Advertisement

Cell and Tissue Research

, Volume 348, Issue 1, pp 141–153 | Cite as

Morphological and functional characterization of a novel Na+/K+-ATPase-immunoreactive, follicle-like structure on the gill septum of Japanese banded houndshark, Triakis scyllium

  • Souichirou TakabeEmail author
  • Keitaro Teranishi
  • Shin Takaki
  • Makoto Kusakabe
  • Shigehisa Hirose
  • Toyoji Kaneko
  • Susumu Hyodo
Regular Article

Abstract

In teleost fishes, it is well-established that the gill serves as an important ionoregulatory organ in addition to its primary function of respiratory gas exchange. In elasmobranch fish, however, the ionoregulatory function of the gills is still poorly understood. Although mitochondria-rich (MR) cells have also been found in elasmobranch fish, these cells are considered to function primarily in acid-base regulation. In this study, we found a novel aggregate structure made up of cells with basolaterally-expressed Na+/K+-ATPase (NKA), in addition to NKA-immunoreactive MR cells that have already been described in the gill filament and lamella. The cell aggregates, named follicularly-arranged NKA-rich cells (follicular NRCs), were found exclusively in the epithelial lining of the venous web in the cavernous region of the filament and the inter-filamental space of the gill septum. The follicular NRCs form a single-layered follicular structure with a large lumen leading to the external environment. The follicular NRCs were characterized by: (i) well-developed microvilli on the apical membrane, (ii) less prominent infoldings of the basolateral membrane and (iii) typical junction structures including deep tight junction between cells. In addition, large numbers of vesicles were observed in the cytoplasm and some of them were fused to the lateral membrane. The follicular NRCs expressed Na+/H+ exchanger 3 and Ca2+ transporter 1. The follicular NRCs thus have the characteristics of absorptive ionoregulatory cells and this suggests that the elasmobranch gill probably contributes more importantly to body fluid homeostasis than previously thought.

Keywords

Elasmobranch Gill Na+/K+-ATPase rich cell Follicular structure Ion regulation 

Notes

Acknowledgements

We sincerely thank Prof. Christopher A Loretz of Univ. of Buffalo for critical reading of the manuscript and Dr. Soichi Watanabe of Univ. of Tokyo for his invaluable discussion and encouragement. This study was supported by Grants-in-Aid for Scientific Research to TK and SH.

