Abstract
Transient receptor potential vanilloid channel 2 (TRPV2) is required for normal cardiac contractility. The stimulation of TRPV1 in isolated cardiomyocytes can aggravate the effect of hypoxia/ reoxygenation (H/R) on H9C2 cells. The knockout of the TRPV1 gene promotes increased tolerance of the isolated perfused heart to the impact of ischemia/reperfusion (I/R). However, activation of TRPV1 increases the resistance of the heart to I/R due to calcitonin gene-related peptide (CGRP) release from afferent nerve endings. It has been established that TRPV1 and TRPV2 are involved in the pathogenesis of myocardial infarction and, in all likelihood, ensure the cardiac tolerance to the ischemia/reperfusion. It has also been documented that the activation of TRPV4 negatively affects the stability of cardiomyocytes to the H/R. The blockade of TRPV4 can be considered as a new approach to the prevention of I/R injury of the heart. Studies also indicate that TRPV1 is involved in the pathogenesis of cardiac hypertrophy and that TRPV2 channels participate in the pathogenesis of dilated cardiomyopathy. Excessive expression of TRPV2 leads to chronic Ca2+- overload of cardiomyocytes, which may contribute to the development of cardiomyopathy.
Keywords: Heart, TRPV1, TRPV2, TRPV4, cardiomyocytes, cardiomyopathy.
Graphical Abstract
[1]
Li M, Yu Y, Yang J. Structural biology of TRP channels. Chapter
1. In: Transient Receptor Potential Channels.Adv Exp Med Biol
Islam MS, ed. 2011; 704: pp. Berlin: Springer. 1-23.
[2]
De Petrocellis L, Nabissi M, Santoni G, Ligresti A. Actions and regulation of ionotropic cannabinoid receptors. Adv Pharmacol 2017; 80: 249-89.
[3]
Vriens J, Nilius B, Voets T. Peripheral thermosensation in mammals. Nat Rev Neurosci 2014; 15(9): 573-89.
[4]
Guo A, Vulchanova L, Wang J, Li X, Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): Relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 1999; 11(3): 946-58.
[5]
Szallasi A, Blumberg PM, Annicelli LL, Krause JE, Cortright DN. The cloned rat vanilloid receptor VR1 mediates both R-type binding and C-type calcium response in dorsal root ganglion neurons. Mol Pharmacol 1999; 56(3): 581-7.
[6]
Ward SM, Bayguinov J, Won KJ, Grundy D, Berthoud HR. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol 2003; 465(1): 121-35.
[7]
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997; 389: 816-24.
[8]
Tominaga M, Caterina MJ, Malmberg AB, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998; 21(3): 531-43.
[9]
Zahner MR, Li DP, Chen SR, Pan HL. Cardiac vanilloid receptor 1-expressing afferent nerves and their role in the cardiogenic sympathetic reflex in rats. J Physiol 2003; 551(Pt 2): 515-23.
[10]
Sun Z, Han J, Zhao W, et al. TRPV1 activation exacerbates hypoxia/reoxygenation-induced apoptosis in H9C2 cells via calcium overload and mitochondrial dysfunction. Int J Mol Sci 2014; 15(10): 18362-80.
[11]
Szallasi A, Blumberg PM. Resiniferatoxin, a phorbol-related diterpene, acts as an ultrapotent analog of capsaicin, the irritant constituent in red pepper. Neuroscience 1989; 30(2): 515-20.
[12]
De Petrocellis L, Schiano Moriello A. Modulation of the TRPV1 channel: Current clinical trials and recent patents with focus on neurological conditions. Recent Patents CNS Drug Discov 2013; 8(3): 180-204.
[13]
Bevan S, Hothi S, Hughes G, et al. Capsazepine: A competitive antagonist of the sensory neuron excitant capsaicin. Br J Pharmacol 1992; 107(2): 544-52.
