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Salinity-dependent expression of calcium-sensing receptors in Atlantic salmon (Salmo salar) tissues

Abstract

Multiple reports suggest that calcium-sensing receptors (CaSRs) are involved in calcium homeostasis, osmoregulation, and/or salinity sensing in fish (Loretz 2008, Herberger and Loretz 2013). We have isolated three unique full-length CaSR cDNAs from Atlantic salmon (Salmo salar) kidney that share many features with other reported CaSRs. Using anti-CaSR antibodies and PCR primers specific for individual salmon CaSR transcripts we show expression in osmoregulatory, neuroendocrine and sensory tissues. Furthermore, CaSRs are expressed in different patterns in salmon tissues where mRNA and protein expression are modified by freshwater or seawater acclimation. For example, in seawater, CaSR mRNA and protein expression is increased significantly in kidney as compared to freshwater. Electrophysiological recordings of olfactory responses produced upon exposure of salmon olfactory epithelium to CaSR agonists suggest a role for CaSRs in chemoreception in this species consistent with other freshwater, anadromous, and marine species where similar olfactory responses to divalent and polyvalent cations have been reported. These data provide further support for a role of CaSR proteins in osmoregulatory and sensory functions in Atlantic salmon, an anadromous species that experiences a broad range of environmental salinities in its life history.

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Abbreviations

ASW:

Artificial seawater

cAMP:

Cyclic adenosine monophosphate

CaSR:

Calcium-sensing receptor

cDNA:

Complimentary deoxyribonucleic acid

ECD:

Extracellular domain

FW:

Freshwater

GPCR:

G-protein coupled receptor

HupCaR:

Human parathyroid calcium-sensing receptor

ICD:

Intracellular domain

IP3 :

Inositol triphosphate

mRNA:

Messenger ribonucleic acid

RT-PCR:

Reverse transcriptase polymerase chain reaction

SalmoKCaR:

Salmon kidney calcium-sensing receptor

SKCaR:

Shark kidney calcium-sensing receptor

SW:

Seawater

UTR:

Untranslated region

ORF:

Open reading frame

CS:

Corpuscle of Stannius

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Acknowledgements

The authors wish to thank: A. Wisinski, K. Pigeon and C. Holm for excellent technical assistance. The authors are also grateful to Dr. T. Linley, D. Russell and T. Davis as well as Dr. E. M. Brown of Brigham and Women’s Hospital for helpful discussions. The paper has also been improved by comments from two anonymous reviewers.

Funding

This study was supported by funds from MariCal Inc. of Portland, ME.

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Correspondence to S. Jury.

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Conflict of interest

The authors declare they have no financial interests nor conflicts of interest to declare that are relevant to the content of this article. HW Harris has served as a paid expert technical witness for US and Norwegian patent litigations in 2019 and 2020, respectively, regarding the validity and enforcement of US and foreign issued patents granted to MariCal Inc. and licensed to STIM AS of Lofoten, Norway that disclose commercial technology based on the roles of CaSRs in anadromous fish. However, Harris has no direct or indirect financial interests in either MariCal or STIM.

Ethics approval

These studies followed the ethical guidelines from the American Fisheries Society Guidelines for Use of Fishes in Research (2004 and updated in 2014) (citation: Use of Fishes in Research Committee (joint committee of the American Fisheries Society, the American Institute of Fishery Research Biologists, and the American Society of Ichthyologists and Herpetologists). 2014. Guidelines for the use of fishes in research. American Fisheries Society, Bethesda, Maryland.)

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Jury, S., Betka, M., Nearing, J. et al. Salinity-dependent expression of calcium-sensing receptors in Atlantic salmon (Salmo salar) tissues. J Comp Physiol A 207, 505–522 (2021). https://doi.org/10.1007/s00359-021-01493-3

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Keywords

  • Calcium-sensing receptor
  • Olfaction
  • Atlantic salmon