Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii).
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.
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan; hase0421kumi@aori.u-tokyo.ac.jp.
Kumi
K
Hasegawa
Center for Biological Resources and Informatics and Department of Biological Sciences, Tokyo Institute of Technology, Yokohama, Japan; Departments of Physiology and Biomedical Engineering, Nephrology, and Hypertension, Mayo Clinic College of Medicine, Rochester, Minnesota;
Akira
A
Kato
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan;
Taro
T
Watanabe
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan; Evolutionary Morphology Laboratory, RIKEN Center for Life Science and Technologies, Kobe, Japan;
Wataru
W
Takagi
Departments of Physiology and Biomedical Engineering, Nephrology, and Hypertension, Mayo Clinic College of Medicine, Rochester, Minnesota;
Michael F
MF
Romero
School of Life and Environmental Sciences, Deakin University, Geelong, Australia; and Institute for Marine and Antarctic Studies, The University of Tasmania, Taroona, Australia.
Justin D
JD
Bell
School of Life and Environmental Sciences, Deakin University, Geelong, Australia; and.
Tes
T
Toop
School of Life and Environmental Sciences, Deakin University, Geelong, Australia; and.
John A
JA
Donald
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan;
Susumu
S
Hyodo
D000595:Amino Acid Sequence; D000818:Animals; D018076:DNA, Complementary / Q000235:genetics; D004555:Electric Fish / Q000378:metabolism*; D004625:Embryo, Nonmammalian / Q000378:metabolism; D029941:Fish Proteins / Q000378:metabolism; D007668:Kidney / Q000378:metabolism*; D007687:Kidney Tubules, Proximal / Q000378:metabolism*; D026901:Membrane Transport Proteins / Q000378:metabolism*; D009399:Nephrons / Q000378:metabolism; D009865:Oocytes / Q000378:metabolism; D013431:Sulfates / Q000378:metabolism*; D014018:Tissue Distribution; D014981:Xenopus
D018076:DNA, Complementary; D029941:Fish Proteins; D026901:Membrane Transport Proteins; D013431:Sulfates
cartilaginous fish; elephant fish; kidney; secretion; sulfate transporter