[14]
Walpole CSJ, Bevan S, Bovermann G, et al. The discovery of capsazepine, the first competitive antagonist of the sensory neuron excitant capsaicin and resiniferatoxin. J Med Chem 1994; 37(13): 1942-54.
[15]
Szallasi A, Blumberg PM. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 1999; 51(2): 159-212.
[16]
Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 1999; 398(6726): 436-41.
[17]
Muraki K, Iwata Y, Katanosaka Y, et al. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 2003; 93(9): 829-38.
[18]
Koch SE, Gao X, Haar L, et al. Probenecid: Novel use as a non-injurious positive inotrope acting via cardiac TRPV2 stimulation. J Mol Cell Cardiol 2012; 53(1): 134-44.
[19]
Iwata Y, Katanosaka Y, Arai Y, Kamamura K, Miyatake K, Shigekawa M. A novel mechanism of myocyte degeneration involving Ca2+-permeable growth factor-regulated channel. J Cell Biol 2003; 161(5): 957-67.
[20]
Iwata Y, Ohtake H, Suzuki O, Matsuda J, Komamura K, Wakabayashi S. Blockade of sarcolemmal TRPV2 accumulation inhibits progression of dilated cardiomyopathy. Cardiovasc Res 2013; 99(4): 760-8.
[21]
Lorin C, Vögeli I, Niggli E. Dystrophic cardiomyopathy: Role of TRPV2 channels in stretch-induced cell damage. Cardiovasc Res 2015; 106(1): 153-62.
[22]
Bang S, Kim KY, Yoo S, Lee SH, Hwang SW. Transient receptor potential V2 expressed in sensory neurons is activated by probenecid. Neurosci Lett 2007; 425(2): 120-5.
[23]
Mihara H, Boudaka A, Shibasaki K, Yamanaka A, Sugiyama T, Tominaga M. Involvement of TRPV2 activation in intestinal movement through nitric oxide production in mice. J Neurosci 2010; 30(49): 16536-44.
[24]
Liedtke W, Choe Y, Marti-Renom MA, et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 2000; 103(3): 525-35.
[25]
Wu QF, Qian C, Zhao N, et al. Activation of transient receptor potential vanilloid 4 involves in hypoxia/reoxygenation injury in cardiomyocytes. Cell Death Dis 2017; 8(5)e2828
[26]
Rubinstein J, Lasko VM, Koch SE, et al. Novel role of transient receptor potential vanilloid 2 in the regulation of cardiac performance. Am J Physiol Heart Circ Physiol 2014; 306(4): H574-84.
[27]
Koch SE, Nieman ML, Robbins N, et al. Tranilast blunts the hypertrophic and fibrotic response to increased afterload independent of cardiomyocyte transient receptor potential vanilloid 2 channels. J Cardiovasc Pharmacol 2018; 72(1): 40-8.
[28]
Katanosaka Y, Iwasaki K, Ujihara Y, et al. TRPV2 is critical for the maintenance of cardiac structure and function in mice. Nat Commun 2014; 5: 3932.
[29]
Naticchioni M, Karani R, Smith MA, et al. Transient receptor potential vanilloid 2 regulates myocardial response to exercise. PLoS One 2015; 10(9)e0136901
[30]
Li J, Wang MH, Wang L, et al. Role of transient receptor potential vanilloid 4 in the effect of osmotic pressure in myocardial contractility in rat. Acta Phys Sin 2008; 60(2): 181-8.
[31]
Willette RN, Bao W, Nerurkar S, et al. Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse: Part 2. J Pharmacol Exp Ther 2008; 326(2): 443-52.
[32]
Wang L, Wang DH. TRPV1 gene knockout impairs postischemic recovery in isolated perfused heart in mice. Circulation 2005; 112(23): 3617-23.
