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The Journal of Membrane Biology

, Volume 248, Issue 1, pp 31–38 | Cite as

Capsaicin and N-Arachidonoyl-dopamine (NADA) Decrease Tension by Activating Both Cannabinoid and Vanilloid Receptors in Fast Skeletal Muscle Fibers of the Frog

  • Xóchitl Trujillo
  • Mónica Ortiz-Mesina
  • Tannia Uribe
  • Elena Castro
  • Rocío Montoya-Pérez
  • Zorayda Urzúa
  • Alfredo Feria-Velasco
  • Miguel Huerta
Article

Abstract

Previous studies have indicated that vanilloid receptor (VR1) mRNA is expressed in muscle fibers. In this study, we evaluated the functional effects of VR1 activation. We measured caffeine-induced contractions in bundles of the extensor digitorum longus muscle of Rana pipiens. Isometric tension measurements showed that two VR1 agonists, capsaicin (CAP) and N-arachidonoyl-dopamine (NADA), reduced muscle peak tension to 57 ± 4 % and 71 ± 3 % of control, respectively. The effect of CAP was partially blocked by a VR1 blocker, capsazepine (CPZ), but the effect of NADA was not changed by CPZ. Because NADA is able to act on cannabinoid receptors, which are also present in muscle fibers, we tested the cannabinoid antagonist AM281. We found that AM281 antagonized both CAP and NADA effects. AM281 alone reduced peak tension to 80 ± 6 % of control. With both antagonists, the CAP effect was completely blocked, and the NADA effect was partially blocked. These results provide pharmacological evidence of the functional presence of the VR1 receptor in fast skeletal muscle fibers of the frog and suggest that capsaicin and NADA reduce tension by activating both cannabinoid and vanilloid receptors.

Keywords

Vanilloid receptor Cannabinoids receptor Capsaicin NADA Skeletal muscle Caffeine contracture Frog 

