Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish

P. Laurent, C. M. Wood, Y. Wang, S. F. Perry, K. M. Gilmour, P. Part, C. Chevalier, M. West, P. J. Walsh

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Most teleost fish are ammoniotelic, and relatively few are ureotelic, in which the majority of nitrogenous waste is excreted as urea. This study aimed to determine whether the gill ultrastructure of ureotelic fish might have specific, unique characteristics compared with ammoniotelic fish. The gill morphology was studied in three closely related species of the family Batrachoididae: Opsanus beta, the gulf toadfish; Opsanus tau, the oyster toadfish; and Porichthys notatus, the plainfin midshipman, because prior studies have demonstrated that the two former species are ureotelic and excrete urea in unique, short daily pulses, whereas the latter is ammoniotelic. Ultrastructural studies demonstrated significant trafficking of dense-cored vesicles (50-200 nm) between the Golgi apparatus and the apical membrane of epithelial cells surrounding gill filaments and lamellae in these two Opsanus spp. The material constituting the core of these vesicles was intensely stained by lead salt and was unloaded externally when vesicles contacted the apical membrane. Another characteristic of these urea-secreting fish was the presence of numerous large, black-stained lysosomes, which contained cored vesicles, suggesting a second destination for the dense-cored vesicles. As a working hypothesis, the present data suggest that the urea-transporter protein, recently found in toadfish gills, is inserted in the vesicle. Subsequently, it could serve to either sequester cytosolic urea that ultimately is secreted into the water after contact of these vesicles with the pavement cell apical membrane, or it could allow facilitated diffusion of urea across the plasma membrane following insertion into the membrane. As further comparative evidence, the ammoniotelic P. notatus exhibited neither the vesicular trafficking nor the population of lysosomes both found in Opsanus spp.

Original languageEnglish
Pages (from-to)197-210
Number of pages14
JournalCell and Tissue Research
Volume303
Issue number2
DOIs
StatePublished - Mar 14 2001

Fingerprint

Batrachoidiformes
Fish
Urea
Fishes
Epithelium
Cell membranes
Membranes
Lysosomes
Pavements
Cell Membrane
Facilitated Diffusion
Ostreidae
Salts
Golgi Apparatus
Water
Epithelial Cells
Proteins

Keywords

  • Gill epithelium
  • Lysosome vesicle trafficking
  • Opsanus beta
  • Opsanus tau
  • Pavement cell
  • Porichthys notatus (Teleostei, Batrachoididae)
  • Ultrastructure

ASJC Scopus subject areas

  • Anatomy
  • Clinical Biochemistry
  • Cell Biology

Cite this

Laurent, P., Wood, C. M., Wang, Y., Perry, S. F., Gilmour, K. M., Part, P., ... Walsh, P. J. (2001). Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish. Cell and Tissue Research, 303(2), 197-210. https://doi.org/10.1007/s004410000312

Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish. / Laurent, P.; Wood, C. M.; Wang, Y.; Perry, S. F.; Gilmour, K. M.; Part, P.; Chevalier, C.; West, M.; Walsh, P. J.

In: Cell and Tissue Research, Vol. 303, No. 2, 14.03.2001, p. 197-210.

Research output: Contribution to journalArticle

Laurent, P, Wood, CM, Wang, Y, Perry, SF, Gilmour, KM, Part, P, Chevalier, C, West, M & Walsh, PJ 2001, 'Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish', Cell and Tissue Research, vol. 303, no. 2, pp. 197-210. https://doi.org/10.1007/s004410000312
Laurent P, Wood CM, Wang Y, Perry SF, Gilmour KM, Part P et al. Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish. Cell and Tissue Research. 2001 Mar 14;303(2):197-210. https://doi.org/10.1007/s004410000312
Laurent, P. ; Wood, C. M. ; Wang, Y. ; Perry, S. F. ; Gilmour, K. M. ; Part, P. ; Chevalier, C. ; West, M. ; Walsh, P. J. / Intracellular vesicular trafficking in the gill epithelium of urea-excreting fish. In: Cell and Tissue Research. 2001 ; Vol. 303, No. 2. pp. 197-210.
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