[33]
Entin-Meer M, Levy R, Goryainov P, et al. The transient receptor potential vanilloid 2 cation channel is abundant in macrophages accumulating at the peri-infarct zone and may enhance their migration capacity towards injured cardiomyocytes following myocardial infarction. PLoS One 2014; 9(8)e105055
[34]
Sexton A, McDonald M, Cayla C, Thiemermann C, Ahluwalia A. 12-Lipoxygenase-derived eicosanoids protect against myocardial ischemia/reperfusion injury via activation of neuronal TRPV1. FASEB J 2007; 21(11): 2695-703.
[35]
Huang W, Rubinstein J, Prieto AR, Thang LV, Wang DH. Transient receptor potential vanilloid gene deletion exacerbates inflammation and atypical cardiac remodeling after myocardial infarction. Hypertension 2009; 53(2): 243-50.
[36]
Lei J, Zhu F, Zhang Y, Duan L, Lei H, Huang W. Transient receptor potential vanilloid subtype 1 inhibits inflammation and apoptosis via the release of calcitonin gene-related peptide in the heart after myocardial Infarction. Cardiology 2016; 134(4): 436-43.
[37]
Randhawa PK, Jaggi AS. Exploring the putative role of TRPV1-dependent CGRP release in remote hind preconditioning-induced cardioprotection. Cardiovasc Ther 2017; 35(5)
[http://dx.doi.org/10.1111/1755-5922.12276]
[http://dx.doi.org/10.1111/1755-5922.12276]
[38]
Randhawa PK, Jaggi AS. Investigating the involvement of glycogen synthase kinase-3β and gap junction signaling in TRPV1 and remote hind preconditioning-induced cardioprotection. Eur J Pharmacol 2017; 814: 9-17.
[39]
Jiang XX, Liu GY, Lei H, Li ZL, Feng QP, Huang W. Activation of transient receptor potential vanilloid 1 protects the heart against apoptosis in ischemia/reperfusion injury through upregulating the PI3K/Akt signaling pathway. Int J Mol Med 2018; 41(3): 1724-30.
[40]
Wei Z, Wang L, Han J, et al. Decreased expression of transient receptor potential vanilloid 1 impaires the postischemic recovery of diabetic mouse hearts. Circ J 2009; 73(6): 1127-32.
[41]
Hurt CM, Lu Y, Stary CM, et al. Transient receptor potential vanilloid 1 regulates mitochondrial membrane potential and myocardial reperfusion injury. J Am Heart Assoc 2016; 5(9)e003774
[42]
Wu Y, Heymann HM, Gross ER. Non-opioid analgesic use and concerns for impaired organ protection. Br J Anaesth 2018; 120(2): 403-5.
[43]
Heymann HM, Wu Y, Lu Y, Qvit N, Gross GJ, Gross ER. Transient receptor potential vanilloid 1 inhibitors block laparotomy- and opioid-induced infarct size reduction in rats. Br J Pharmacol 2017; 174(24): 4826-35.
[44]
Bisogno T, Hanus L, De Petrocellis L, et al. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br J Pharmacol 2001; 134(4): 845-52.
[45]
De Petrocellis L, Ligresti A, Schiano Moriello A, et al. Effects of cannabinoids and cannabinoid-enriched Cannabis extracts on TRP channels and endocannabinoid metabolic enzymes. Br J Pharmacol 2011; 163(7): 1479-94.
[46]
Qin N, Neeper MP, Liu Y, Hutchinson TL, Lubin ML, Flores CM. TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J Neurosci 2008; 28(24): 6231-8.
[47]
Durst R, Danenberg H, Gallily R, et al. Cannabidiol, a nonpsychoactive Cannabis constituent, protects against myocardial ischemic reperfusion injury. Am J Physiol Heart Circ Physiol 2007; 293(6): H3602-7.
[48]
Rajesh M, Mukhopadhyay P, Bátkai S, et al. Cannabidiol attenuates cardiac dysfunction, oxidative stress, fibrosis, and inflammatory and cell death signaling pathways in diabetic cardiomyopathy. J Am Coll Cardiol 2010; 56(25): 2115-25.
