Unveiling TRPV1 spatio-temporal organization in live cell membranes

PloS One
Barbara StortiFabio Beltram

Abstract

Transient Receptor Potential Vanilloid 1 (TRPV1) is a non-selective cation channel that integrates several stimuli into nociception and neurogenic inflammation. Here we investigated the subtle TRPV1 interplay with candidate membrane partners in live cells by a combination of spatio-temporal fluctuation techniques and fluorescence resonance energy transfer (FRET) imaging. We show that TRPV1 is split into three populations with fairly different molecular properties: one binding to caveolin-1 and confined into caveolar structures, one actively guided by microtubules through selective binding, and one which diffuses freely and is not directly implicated in regulating receptor functionality. The emergence of caveolin-1 as a new interactor of TRPV1 evokes caveolar endocytosis as the main desensitization pathway of TRPV1 receptor, while microtubule binding agrees with previous data suggesting the receptor stabilization in functional form by these cytoskeletal components. Our results shed light on the hitherto unknown relationships between spatial organization and TRPV1 function in live-cell membranes.

References

Dec 1, 1989·The Journal of Cell Biology·J KartenbeckA Helenius
Jun 22, 2000·Proceedings of the National Academy of Sciences of the United States of America·S E JordtD Julius
Nov 15, 2001·Proceedings of the National Academy of Sciences of the United States of America·G SowaW C Sessa
Oct 12, 2002·Journal of Cell Science·Dorothy I MundyGeorge S Bloom
Mar 5, 2004·The Journal of Biological Chemistry·Narender R GavvaJames J S Treanor
May 7, 2004·European Journal of Biochemistry·Daniel N Cortright, Arpad Szallasi
Feb 17, 2005·Journal of Cell Science·Nicole HellwigMichael Schaefer
Feb 22, 2005·Current Opinion in Biotechnology·Herbert Schneckenburger
Oct 7, 2005·Microscopy Research and Technique·Jérôme N FeigeLaurent Gelman
Jun 28, 2006·The European Journal of Neuroscience·Min LiuJohn V Priestley
Dec 30, 2006·Nature Reviews. Neuroscience·John A AllenMark M Rasenick
Jan 11, 2007·Journal of Microscopy·S Bolte, F P Cordelières
Jun 9, 2007·Biochemical and Biophysical Research Communications·David Stepensky
Jun 19, 2007·Nature Methods·Ekaterina M MerzlyakDmitriy M Chudakov
Sep 4, 2007·Trends in Biochemical Sciences·David W Piston, Gert-Jan Kremers
May 21, 2008·Proceedings of the National Academy of Sciences of the United States of America·Vera Y Moiseenkova-BellTheodore G Wensel
Dec 5, 2008·American Journal of Physiology. Cell Physiology·Premanand C SundivakkamChinnaswamy Tiruppathi
Dec 9, 2008·Antioxidants & Redox Signaling·Hemal H Patel, Paul A Insel
Dec 11, 2008·Microscopy Research and Technique·Michelle A Digman, Enrico Gratton
Mar 4, 2009·Biophysical Journal·Jonas RiesPetra Schwille
Jul 31, 2009·Molecular Biology of the Cell·Lidiya OrlichenkoMark A McNiven
Sep 26, 2009·The Journal of Biological Chemistry·Sonia Gallego-SandínJavier García-Sancho
Nov 10, 2009·Proceedings of the National Academy of Sciences of the United States of America·Biswaranjan PaniIndu S Ambudkar
Mar 31, 2010·The Journal of Cell Biology·Amanda M MarchiandoJerrold R Turner
Sep 3, 2011·PloS One·Simone KöhlerAndreas R Bausch
Sep 16, 2011·Trends in Biochemical Sciences·Akihiro KusumiTakahiro K Fujiwara
Jan 21, 2012·The Journal of Biological Chemistry·Barbara StortiFabio Beltram
Apr 12, 2012·The Journal of Biological Chemistry·Lucía Sanz-SalvadorRosa Planells-Cases
Jul 10, 2013·Proceedings of the National Academy of Sciences of the United States of America·Carmine Di RienzoFrancesco Cardarelli
Apr 1, 2014·Current Neurovascular Research·Kenneth Maiese
Apr 30, 2014·British Journal of Pharmacology·Peter Holzer, Angelo A Izzo
Jun 26, 2014·Handbook of Experimental Pharmacology·Ute A Hellmich, Rachelle Gaudet

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Citations

Feb 18, 2016·Advances in Pharmacological Sciences·Gregory Smutzer, Roni K Devassy
Feb 18, 2016·Neural Plasticity·R Ramírez-BarrantesP Olivero
Nov 1, 2015·Biochimica Et Biophysica Acta·Maria Grazia CiardoAntonio Ferrer-Montiel
May 26, 2016·Biophysical Journal·David J RowlandJulie S Biteen
Jan 12, 2017·Biophysical Journal·Hermanus Johannes RuigrokYann Percherancier
Feb 8, 2020·International Journal of Molecular Sciences·Péter SánthaGábor Jancsó
May 8, 2020·Biological & Pharmaceutical Bulletin·Barbora MelkesJiri Novotny
Feb 26, 2019·Proceedings of the National Academy of Sciences of the United States of America·Quan TianJing Yao
Jul 23, 2016·Microscopy Research and Technique·Gerardo AbbandonatoRanieri Bizzarri
Jun 18, 2020·Scientific Reports·Masayoshi KawaseMakoto Kanzaki
Apr 4, 2021·International Journal of Molecular Sciences·Joanna K BujakPiotr Bednarczyk
May 1, 2021·International Journal of Molecular Sciences·Marina Ramal-SanchezBarbara Barboni
Aug 28, 2021·International Journal of Molecular Sciences·Yutaro KuwashimaYasushi Sako

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Methods Mentioned

BETA
Fluorescence
FRET
transfection
confocal microscopy

Software Mentioned

ImageJ
MatLab library
Image Correlation
STICS
Evrogen

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