References

  1. Bianco SD, Peng JB, Takanaga H, Suzuki Y, Crescenzi A et al (2007) Marked disturbance of calcium homeostasis in mice with targeted disruption of the Trpv6 calcium channel gene. J Bone Miner Res 22:274–285PubMedCrossRefGoogle Scholar
  2. Braissant O, Wahli W (1998) A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochem 1:10–16Google Scholar
  3. Burger JW (1965) Roles of the rectal gland and kidneys in salt and water excretion in the spiny dogfish. Physiol Zool 38:191–196Google Scholar
  4. Choe KP, Kato A, Hirose S, Plata C, Sindic A, Romero MF, Claiborne JB, Evans DH (2005) NHE3 in an ancestral vertebrate: primary sequence, distribution, localization, and function in gills. Am J Physiol Regul Integ Comp Physiol 289:R1520–R1534CrossRefGoogle Scholar
  5. Choe KP, Edwards SL, Claiborne JB, Evans DH (2007) The putative mechanism of Na+ absorption in euryhaline elasmobranchs exists in the gills of a stenohaline marine elasmobranch, Squalus acanthias. Comp Biochem Physiol A 146:155–162CrossRefGoogle Scholar
  6. Crespo S (1982) Surface morphology of dogfish (Scyliorhinus canicula) gill epithelium, and surface morphological changes following treatment with zinc sulphate: a scanning electron microscope study. Mar Biol 67:159–166CrossRefGoogle Scholar
  7. De Vries R, De Jager S (1984) The gill in the spiny dogfish, Squalus acanthia: respiratory and nonrespiratory function. Am J Ana 169:1–29CrossRefGoogle Scholar
  8. Evans DH, Piermarini PM, Potts WTW (1999) Ionic transport in the gill epithelium. J Exp Zool 283:641–652CrossRefGoogle Scholar
  9. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas excahange, osmoregulation, acid base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177PubMedCrossRefGoogle Scholar
  10. Hirata T, Kaneko T, Ono T, Nakazato T, Furukawa N, Hasegawa S, Wakabayashi S, Shigekawa M, Chang MH, Romero MF, Hirose S (2003) Mechanism of acid adaptation of fish living in a pH 3.5 lake. Am J Physiol Regul Integr Comp Physiol 284:R1199–R1212PubMedGoogle Scholar
  11. Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T (2008) Evidence for an apical Na-Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211:2584–2599PubMedCrossRefGoogle Scholar
  12. Hoenderop JG, Nilius B, Bindels RJ (2005) Calcium absorption across epithelia. Physiol Rev 85:373–422PubMedCrossRefGoogle Scholar
  13. Hwang PP, Lee TH (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A Mol Integr Physiol 148:479–497PubMedCrossRefGoogle Scholar
  14. Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47PubMedCrossRefGoogle Scholar
  15. Hyodo S, Katoh F, Kaneko T, Takei Y (2004) A facilitative urea transporter is localized in the renal collecting tubule of the dogfish Triakis scyllia. J Exp Biol 207:347–356PubMedCrossRefGoogle Scholar
  16. Kaneko T, Hasegawa S, Uchida K, Ogasawara T, Oyagi A, Hirano T (1999) Acid tolerance of Japanese dase (acyprinid teleost) in lake Osorezan, a remarkable acid lake. Zool Sci 16:871–877CrossRefGoogle Scholar
  17. Kaneko T, Watanabe S, Lee KM (2008) Functional morphology of mitochondrion-rich cells in euryhaline and stenohaline teleosts. Aqua BioSci Monogr 1:1–62Google Scholar
  18. Katoh F, Kaneko T (2003) Short-term transformation and longterm replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established ‘time-differential double fluorescent staining’ technique. J Exp Biol 206:4113–4123PubMedCrossRefGoogle Scholar
  19. Larsson D, Nemere I (2002) Vectorial transcellular calcium transport in intestine: integration of current models. J Biomed Biotech 2:117–119CrossRefGoogle Scholar
  20. Olson KR, Kent B (1980) The microvasculature of the elasmobranch gill. Cell Tissue Res 209:49–63PubMedCrossRefGoogle Scholar
  21. Piermarini PM, Evans DH (2000) Effects of environmental salinity on Na+/K+-ATPase in the gills and rectal gland of a euryhaline elasmobranch (Dasyatis sabina). J Exp Biol 203:2957–2966PubMedGoogle Scholar
  22. Piermarini PM, Verlander JW, Royaux IE, Evans DH (2002) Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol Regul Integr Comp Physio 283:R983–R992Google Scholar
  23. Riordan JR, Forbush B III, Hanrahan JW (1994) The molecular basis of chloride transport in shark rectal gland. J Exp Biol 196:405–418PubMedGoogle Scholar
  24. Shiraishi K, Kaneko T, Hasegawa S, Hirano T (1997) Development of multicellular complexes of chloride cells in the yolk-sac membrane of tilapia (Oreochromis mossambicus) embryos and larvae in seawater. Cell Tissue Res 288:583–590PubMedCrossRefGoogle Scholar
  25. Teranishi K, Kaneko T (2010) Spatial, cellular and intracellular localization of Na/K-ATPase in the sterically-disposed renal tubules of Japanese eel. J Histochem Cytochem 58:707–719PubMedCrossRefGoogle Scholar
  26. Tresguerres M, Katoh F, Fenton H, Jasinska E, Goss GG (2004) Regulation of branchial V-H+-ATPase Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J Exp Biol 208:345–354CrossRefGoogle Scholar
  27. Tresguerres M, Parks SK, Wood CM, Goss GG (2007) V-H + -ATPase translocation during blood alkalosis in dogfish gills: interaction with carbonic anhydrase and involvement in the postfeeding alkaline tide. Am J Physiol 292:R2012–R2019Google Scholar
  28. Ura K, Soyano K, Omoto N, Adachi S, Yamauchi K (1996) Localization of Na+, K + -ATPase in tissues of rabbit and teleosts using an antiserum directed against a partial sequence of the alpha-subunit. Zool Sci 13:219–227PubMedCrossRefGoogle Scholar
  29. Van de Graaf SF, Van der Kemp AW, Van den Berg D, Van Oorschot M, Hoenderop JG, Bindels RJ (2006) Identification of BSPRY as a novel auxiliary protein inhibiting TRPV5 activity. J Am Soc Nephrol 17:26–30PubMedCrossRefGoogle Scholar
  30. Wilson JM, Laurent P (2002) Fish gill morphology: inside out. J Exp Zool 293:192–213PubMedCrossRefGoogle Scholar
  31. Wilson JM, Morgan JD, Vogl AW, Randall DJ (2002) Branchial mitochondria-rich cells in the dogfish Squalus acanthias. Comp Biochem Physiol A 132:365–374CrossRefGoogle Scholar
  32. Wright DE (1973) The structure of the gills of the elasmobranch, Scyliorhinus canicula (L). Z Zellforsch 144:489–509PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Souichirou Takabe
    • 1
    • 2
    Email author
  • Keitaro Teranishi
    • 3
  • Shin Takaki
    • 1
  • Makoto Kusakabe
    • 1
  • Shigehisa Hirose
    • 4
  • Toyoji Kaneko
    • 3
  • Susumu Hyodo
    • 1
  1. 1.Laboratory of Physiology, Atmosphere and Ocean Research InstituteUniversity of TokyoTokyoJapan
  2. 2.KashiwaJapan
  3. 3.Department of Aquatic Bioscience, Graduate School of Agricultural and Life SciencesUniversity of TokyoTokyoJapan
  4. 4.Department of Biological SciencesTokyo Institute of TechnologyYokohamaJapan

Personalised recommendations