References

  1. Alworth LC, Harvey SB (2007) IACUC issues associated with amphibian research. ILAR J 48(3):278–289CrossRefPubMedGoogle Scholar
  2. Bisogno T, Melck D, Bobrov MYu, Gretskaya NM, Bezuglov VV, De Petrocellis L, Di Marzo V (2000) N-acyl-dopamines: novel synthetic CB(1) cannabinoid-receptor ligands and inhibitors of anandamide inactivation with cannabimimetic activity in vitro and in vivo. Biochem J 351(3):817–824PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bleakman D, Brorson JR, Miller RJ (1990) The effect of capsaicin on voltage-gated calcium currents and calcium signals in cultured dorsal root ganglion cells. Br J Pharmacol 101(2):423–431PubMedCentralCrossRefPubMedGoogle Scholar
  4. Cavuoto P, McAinch AJ, Hatzinikolas G, Janovská A, Game P, Wittert GA (2007) The expression of receptors for endocannabinoids in human and rodent skeletal muscle. Biochem Biophys Res Comm 364:105–110CrossRefPubMedGoogle Scholar
  5. Dewey WL (1986) Cannabinoid pharmacology. Pharmacol Rev 38:151–178PubMedGoogle Scholar
  6. Gilly WF, Hui CS (1980) Mechanical activation in slow and twitch skeletal muscle fibers of the frog. J Physiol 301:137–156PubMedCentralCrossRefPubMedGoogle Scholar
  7. Hillard CJ, Manna S, Greenberg MJ, DiCamelli R, Ross RA, Stevenson LA, Murphy V, Pertwee RG, Campbell WB (1999) Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J Pharmacol Exp Ther 289(3):1427–1428PubMedGoogle Scholar
  8. Hopps JJ, Dunn WR, Randall MD (2012) Vasorelaxation to capsaicin and its effects on calcium influx in arteries. Eur J Pharmacol 681(1–3):88–93CrossRefPubMedGoogle Scholar
  9. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54(2):161–202CrossRefPubMedGoogle Scholar
  10. Huang SM, Walker JM (2006) Enhancement of spontaneous and heat-evoked activity in spinal nociceptive neurons by the endovanilloid/endocannabinoid N-arachidonoyldopamine (NADA). J Neurophysiol 95(2):1207–1212CrossRefPubMedGoogle Scholar
  11. Huang SM, Bisogno T, Trevisani M, Al-Hayani A, De Petrocellis L, Fezza F, Tognetto M, Petros TJ, Krey JF, Chu CJ, Miller JD, Davies SN, Geppetti P, Walker JM, Di Marzo V (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci 99(12):8400–8405PubMedCentralCrossRefPubMedGoogle Scholar
  12. Huerta M, Muñiz J, Stefani E (1986) Effects of external calcium on potassium contracture in tonic muscle fibers of the frog (Rana pipiens). J Physiol 376:219–230PubMedCentralCrossRefPubMedGoogle Scholar
  13. Huerta M, Ortiz-Mesina M, Trujillo X, Sánchez-Pastor E, Vásquez C, Castro E, Velasco R, Montoya-Pérez R, Onetti C (2009) Effects of cannabinoid on caffeine contractures in slow and fast skeletal muscle fibers of the frog. J Membr Biol 229(2):91–99PubMedCentralCrossRefPubMedGoogle Scholar
  14. Huerta M, Sánchez-Pastor E, Trujillo X, Andrade F (2011) Co-localization of the cannabinoid 1 and acetylcholine receptors in the motor-endplate of the frog. 40th Annual meeting Washington USA C920Google Scholar
  15. Institute for Laboratory Animal Research (1996) Guide for the care and use of laboratory animals. National Research Council, Commision on life science, pp 1–50Google Scholar
  16. Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108(3):421–430CrossRefPubMedGoogle Scholar
  17. Kuffler SW, Vaughan-Williams EM (1953) Properties of the ‘slow’ skeletal muscles fibers of the frog. J Physiol 21(2):318–340CrossRefGoogle Scholar
  18. Lo YC, Wu SN, Wu JR, Chen IJ (1995) Effect of capsaicin on membrane currents in cultured vascular smooth muscle cells of rat aorta. Eur J Pharmacol 292(3–4):321–328PubMedGoogle Scholar
  19. Lotteau S, Ducreux S, Romestaing C, Legrand C, Van Coppenolle F (2013) Characterization of functional TRPV1 channels in the sarcoplasmic reticulum of mouse skeletal muscle. PLoS ONE 8(3):e58673PubMedCentralCrossRefPubMedGoogle Scholar
  20. Marinelli S, Di Marzo V, Florenzano F, Fezza F, Viscomi MT, van der Stelt M, Bernardi G, Molinari M, Maccarrone M, Mercuri NB (2007) N-arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32(2):298–308CrossRefPubMedGoogle Scholar
  21. Olah Z, Szabos T, Karai L, Hough C, Fields RD, Caudle RM, Blumberg PM, Ladarola MJ (2001) Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 276:11021–11030CrossRefPubMedGoogle Scholar
  22. Sánchez-Pastor E, Trujillo X, Huerta M, Andrade F (2007) Effects of cannabinoids on synaptic transmission in the frog neuromuscular junction. J Pharmacol Exp Ther 321(2):439–445CrossRefPubMedGoogle Scholar
