Serotonin contracts the rat mesenteric artery by inhibiting 4-aminopyridine-sensitive Kv channels via the 5-HT2A receptor and Src tyrosine kinase

Experimental and Molecular Medicine

Volumn 45, Issue 12, 2013, Pages

  Sung, Dong Jun ^a,b   Noh, Hyun Ju ^c   Kim, Jae Gon ^c   Park, Sang Woong ^c   Kim, Bokyung ^c   Cho, Hana ^a   Bae, Young Min ^c  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b Konkuk University   (South Korea)

^c Konkuk University School of Medicine   (South Korea)

Author keywords

5 HT2A receptor; Mesenteric artery; Serotonin (5 hydroxytryptamine)

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; 4 AMINOPYRIDINE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM ACTIVATED POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; KETANSERIN; NIFEDIPINE; POTASSIUM CHLORIDE; PROTEIN TYROSINE KINASE; SEROTONIN; SEROTONIN 2 AGONIST; SEROTONIN 2A RECEPTOR; SPIPERONE; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL BLOCKING AGENT; PROTEIN KINASE INHIBITOR; SEROTONIN 2 ANTAGONIST;

ANIMAL CELL; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTERY TONE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CONTROLLED STUDY; ISOMETRICS; MALE; MESENTERIC ARTERY; NONHUMAN; PATCH CLAMP TECHNIQUE; RAT; SMOOTH MUSCLE FIBER; ACTION POTENTIAL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CELLS, CULTURED; KETANSERIN; MALE; MESENTERIC ARTERIES; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NIFEDIPINE; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN KINASE INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SPIPERONE; SRC-FAMILY KINASES; VASOCONSTRICTION;

EID: 84892154521     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2013.116     Document Type: Article

References (46)

