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Casein kinase-mediated phosphorylation of serine 839 is necessary for basolateral localization of the Ca2+-activated non-selective cation channel TRPM4

  • Ion channels, receptors and transporters
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Abstract

Transient receptor potential melastatin-like 4 (TRPM4) is a Ca2+-activated non-selective cation channel expressed in a wide range of human tissues. TRPM4 participates in a variety of physiological processes such as T cell activation, myogenic vasoconstriction, and allergic reactions. TRPM4 Ca2+ sensitivity is enhanced by calmodulin (CaM) and phosphathydilinositol 4, 5-bisphosphate (PI(4,5)P2) binding, as well as, under certain conditions, PKC activation. However, information as to the mechanisms of modulation of this channel remains unknown, including direct identification of phosphorylation sites on TRPM4 and their role in channel features. Here, we use mass-spectrometric-based proteomic approaches (immunoprecipitation and tandem mass spectrometry) to unambiguously identify S839 as a phosphorylation site present on human TRPM4 expressed in a human cell line. Site-directed mutagenesis employing a serine to alanine mutation to eliminate phosphorylation, and a phospho-mimetic aspartate mutation, as well as biochemical and immunocytochemical experiments, revealed a role for S839 phosphorylation in the basolateral expression of TRPM4 channels in epithelial cells. Moreover, we demonstrated that casein kinase 1 (CK1) phosphorylates S839 and is responsible for the basolateral localization of TRPM4.

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Abbreviations

TRPM4:

Transient receptor potential melastatin-like 4

PI(4,5)P2 :

Phosphatidylinositide 4, 5-bisphosphate

PKC:

Protein kinase C

LC-MS/MS:

Liquid chromatography coupled-tandem mass spectrometry

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Acknowledgments

We thank Dr. Pierre Launay for providing the pcDNA4/TO-hTRPM4. We also thank Dr. David Virshup for providing the 4HA-CKIε and 4HA-CKIε (K38R) plasmids (via Addgene, plasmids 13724, and 13725, respectively). We are grateful to Dr. Jon Sack and Ms. Ashleigh Evans for the discussion and critical comments to the manuscript. We also thank to Dr. Ricardo Armisén for constructive discussions and Ms. Heidi Pérez, Mr. Nicanor Villarroel and Mr. Francisco Alfaro for technical support. Mass spectrometry was performed at the University of California Davis Proteomics Facility. FONDECYT 11121239 to O.C., National Institutes of Health Grant NS42225 to J.S.T and FONDAP 15010006 to A.S. funded this research. FONDECYT 3120041 Postdoctoral Grant supported M.C. MECESUP UCH0301 Doctoral Fellowship supported E.L.S. and Conicyt Doctoral Fellowship funded A.R.

Author’s contributions

O.C., J.S.T., and A.S. designed research. O.C., M.C., K-S.P, E.L-S., and A.R. performed research. O.C., M.C., K-S.P, E.L-S, D.V., J.S.T, and A.S. analyzed data. O.C., J.S.T., and A.S. wrote the manuscript.

Conflict of interest

The authors declare no conflict of interests.

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Authors and Affiliations

  1. Programa de Biología Celular y Molecular, Facultad de Medicina, ICBM, Universidad de Chile, Independencia 1027, 8380453, Santiago, Chile

    Oscar Cerda, Mónica Cáceres & Aníbal Romero

  2. Centro de Estudios Moleculares de la Célula (CEMC), Facultad de Medicina, Universidad de Chile, Santiago, Chile

    Oscar Cerda, Elías Leiva-Salcedo, Diego Varela & Andrés Stutzin

  3. Department of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, CA, 95616, USA

    Oscar Cerda, Mónica Cáceres, Kang-Sik Park & James S. Trimmer

  4. Department of Physiology, Kyung Hee University School of Medicine, Seoul, South Korea, 130-701

    Kang-Sik Park

  5. Programa de Fisiopatología, Facultad de Medicina, ICBM, Universidad de Chile, Santiago, Chile

    Elías Leiva-Salcedo, Diego Varela & Andrés Stutzin

  6. Department of Physiology and Membrane Biology, School of Medicine, University of California, Davis, CA, 95616, USA

    James S. Trimmer

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  1. Oscar Cerda
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Correspondence to Oscar Cerda.

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James S. Trimmer and Andrés Stutzin contributed equally.

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Cerda, O., Cáceres, M., Park, KS. et al. Casein kinase-mediated phosphorylation of serine 839 is necessary for basolateral localization of the Ca2+-activated non-selective cation channel TRPM4. Pflugers Arch - Eur J Physiol 467, 1723–1732 (2015). https://doi.org/10.1007/s00424-014-1610-3

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