VAMP7 Regulates Constitutive Membrane Incorporation of the Cold-activated Channel TRPM8

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Feb 5

PMID 26843440

Citations 25

Authors

Debapriya Ghosh

Silvia Pinto

Lydia Danglot

Ine Vandewauw

Andrei Segal

Nele Van Ranst

Melissa Benoit

Annelies Janssens

Rudi Vennekens

Pieter Vanden Berghe

Thierry Galli

Joris Vriens

Thomas Voets

Affiliations

Soon will be listed here.

Abstract

The cation channel TRPM8 plays a central role in the somatosensory system, as a key sensor of innocuously cold temperatures and cooling agents. Although increased functional expression of TRPM8 has been implicated in various forms of pathological cold hypersensitivity, little is known about the cellular and molecular mechanisms that determine TRPM8 abundance at the plasma membrane. Here we demonstrate constitutive transport of TRPM8 towards the plasma membrane in atypical, non-acidic transport vesicles that contain lysosomal-associated membrane protein 1 (LAMP1), and provide evidence that vesicle-associated membrane protein 7 (VAMP7) mediates fusion of these vesicles with the plasma membrane. In line herewith, VAMP7-deficient mice exhibit reduced functional expression of TRPM8 in sensory neurons and concomitant deficits in cold avoidance and icilin-induced cold hypersensitivity. Our results uncover a cellular pathway that controls functional plasma membrane incorporation of a temperature-sensitive TRP channel, and thus regulates thermosensitivity in vivo.

Citing Articles

The odyssey of the TR(i)P journey to the cellular membrane.

Rivera B, Orellana-Serradell O, Servili E, Santos R, Brauchi S, Cerda O Front Cell Dev Biol. 2024; 12:1414935.

PMID: 39108834 PMC: 11300232. DOI: 10.3389/fcell.2024.1414935.

Validation of Six Commercial Antibodies for the Detection of Heterologous and Endogenous TRPM8 Ion Channel Expression.

Hernandez-Ortego P, Torres-Montero R, de la Pena E, Viana F, Fernandez-Trillo J Int J Mol Sci. 2022; 23(24).

PMID: 36555804 PMC: 9784522. DOI: 10.3390/ijms232416164.

Mutations of TRPM8 channels: Unraveling the molecular basis of activation by cold and ligands.

Plaza-Cayon A, Gonzalez-Muniz R, Martin-Martinez M Med Res Rev. 2022; 42(6):2168-2203.

PMID: 35976012 PMC: 9805079. DOI: 10.1002/med.21920.

A Novel Role of the TRPM4 Ion Channel in Exocytosis.

Stoklosa P, Kappel S, Peinelt C Cells. 2022; 11(11).

PMID: 35681487 PMC: 9180413. DOI: 10.3390/cells11111793.

Bradykinin-Induced Sensitization of Transient Receptor Potential Channel Melastatin 3 Calcium Responses in Mouse Nociceptive Neurons.

Behrendt M, Solinski H, Schmelz M, Carr R Front Cell Neurosci. 2022; 16:843225.

PMID: 35496916 PMC: 9043526. DOI: 10.3389/fncel.2022.843225.

References

Proux-Gillardeaux V, Raposo G, Irinopoulou T, Galli T . Expression of the Longin domain of TI-VAMP impairs lysosomal secretion and epithelial cell migration. Biol Cell. 2007; 99(5):261-71. DOI: 10.1042/BC20060097. View

Stein A, Ufret-Vincenty C, Hua L, Santana L, Gordon S . Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol. 2006; 128(5):509-22. PMC: 2151588. DOI: 10.1085/jgp.200609576. View

Ghosh D, Segal A, Voets T . Distinct modes of perimembrane TRP channel turnover revealed by TIR-FRAP. Sci Rep. 2014; 4:7111. PMC: 4236744. DOI: 10.1038/srep07111. View

McKemy D, Neuhausser W, Julius D . Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 2002; 416(6876):52-8. DOI: 10.1038/nature719. View

