Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii)

Kumi Hasegawa, Akira Kato, Taro Watanabe, Wataru Takagi, Michael F Romero, Justin D. Bell, Tes Toop, John A. Donald, Susumu Hyodo

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Most vertebrates, including cartilaginous fishes, maintain their plasma SO4 2- concentration ([SO4 2-]) within a narrow range of 0.2–1 mM. As seawater has a [SO4 2-] about 40 times higher than that of the plasma, SO4 2- excretion is the major role of kidneys in marine teleost fishes. It has been suggested that cartilaginous fishes also excrete excess SO4 2- via the kidney. However, little is known about the underlying mechanisms for SO4 2- transport in cartilaginous fish, largely due to the extraordinarily elaborate four-loop configuration of the nephron, which consists of at least 10 morphologically distinguishable segments. In the present study, we determined cDNA sequences from the kidney of holocephalan elephant fish (Callorhinchus milii) that encoded solute carrier family 26 member 1 (Slc26a1) and member 6 (Slc26a6), which are SO4 2- transporters that are expressed in mammalian and teleost kidneys. Elephant fish Slc26a1 (cmSlc26a1) and cmSlc26a6 mRNAs were coexpressed in the proximal II (PII) segment of the nephron, which comprises the second loop in the sinus zone. Functional analyses using Xenopus oocytes and the results of immunohistochemistry revealed that cmSlc26a1 is a basolaterally located electroneutral SO4 2- transporter, while cmSlc26a6 is an apically located, electrogenic Cl-/SO4 2- exchanger. In addition, we found that both cmSlc26a1 and cmSlc26a6 were abundantly expressed in the kidney of embryos; SO4 2- was concentrated in a bladder-like structure of elephant fish embryos. Our results demonstrated that the PII segment of the nephron contributes to the secretion of excess SO4 2- by the kidney of elephant fish. Possible mechanisms for SO4 2- secretion in the PII segment are discussed.

Original languageEnglish (US)
Pages (from-to)R66-R78
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume311
Issue number1
DOIs
StatePublished - Jul 1 2016

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Proximal Kidney Tubule
Sulfates
Fishes
Kidney
Nephrons
Embryonic Structures
Seawater
Xenopus
Oocytes
Vertebrates
Urinary Bladder
Complementary DNA
Immunohistochemistry
Messenger RNA

Keywords

  • Cartilaginous fish
  • Elephant fish
  • Kidney
  • Secretion
  • Sulfate transporter

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii). / Hasegawa, Kumi; Kato, Akira; Watanabe, Taro; Takagi, Wataru; Romero, Michael F; Bell, Justin D.; Toop, Tes; Donald, John A.; Hyodo, Susumu.

In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology, Vol. 311, No. 1, 01.07.2016, p. R66-R78.

Research output: Contribution to journalArticle

Hasegawa, Kumi ; Kato, Akira ; Watanabe, Taro ; Takagi, Wataru ; Romero, Michael F ; Bell, Justin D. ; Toop, Tes ; Donald, John A. ; Hyodo, Susumu. / Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii). In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 2016 ; Vol. 311, No. 1. pp. R66-R78.
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AU - Takagi, Wataru

AU - Romero, Michael F

AU - Bell, Justin D.

AU - Toop, Tes

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