RT Journal Article
T1 A Cftr-independent, Ano1-rich seawater-adaptive ionocyte in sea lamprey gills
A1 Shaughnessy, Ciaran A.
A1 Hall, Daniel J.
A1 Norstog, Jessica L.
A1 Barany Ruiz, André
A1 Regish, Amy M.
A1 Ferreira-Martins, Diogo
A1 Breves, Jason P.
A1 Komoroske, Lisa M.
A1 McCormick, Stephen D.
AB All ionoregulating marine fishes examined to date utilize seawater-type ionocytes expressing the apical Cl− channel, cystic fibrosis transmembrane conductance regulator (Cftr) to secrete Cl−. We performed transcriptomic, molecular and functional studies to identify Cl− transporters in the seawater-type ionocytes of sea lamprey (Petromyzon marinus). Gill cftr expression was minimal or undetectable in larvae and post-metamorphic juveniles. We identified other Cl− transporters highly expressed in the gills and/or upregulated following metamorphosis and further investigated two candidates that stood out in our analysis, a Ca2+-activated Cl− channel, anoctamin 1 (ano1), and the Clc chloride channel family member 2 (clcn2). Of these, ano1 was expressed 10–100 times more than clcn2 in the gills; moreover, ano1 was upregulated during seawater acclimation, while clcn2 was not. Using an antibody raised against sea lamprey Ano1, we did not detect Ano1 in the gills of larvae, found elevated levels in juveniles and observed a 4-fold increase in juveniles after seawater acclimation. Ano1 was localized to seawater-type branchial ionocytes but, surprisingly, was localized to the basolateral membrane. In vivo pharmacological inhibition experiments demonstrated that a DIDS-sensitive mechanism was critical to the maintenance of osmoregulatory homeostasis in seawater- but not freshwater-acclimated sea lamprey. Taken together, our results provide evidence of a Cftr-independent mechanism for branchial Cl− secretion in sea lamprey that leverages Ano1-expressing ionocytes. Once further characterized, the Cftr-independent, Ano1-rich ionocytes of sea lamprey could reveal novel strategies for branchial Cl− secretion, whether by Ano1 or some other Cl− transporter, not previously known in ionoregulating marine organisms.
PB The Company of Biologists
SN 0022-0949
YR 2025
FD 2025-04-02
LK https://hdl.handle.net/20.500.14352/119169
UL https://hdl.handle.net/20.500.14352/119169
LA eng
NO Shaughnessy, C. A., Hall, D. J., Norstog, J. L., Barany, A., Regish, A. M., Ferreira-Martins, D., Breves, J. P., Komoroske, L. M., & McCormick, S. D. (2024). A Cftr-independent, Ano1-rich seawater-adaptive ionocyte in sea lamprey gills. Journal of Experimental Biology, 228(7), jeb250110. https://doi.org/10.1242/jeb.250110
NO The authors thank A. Weinstock, S. Banerjee, Y. Yamaguchi, A. Daigle, H. Kerr, E. Walton and R. Pelis for their help in animal collection, experimentation, tissue sampling, molecular/bioinformatic analyses or interpretation of our data. Next-generation sequencing was facilitated by the Institute of Applied Life Sciences Core Facilities at the University of Massachusetts Amherst. The authors acknowledge resources and support from the Immunopathology Core, part of the Oklahoma State University Oklahoma Center for Respiratory and Infectious Diseases (OCRID), supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number P30GM149368.FootnotesAuthor contributionsConceptualization: C.A.S., S.D.M.; Data curation: C.A.S., D.J.H.; Formal analysis: C.A.S., D.J.H.; Funding acquisition: C.A.S., J.P.B., L.M.K., S.D.M.; Investigation: C.A.S., D.J.H., J.L.N., A.B., A.M.R., D.F.-M., J.P.B., S.D.M.; Methodology: C.A.S., D.J.H., J.L.N., A.B., A.M.R., D.F.-M., J.P.B., L.M.K., S.D.M.; Project administration: C.A.S., S.D.M.; Resources: J.P.B., L.M.K., S.D.M.; Software: C.A.S., D.J.H., L.M.K.; Supervision: C.A.S., L.M.K., S.D.M.; Validation: C.A.S., D.J.H., A.M.R., L.M.K., S.D.M.; Visualization: C.A.S.; Writing – original draft: C.A.S.; Writing - review & editing: C.A.S., D.J.H., J.L.N., A.B., A.M.R., D.F.-M., J.P.B., L.M.K., S.D.M.FundingThis work was funded by the Great Lakes Fishery Commission (2016-MCC-54056 to S.D.M.) and the National Science Foundation (DBI-2109626 to C.A.S., IOS-1755131 to J.P.B., and IOS-1558037 to S.D.M.). A.B. was supported by a Margarita Salas Postdoctoral Fellowship (Ministerio de Universidades). Open Access funding provided by Oklahoma State University. Deposited in PMC for immediate release.
NO Great Lakes Fishery Commission (Estados Unidos)
NO National Science Foundation (Estados Unidos)
NO Ministerio de Universidades (España)
NO Oklahoma Center for Respiratory and Infectious Diseases (Estados Unidos)
DS Docta Complutense
RD 22 ene 2026