Hua Z, Leal-Ortiz S, Foss S, Waites C, Garner C, Voglmaier S . v-SNARE composition distinguishes synaptic vesicle pools. Neuron. 2011; 71(3):474-87. PMC: 3155686. DOI: 10.1016/j.neuron.2011.06.010. View

Voets T, Owsianik G, Janssens A, Talavera K, Nilius B . TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol. 2007; 3(3):174-82. DOI: 10.1038/nchembio862. View

Danglot L, Zylbersztejn K, Petkovic M, Gauberti M, Meziane H, Combe R . Absence of TI-VAMP/Vamp7 leads to increased anxiety in mice. J Neurosci. 2012; 32(6):1962-8. PMC: 6621696. DOI: 10.1523/JNEUROSCI.4436-11.2012. View

Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T . Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature. 2000; 406(6798):906-10. DOI: 10.1038/35022604. View

Hesketh G, Perez-Dorado I, Jackson L, Wartosch L, Schafer I, Gray S . VARP is recruited on to endosomes by direct interaction with retromer, where together they function in export to the cell surface. Dev Cell. 2014; 29(5):591-606. PMC: 4059916. DOI: 10.1016/j.devcel.2014.04.010. View

10.

Gorvel J, Chavrier P, Zerial M, Gruenberg J . rab5 controls early endosome fusion in vitro. Cell. 1991; 64(5):915-25. DOI: 10.1016/0092-8674(91)90316-q. View

11.

Ryan T . Kiss-and-run, fuse-pinch-and-linger, fuse-and-collapse: the life and times of a neurosecretory granule. Proc Natl Acad Sci U S A. 2003; 100(5):2171-3. PMC: 151312. DOI: 10.1073/pnas.0530260100. View

12.

Mindell J . Lysosomal acidification mechanisms. Annu Rev Physiol. 2012; 74:69-86. DOI: 10.1146/annurev-physiol-012110-142317. View

13.

Schmidt M, Dubin A, Petrus M, Earley T, Patapoutian A . Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron. 2009; 64(4):498-509. PMC: 2854037. DOI: 10.1016/j.neuron.2009.09.030. View

14.

Xing H, Chen M, Ling J, Tan W, Gu J . TRPM8 mechanism of cold allodynia after chronic nerve injury. J Neurosci. 2007; 27(50):13680-90. PMC: 6673615. DOI: 10.1523/JNEUROSCI.2203-07.2007. View

15.

Almeida M, Hew-Butler T, Soriano R, Rao S, Wang W, Wang J . Pharmacological blockade of the cold receptor TRPM8 attenuates autonomic and behavioral cold defenses and decreases deep body temperature. J Neurosci. 2012; 32(6):2086-99. PMC: 3566779. DOI: 10.1523/JNEUROSCI.5606-11.2012. View

16.

Vanoevelen J, Dode L, Van Baelen K, Fairclough R, Missiaen L, Raeymaekers L . The secretory pathway Ca2+/Mn2+-ATPase 2 is a Golgi-localized pump with high affinity for Ca2+ ions. J Biol Chem. 2005; 280(24):22800-8. DOI: 10.1074/jbc.M501026200. View

17.

Huynh K, Eskelinen E, Scott C, Malevanets A, Saftig P, Grinstein S . LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 2007; 26(2):313-24. PMC: 1783450. DOI: 10.1038/sj.emboj.7601511. View

18.

Melli G, Hoke A . Dorsal Root Ganglia Sensory Neuronal Cultures: a tool for drug discovery for peripheral neuropathies. Expert Opin Drug Discov. 2010; 4(10):1035-1045. PMC: 2908326. DOI: 10.1517/17460440903266829. View

19.

Vriens J, Owsianik G, Hofmann T, Philipp S, Stab J, Chen X . TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron. 2011; 70(3):482-94. DOI: 10.1016/j.neuron.2011.02.051. View

20.

Zakharian E, Cao C, Rohacs T . Gating of transient receptor potential melastatin 8 (TRPM8) channels activated by cold and chemical agonists in planar lipid bilayers. J Neurosci. 2010; 30(37):12526-34. PMC: 2989179. DOI: 10.1523/JNEUROSCI.3189-10.2010. View