K.P.), and the German Research Foundation (DFG to R.P.) are gratefully acknowledged by the authors. We are greatly indebted to Achim Stommel, State office for nature, environment, and customer protection, North-Rhine Westphalia (LaNUV), Bonn, Germany, for providing Daphnia magna and green algae stocks and many useful rearing advises. The authors also wish to thank Dr. S.G. Webster, University of North Wales, Bangor, UK for his generous gift of synthetic Uca-beta-PDH. The authors wish to thank our facility manager Dr. Stina Höglund, Wenner-Gren institute, Stockholm University, for technical help with confocal microscopy, and Dr. Anthony Poole, Department of Molecular Biology and Functional Genomics, Stockholm University, for help with final stylistical polishing of the text.

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Authors and Affiliations

  1. Department of Zoology, Stockholm University, Svante Arrhenius väg 18A, 10691, Stockholm, Sweden

    Johannes Strauß & Heinrich Dircksen

  2. Dr. Senckenbergische Anatomie, Institute of Anatomy II, J.-W. Goethe-University of Frankfurt, Frankfurt, Germany

    Qian Zhang

  3. Department of Biology, K. U. Leuven, Leuven, Belgium

    Peter Verleyen, Jurgen Huybrechts & Kevin Pauwels

  4. Institute of General Zoology and Animal Physiology, Friedrich-Schiller-University, Jena, Germany

    Susanne Neupert & Reinhard Predel

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  8. Heinrich Dircksen
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Correspondence to Heinrich Dircksen.

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Strauß, J., Zhang, Q., Verleyen, P. et al. Pigment-dispersing hormone in Daphnia interneurons, one type homologous to insect clock neurons displaying circadian rhythmicity. Cell. Mol. Life Sci. 68, 3403–3423 (2011). https://doi.org/10.1007/s00018-011-0636-3

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  • DOI: https://doi.org/10.1007/s00018-011-0636-3

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