  23. Sañudo-Peña MC, Romero J, Seale GE, Fernandez-Ruiz JJ, Walker JM (2000) Activational role of cannabinoids on movement. Eur J Pharmacol. 391(3):269–274CrossRefPubMedGoogle Scholar
  24. Silveira PE, Silveira NA, Morini Vde C, Kushmerick C, Naves LA (2010) Opposing effects of cannabinoids and vanilloids on evoked quantal release at the frog neuromuscular junction. Neurosci Lett 473(2):97–101CrossRefPubMedGoogle Scholar
  25. Soderstrom K, Leid M, Moore FL, Murray TF (2000) Behavioral, pharmacological, and molecular characterization of an amphibian cannabinoid receptor. J Neurochem 75(1):413–423CrossRefPubMedGoogle Scholar
  26. Starowicz K, Nigam S, Di Marzo V (2007) Biochemistry and pharmacology of endovanilloids. Pharmacol Ther 114(1):13–33CrossRefPubMedGoogle Scholar
  27. Starowicz K, Cristino L, Di Marzo V (2008) TRPV1 receptors in the central nervous system: potential for previously unforeseen therapeutic applications. Curr Pharm Des 14(1):42–54CrossRefPubMedGoogle Scholar
  28. Starowicz K, Makuch W, Osikowicz M, Piscitelli F, Petrosino S, Di Marzo V, Przewlocka B (2012) Spinal anandamide produces analgesia in neuropathic rats: possible CB(1)- and TRPV1-mediated mechanisms. Neuropharmacology 62(4):1746–1755CrossRefPubMedGoogle Scholar
  29. Szallasi A, Blumberg PM (1999) Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 51(2):159–212PubMedGoogle Scholar
  30. Thyagarajan B, Krivitskaya N, Potian JG, Hognason K, Garcia CC, McArdle JJ (2009) Capsaicin protects mouse neuromuscular junctions from the neuroparalytic effects of botulinum neurotoxin A. J Pharmacol Exp Ther 331(2):361–371PubMedCentralCrossRefPubMedGoogle Scholar
  31. Tóth A, Boczán J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135(1–2):162–168CrossRefPubMedGoogle Scholar
  32. Trujillo X, Sánchez-Pastor E, Andrade F, Huerta M (2014a) Effects of cannabinoids on tension induced by acetylcholine and choline in slow skeletal muscle fibers of the frog. J Membr Biol 247(1):57–62CrossRefPubMedGoogle Scholar
  33. Trujillo X, Sánchez-Pastor E, Andrade F, Huerta M (2014b) Presence and colocalization of type-1 cannabinoid receptors with acetylcholine receptors in the motor end-plate of twitch skeletal muscle fibers in the frog. J Membr Biol. doi: 10.1007/s00232-014-9721-5 Google Scholar
  34. Velasco R, Trujillo X, Vásquez C, Huerta M, Trujillo-Hernández B (2003) Effect of dimethyl sulfoxide on excitation-contraction coupling in chicken slow skeletal muscle. J Pharmacol Sci 93(2):149–154CrossRefPubMedGoogle Scholar
  35. Vriens J, Appendino G, Nilius B (2009) Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75(6):1262–1279CrossRefPubMedGoogle Scholar
  36. Wu ZZ, Chen SR, Pan HL (2005) Transient receptor potential vanilloid type 1 activation down-regulates voltage-gated calcium channels through calcium-dependent calcineurin in sensory neurons. J Biol Chem 280(18):18142–18151CrossRefPubMedGoogle Scholar
  37. Xin H, Tanaka H, Yamaguchi M, Takemori S, Nakamura A, Kohama K (2005) Vanilloid receptor expressed in the sarcoplasmic reticulum of rat skeletal muscle. Biochem Biophys Res Comm 332:756–762CrossRefPubMedGoogle Scholar
  38. Yeon D, Kwon S, Lee Y, Leem J, Nam T, Ahn D (2001) Capsaicin-induced relaxation in rabbit coronary artery. J Vet Med Sci 63(5):499–503CrossRefPubMedGoogle Scholar
  39. Zajicek J, Fox P, Sanders H, Wright D, Vickery J, Nunn A, Thompson A, UK MS Research Group (2003) Cannabinoids for treatment of spasticity and other symptoms related to multiple sclerosis (CAMS study): multicentre randomised placebo-controlled trial. Lancet 362(9395):1517–1526CrossRefPubMedGoogle Scholar
  40. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400(6743):452–457CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Xóchitl Trujillo
    • 1
  • Mónica Ortiz-Mesina
    • 1
  • Tannia Uribe
    • 1
  • Elena Castro
    • 1
  • Rocío Montoya-Pérez
    • 2
  • Zorayda Urzúa
    • 3
  • Alfredo Feria-Velasco
    • 4
  • Miguel Huerta
    • 1
  1. 1.Unidad de Investigación Dr. Enrico StefaniCentro Universitario de Investigaciones Biomédicas de la Universidad de ColimaColimaMexico
  2. 2.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  3. 3.Clínica de Medicina Familiar No. 19Instituto Mexicano del Seguro SocialColimaMexico
  4. 4.Coordinación General de Investigación y Posgrado de la Universidad de GuadalajaraGuadalajaraMexico

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