Characterization of Functional TRPV1 Channels in the Sarcoplasmic Reticulum of Mouse Skeletal Muscle

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Lotteau, Sabine ^a,b,c   Ducreux, Sylvie ^a,b,c   Romestaing, Caroline ^b,d   Legrand, Claude ^a,b   Van Coppenolle, Fabien ^a,b,c  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c CarMeN   (France)

^d UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CAPSAICIN; DANTROLENE; RESINIFERATOXIN; RYANODINE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; MOLECULAR IMAGING; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CAPSAICIN; MALE; MICE; MUSCLE, SKELETAL; PROTEIN TRANSPORT; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; TRPV CATION CHANNELS;

EID: 84874830784     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058673     Document Type: Article

References (41)

1. Kunert-Keil C, Bisping F, Krüger J, Brinkmeier H, (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7: 159 doi:10.1186/1471-2164-7-159.
2. Rizzuto R, Pozzan T, (2003) When calcium goes wrong: genetic alterations of a ubiquitous signaling route. Nature Genetics 34: 135-141 doi:10.1038/ng0603-135.
3. MacLennan DH, Duff C, Zorzato F, Fujii J, Phillips M, et al. (1990) Ryanodine receptor gene is a candidate for predisposition to malignant hyperthermia. Nature 343: 559-561 doi:10.1038/343559a0.
4. Haan EA, Freemantle CJ, McCure JA, Friend KL, Mulley JC, (1990) Assignment of the gene for central core disease to chromosome 19. Hum Genet 86: 187-190.
5. Loke J, MacLennan DH, (1998) Malignant Hyperthermia and Central Core Disease: Disorders of Ca2 Release Channels. The American Journal of Medicine 104: 470-486 doi:10.1016/S0002-9343(98)00108-9.
6. Deng H-X, Klein CJ, Yan J, Shi Y, Wu Y, et al. (2010) Scapuloperoneal spinal muscular atrophy and CMT2C are allelic disorders caused by alterations in TRPV4. Nat Genet 42: 165-169 doi:10.1038/ng.509.
7. Landouré G, Zdebik AA, Martinez TL, Burnett BG, Stanescu HC, et al. (2010) Mutations in TRPV4 cause Charcot-Marie-Tooth disease type 2C. Nat Genet 42: 170-174 doi:10.1038/ng.512.
8. Auer-Grumbach M, Olschewski A, Papic L, Kremer H, McEntagart ME, et al. (2010) Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C. Nat Genet 42: 160-164 doi:10.1038/ng.508.
9. Astrea G, Brisca G, Fiorillo C, Valle M, Tosetti M, et al. (2012) Muscle MRI in TRPV4-related congenital distal SMA. Neurology 78: 364-365 doi:10.1212/WNL.0b013e318245295a.
10. Zanou N, Iwata Y, Schakman O, Lebacq J, Wakabayashi S, et al. (2009) Essential role of TRPV2 ion channel in the sensitivity of dystrophic muscle to eccentric contractions. FEBS Letters 583: 3600-3604 doi:10.1016/j.febslet.2009.10.033.
11. Flourakis M, Van Coppenolle F, Lehen'kyi V, Beck B, Skryma R, et al. (2006) Passive calcium leak via translocon is a first step for iPLA2-pathway regulated store operated channels activation. FASEB J 20: 1215-1217 doi:10.1096/fj.05-5254fje.
12. Stutzmann GE, Mattson MP, (2011) Endoplasmic Reticulum Ca2+ Handling in Excitable Cells in Health and Disease. Pharmacol Rev 63: 700-727 doi:10.1124/pr.110.003814.
13. Clapham DE, (2003) TRP channels as cellular sensors. Nature 426: 517-524 doi:10.1038/nature02196.
14. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824 doi:10.1038/39807.
15. Xin H, Tanaka H, Yamaguchi M, Takemori S, Nakamura A, et al. (2005) Vanilloid receptor expressed in the sarcoplasmic reticulum of rat skeletal muscle. Biochem Biophys Res Commun 332: 756-762 doi:10.1016/j.bbrc.2005.05.016.
16. Cavuoto P, McAinch AJ, Hatzinikolas G, Janovská A, Game P, et al. (2007) The expression of receptors for endocannabinoids in human and rodent skeletal muscle. Biochem Biophys Res Commun 364: 105-110 doi:10.1016/j.bbrc.2007.09.099.
17. Luo Z, Ma L, Zhao Z, He H, Yang D, et al. (2011) TRPV1 activation improves exercise endurance and energy metabolism through PGC-1α upregulation in mice. Cell Research. Available:http://www.ncbi.nlm.nih.gov/pubmed/22184011. Accessed 16 February 2012.
18. Sammels E, Parys JB, Missiaen L, De Smedt H, Bultynck G, (2010) Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 47: 297-314 doi:10.1016/j.ceca.2010.02.001.
19. Saito A, Seiler S, Chu A, Fleischer S, (1984) Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. The Journal of Cell Biology 99: 875-885 doi:10.1083/jcb.99.3.875.
20. Szentesi P, Szappanos H, Szegedi C, Gönczi M, Jona I, et al. (2004) Altered Elementary Calcium Release Events and Enhanced Calcium Release by Thymol in Rat Skeletal Muscle. Biophysical Journal 86: 1436-1453 doi:10.1016/S0006-3495(04)74213-7.