[49]
Ligresti A, De Petrocellis L, Di Marzo V. From phytocannabinoids to cannabinoid receptors and endocannabinoids: Pleiotropic physiological and pathological roles through complex pharmacology. Physiol Rev 2016; 96(4): 1593-659.
[50]
Horváth B, Mukhopadhyay P, Haskó G, Pacher P. The endocannabinoid system and plant-derived cannabinoids in diabetes and diabetic complications. Am J Pathol 2012; 180(2): 432-42.
[51]
Lu S, Xu D. Cold stress accentuates pressure overload-induced cardiac hypertrophy and contractile dysfunction: Role of TRPV1/AMPK-mediated autophagy. Biochem Biophys Res Commun 2013; 442(1-2): 8-15.
[52]
Chen M, Xin J, Liu B, et al. Mitogen-activated protein kinase and intracellular polyamine signaling is involved in TRPV1 activation-induced cardiac hypertrophy. J Am Heart Assoc 2016; 5(8)e003718
[53]
Aguettaz E, Lopez JJ, Krzesiak A, et al. Axial stretch-dependent cation entry in dystrophic cardiomyopathy: Involvement of several TRPs channels. Cell Calcium 2016; 59(4): 145-55.
[54]
Dong Q, Li J, Wu QF, et al. Blockage of transient receptor potential vanilloid 4 alleviates myocardial ischemia/reperfusion injury in mice. Sci Rep 2017; 7: 42678.
[55]
Peart JN, Gross ER, Reichelt ME, Hsu A, Headrick JP, Gross GJ. Activation of kappa-opioid receptors at reperfusion affords cardioprotection in both rat and mouse hearts. Basic Res Cardiol 2008; 103(5): 454-63.
[56]
Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection. Cardiovasc Res 2004; 61(3): 372-85.
[57]
Halestrap AP. Calcium, mitochondria and reperfusion injury: A pore way to die. Biochem Soc Trans 2006; 34(Pt 2): 232-77.
[58]
Halestrap AP, Clarke SJ, Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim Biophys Acta 2007; 1767(8): 1007-31.
[59]
Evangelista S. Capsaicin receptor as target of calcitonin generelated
peptide in the gut. In: Abdel-Salam O. (eds) Capsaicin as a
Therapeutic Molecule.Prog Drug Res 2014; 68: 259-76.
[60]
Luo XJ, Liu B, Dai Z, Yang ZC, Peng J. Stimulation of calcitonin gene-related peptide release through targeting capsaicin receptor: A potential strategy for gastric mucosal protection. Dig Dis Sci 2013; 58(2): 320-5.
[61]
Rezaeian AH, Isokane T, Nishibori M, et al. αCGRP and βCGRP transcript amount in mouse tissues of various developmental stages and their tissue expression sites. Brain Dev 2009; 31(9): 682-93.
[62]
Franco-Cereceda A, Lundberg JM, Saria A, Schreibmayer W, Tritthart HA. Calcitonin gene-related peptide: release by capsaicin and prolongation of the action potential in the guinea-pig heart. Acta Physiol Scand 1988; 132(2): 181-90.
[63]
Poyner DR, Marshall I. CGRP receptors: Beyond the CGRP1-CGRP2 subdivision. Trends Pharmacol Sci 2001; 22(5): 223.
[64]
Poyner DR, Sexton PM, Marshall I, et al. International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol Re 2002; 54(2): 233-46.
[65]
Goto K, Miyauchi T, Homma S, Ohshima N. Calcitonin gene-related peptide in the regulation of cardiac function. Ann N Y Acad Sci 1992; 657: 194-203.
[66]
Main MJ, Brown J, Brown S, Fraser NJ, Foord SM. The CGRP receptor can couple via pertussis toxin sensitive and insensitive G proteins. FEBS Lett 1998; 441(1): 6-10.
[67]
Chatterjee TK, Moy JA, Fisher RA. Characterization and regulation of high affinity calcitonin gene-related peptide receptors in cultured neonatal rat cardiac myocytes. Endocrinology 1991; 128(6): 2731-38.
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