The epithelial calcium channel TRPV5 is regulated differentially by klotho and sialidase

J Biol Chem. 2013 Oct 11;288(41):29238-46. doi: 10.1074/jbc.M113.473520. Epub 2013 Aug 22.

Abstract

The transient receptor potential vanilloid type 5 (TRPV5) Ca(2+) channel facilitates transcellular Ca(2+) transport in the distal convoluted tubule (DCT) of the kidney. The channel is glycosylated with a complex type N-glycan and it has been postulated that hydrolysis of the terminal sialic acid(s) stimulate TRPV5 activity. The present study delineates the role of the N-glycan in TRPV5 activity using biochemical assays in Human Embryonic Kidney 293 cells expressing TRPV5, isoelectric focusing and total internal reflection fluorescent microscopy. The anti-aging hormone klotho and other glycosidases stimulate TRPV5-dependent Ca(2+) uptake. Klotho was found to increase the plasma membrane stability of TRPV5, via the TRPV5 N-glycan. Sialidase mimicked this stimulatory action. However, this effect was independent of the N-glycosylation state of TRPV5, since the N-glycosylation mutant (TRPV5(N358Q)) was activated to the same extent. We showed that the increased TRPV5 activity after sialidase treatment is caused by inhibition of lipid raft-mediated internalization. In addition, sialidase modified the N-glycan of transferrin, a model glycoprotein, differently from klotho. Previous studies showed that after klotho treatment, galectin-1 binds the TRPV5 N-glycan and thereby increases TRPV5 activity. However, galectin-3, but not galectin-1, was expressed in the DCT. Furthermore, an increase in TRPV5-mediated Ca(2+) uptake was detected after galectin-3 treatment. In conclusion, two distinct TRPV5 stimulatory mechanisms were demonstrated; a klotho-mediated effect that is dependent on the N-glycan of TRPV5 and a sialidase-mediated stimulation that is lipid raft-dependent and independent of the N-glycan of TRPV5.

Keywords: Calcium; Calcium Channels; Calcium Transport; Glycosylation; Membrane Trafficking; trpv5.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Calcium / metabolism
  • Calcium Channels / genetics
  • Calcium Channels / metabolism
  • Calcium Channels / physiology*
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane / physiology*
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / physiology*
  • Galectin 3 / genetics
  • Galectin 3 / metabolism
  • Galectin 3 / pharmacology
  • Glucuronidase / genetics
  • Glucuronidase / pharmacology
  • Glycoside Hydrolases / genetics
  • Glycoside Hydrolases / pharmacology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HEK293 Cells
  • Humans
  • Klotho Proteins
  • Membrane Microdomains / drug effects
  • Membrane Microdomains / metabolism
  • Membrane Microdomains / physiology
  • Membrane Potentials / drug effects
  • Mice
  • Microscopy, Fluorescence
  • Neuraminidase / genetics
  • Neuraminidase / pharmacology
  • Patch-Clamp Techniques
  • Polysaccharides / metabolism
  • Recombinant Proteins / pharmacology
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism
  • TRPV Cation Channels / physiology*

Substances

  • Calcium Channels
  • Galectin 3
  • Polysaccharides
  • Recombinant Proteins
  • TRPV Cation Channels
  • TRPV5 protein, human
  • Green Fluorescent Proteins
  • Glycoside Hydrolases
  • Neuraminidase
  • Glucuronidase
  • Klotho Proteins
  • Calcium