21. Legrand C, Giacomello E, Berthier C, Allard B, Sorrentino V, et al. (2008) Spontaneous and voltage-activated Ca2+ release in adult mouse skeletal muscle fibres expressing the type 3 ryanodine receptor. The Journal of Physiology 586: 441-457 doi:10.1113/jphysiol.2007.145862.
22. Berbey C, Weiss N, Legrand C, Allard B, (2009) Transient Receptor Potential Canonical Type 1 (TRPC1) Operates as a Sarcoplasmic Reticulum Calcium Leak Channel in Skeletal Muscle. Journal of Biological Chemistry 284: 36387-36394 doi:10.1074/jbc.M109.073221.
23. Olah Z, Szabo T, Karai L, Hough C, Fields RD, et al. (2001) Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 276: 11021-11030 doi:10.1074/jbc.M008392200.
24. Gallego-Sandín S, Rodríguez-García A, Alonso MT, García-Sancho J, (2009) The Endoplasmic Reticulum of Dorsal Root Ganglion Neurons Contains Functional TRPV1 Channels. Journal of Biological Chemistry 284: 32591-32601 doi:10.1074/jbc.M109.019687.
25. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, et al. (2003) Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23: 4054-4065.
26. Vriens J, Appendino G, Nilius B, (2009) Pharmacology of Vanilloid Transient Receptor Potential Cation Channels. Mol Pharmacol 75: 1262-1279 doi:10.1124/mol.109.055624.
27. Tóth A, Kedei N, Szabó T, Wang Y, Blumberg PM, (2002) Thapsigargin binds to and inhibits the cloned vanilloid receptor-1. Biochemical and Biophysical Research Communications 293: 777-782 doi:10.1016/S0006-291X(02)00293-0.
28. Zhao F, Li P, Chen SRW, Louis CF, Fruen BR, (2001) Dantrolene Inhibition of Ryanodine Receptor Ca2+Release Channels. J Biol Chem 276: 13810-13816 doi:10.1074/jbc.M006104200.
29. Palnitkar SS, Mickelson JR, Louis CF, Parness J, (1997) Pharmacological distinction between dantrolene and ryanodine binding sites: evidence from normal and malignant hyperthermia-susceptible porcine skeletal muscle. Biochem J 326 (Pt 3): 847-852.
30. Brinkmeier H (2011) TRP Channels in Skeletal Muscle: Gene Expression, Function and Implications for Disease. In: Islam MS, editor. Transient Receptor Potential Channels. Dordrecht: Springer Netherlands, Vol. 704. 749-758. Available:http://www.springerlink.com.gate1.inist.fr/content/v631467x4538lx74/. Accessed 23 January 2012.
31. Onozawa K, Nakamura A, Tsutsumi S, Yao J, Ishikawa R, et al. (2000) Tissue distribution of capsaicin receptor in the various organs of rats. Proceedings of the Japan Academy, Series B 76: 68-72.
32. Iwata Y, Katanosaka Y, Arai Y, Shigekawa M, Wakabayashi S, (2009) Dominant-negative inhibition of Ca2+ influx via TRPV2 ameliorates muscular dystrophy in animal models. Hum Mol Genet 18: 824-834 doi:10.1093/hmg/ddn408.
33. Touska F, Marsakova L, Teisinger J, Vlachova V, (2011) A "cute" desensitization of TRPV1. Curr Pharm Biotechnol 12: 122-129.
34. Endo M, (2009) Calcium-Induced Calcium Release in Skeletal Muscle. Physiol Rev 89: 1153-1176 doi:10.1152/physrev.00040.2008.
35. Numazaki M, (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proceedings of the National Academy of Sciences 100: 8002-8006 doi:10.1073/pnas.1337252100.
36. Pritschow BW, Lange T, Kasch J, Kunert-Keil C, Liedtke W, et al. (2010) Functional TRPV4 channels are expressed in mouse skeletal muscle and can modulate resting Ca2+ influx and muscle fatigue. Pflügers Archiv- European Journal of Physiology 461: 115-122 doi:10.1007/s00424-010-0883-4.
37. Krakow D, Vriens J, Camacho N, Luong P, Deixler H, et al. (2009) Mutations in the gene encoding the calcium-permeable ion channel TRPV4 produce spondylometaphyseal dysplasia, Kozlowski type and metatropic dysplasia. Am J Hum Genet 84: 307-315 doi:10.1016/j.ajhg.2009.01.021.
38. Krüger J, Kunert-Keil C, Bisping F, Brinkmeier H, (2008) Transient receptor potential cation channels in normal and dystrophic mdx muscle. Neuromuscular Disorders 18: 501-513 doi:10.1016/j.nmd.2008.04.003.
39. Garami A, Pakai E, Oliveira DL, Steiner AA, Wanner SP, et al. (2011) Thermoregulatory Phenotype of the Trpv1 Knockout Mouse: Thermoeffector Dysbalance with Hyperkinesis. J Neurosci 31: 1721-1733 doi:10.1523/JNEUROSCI.4671-10.2011.
40. Jordt S-E, Tominaga M, Julius D, (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proceedings of the National Academy of Sciences 97: 8134-8139 doi:10.1073/pnas.100129497.
41. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, et al. (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430: 748-754 doi:10.1038/nature02732.