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Localization of ion-regulatory epithelia in embryos and hatchlings of two cephalopods

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Abstract

The tissue distribution and ontogeny of Na+/K+-ATPase has been examined as an indicator for ion-regulatory epithelia in whole animal sections of embryos and hatchlings of two cephalopod species: the squid Loligo vulgaris and the cuttlefish Sepia officinalis. This is the first report of the immunohistochemical localization of cephalopod Na+/K+-ATPase with the polyclonal antibody α (H-300) raised against the human α1-subunit of Na+/K+-ATPase. Na+/K+-ATPase immunoreactivity was observed in several tissues (gills, pancreatic appendages, nerves), exclusively located in baso-lateral membranes lining blood sinuses. Furthermore, large single cells in the gill of adult L. vulgaris specimens closely resembled Na+/K+-ATPase-rich cells described in fish. Immunohistochemical observations indicated that the amount and distribution of Na+/K+-ATPase in late cuttlefish embryos was similar to that found in juvenile and adult stages. The ion-regulatory epithelia (e.g., gills, excretory organs) of the squid embryos and paralarvae exhibited less differentiation than adults. Na+/K+-ATPase activities for whole animals were higher in hatchlings of S. officinalis (157.0 ± 32.4 µmol g FM −1  h−1) than in those of L. vulgaris (31.8 ± 3.3 µmol g FM −1  h−1). S. officinalis gills and pancreatic appendages achieved activities of 94.8 ± 18.5 and 421.8 ± 102.3 µmolATP g FM −1  h−1, respectively. High concentrations of Na+/K+-ATPase in late cephalopod embryos might be important in coping with the challenging abiotic conditions (low pH, high pCO2) that these organisms encounter inside their eggs. Our results also suggest a higher sensitivity of squid vs. cuttlefish embryos to environmental acid-base disturbances.

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Acknowledgements

The authors thank Prof. Dr. P. Saftig for providing the confocal microscope (Axiovert 200M) at the Unit of Molecular Cell Biology and Transgenic Research in Kiel and E. Grousset for valuable assistance with classic histology. We are grateful for the valuable suggestions of three anonymous reviewers and to Rainer Kiko for suggestions that improved the manuscript.

Author information

Correspondence to Marian Y. Hu.

Additional information

This study was partly funded by a DFG Excellence Cluster “Future Ocean” grant awarded to F.M. and the BMBF project BIOACID 3.1.3 awarded to F.M. and M.L.

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Hu, M.Y., Sucré, E., Charmantier-Daures, M. et al. Localization of ion-regulatory epithelia in embryos and hatchlings of two cephalopods. Cell Tissue Res 339, 571–583 (2010). https://doi.org/10.1007/s00441-009-0921-8

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Keywords

  • Gill
  • Ion-regulation
  • Pancreatic appendages
  • Loligo vulgaris
  • Sepia officinalis (Mollusca, Cephalopoda)