1. Watts SW. 5-HT in systemic hypertension: foe, friend or fantasy? Clin Sci (Lond) 2005; 108: 399-412.
2. Jakab RL, Goldman-Rakic PS. 5-Hydroxytryptamine2A serotonin receptors in the primate cerebral cortex: possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc Natl Acad Sci USA 1998; 95: 735-740.
3. Miner LA, Backstrom JR, Sanders-Bush E, Sesack SR. Ultrastructural localization of serotonin2A receptors in the middle layers of the rat prelimbic prefrontal cortex. Neuroscience 2003; 116: 107-117.
4. Roth BL, Hanizavareh SM, Blum AE. Serotonin receptors represent highly favorable molecular targets for cognitive enhancement in schizophrenia and other disorders. Psychopharmacology (Berl) 2004; 174: 17-24.
5. Berg KA, Harvey JA, Spampinato U, Clarke WP. Physiological and therapeutic relevance of constitutive activity of 5-HT 2A and 5-HT 2C receptors for the treatment of depression. Prog Brain Res 2008; 172: 287-305.
6. Halford JC, Harrold JA, Lawton CL, Blundell JE. Serotonin (5-HT) drugs: effects on appetite expression and use for the treatment of obesity. Curr Drug Targets 2005; 6: 201-213.
7. Wagstaff AJ, Cheer SM, Matheson AJ, Ormrod D, Goa KL. Spotlight on paroxetine in psychiatric disorders in adults. CNS Drugs 2002; 16: 425-434.
8. Barbey JT, Roose SP. SSRI safety in overdose. J Clin Psychiatry 1998; 59: 42-48.
9. Albert AP, Spyer KM, Brooks PA. The effect of 5-HT and selective 5-HT receptor agonists and antagonists on rat dorsal vagal preganglionic neurones in vitro. Br J Pharmacol 1996; 119: 519-526.
10. Bae YM, Kim A, Kim J, Park SW, Kim TK, Lee YR et al. Serotonin depolarizes the membrane potential in rat mesenteric artery myocytes by decreasing voltage-gated K+ currents. Biochem Biophys Res Commun 2006; 347: 468-476.
11. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 2009; 54: S20-S31.
12. Jin NG, Crow T. Serotonin regulates voltage-dependent currents in type I(e(A)) and I(i) interneurons of Hermissenda. J Neurophysiol 2011; 106: 2557-2569.
13. Zhang M, Fearon IM, Zhong H, Nurse CA. Presynaptic modulation of rat arterial chemoreceptor function by 5-HT: role of K+ channel inhibition via protein kinase C. J Physiol 2003; 551: 825-842.
14. Cogolludo A, Moreno L, Lodi F, Frazziano G, Cobeno L, Tamargo J et al. Serotonin inhibits voltage-gated K+ currents in pulmonary artery smooth muscle cells: role of 5-HT2A receptors, caveolin-1, and Kv1.5 channel internalization. Circ Res 2006; 98: 931-938.
15. Michelakis E. Anorectic drugs and vascular disease: the role of voltagegated K+ channels. Vascul Pharmacol 1995; 38: 51-59.
16. Bonev AD, Nelson MT. Vasoconstrictors inhibit ATP-sensitive K+ channels in arterial smooth muscle through protein kinase C. J Gen Physiol 1996; 108: 315-323.
17. Kleppisch T, Nelson MT. ATP-sensitive K+ currents in cerebral arterial smooth muscle: pharmacological and hormonal modulation. Am J Physiol 1995; 269: H1634-H1640.
18. Teng GQ, Nauli SM, Brayden JE, Pearce WJ. Maturation alters the contribution of potassium channels to resting and 5HT-induced tone in small cerebral arteries of the sheep. Brain Res Dev Brain Res 2002; 133: 81-91.
19. Wang Y, Zhang HT, Su XL, Deng XL, Yuan BX, Zhang W et al. Experimental diabetes mellitus down-regulates large-conductance Ca2+-activated K+ channels in cerebral artery smooth muscle and alters functional conductance. Curr Neurovasc Res 2010; 7: 75-84.
20. Vanhoutte PM. Serotonin, hypertension and vascular disease. Neth J Med 1991; 38: 35-42.
21. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane WJ et al. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol Rev 1994; 46: 158-203.
22. Alexander N, Kuepper Y, Schmitz A, Osinsky R, Kozyra E, Hennig J. Geneenvironment interactions predict cortisol responses after acute stress: implications for the etiology of depression. Psychoneuroendocrinology 2009; 34: 1294-1303.
23. Bhatnagar A, Sheffler DJ, Kroeze WK, Compton-Toth B, Roth BL. Caveolin-1 interacts with 5-HT2A serotonin receptors and profoundly modulates the signaling of selected Gaq-coupled protein receptors. J Biol Chem 2004; 279: 34614-34623.
24. Gray JA, Roth BL. A last GASP for GPCRs? Science 2002; 297: 529-531.
25. Raymond JR, Mukhin YV, Gelasco A, Turner J, Collinsworth G, Gettys TW et al. Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol Ther 2001; 92: 179-212.
26. Lu R, Alioua A, Kumar Y, Kundu P, Eghbali M, Weisstaub NV et al. c-Src tyrosine kinase, a critical component for 5-HT2A receptor-mediated contraction in rat aorta. J Physiol 2008; 586: 3855-3869.
27. Kim A, Bae YM, Kim J, Kim B, Ho WK, Earm YE et al. Direct block by bisindolylmaleimide of the voltage-dependent K+ currents of rat mesenteric arterial smooth muscle. Eur J Pharmacol 2004; 483: 117-126.
28. Kim SH, Bae YM, Sung DJ, Park SW, Woo NS, Kim B et al. Ketamine blocks voltage-gated K+ channels and causes membrane depolarization in rat mesenteric artery myocytes. Pflügers Arch 2007; 454: 891-902.
29. Bae YM, Kim A, Lee YJ, Lim W, Noh YH, Kim EJ et al. Enhancement of receptor-operated cation current and TRPC6 expression in arterial smooth muscle cells of deoxycorticosterone acetate-salt hypertensive rats. J Hypertens 2007; 25: 809-817.
30. Noorani MM, Noel RC, Marrelli SP. Upregulated TRPC3 and downregulated TRPC1 channel expression during hypertension is associated with increased vascular contractility in rat. Front Physiol 2011; 2: 42.
31. Zulian A, Baryshnikov SG, Linde CI, Hamlyn JM, Ferrari P, Golovina VA. Upregulation of Na+/Ca2+ exchanger and TRPC6 contributes to abnormal Ca2+ homeostasis in arterial smooth muscle cells from Milan hypertensive rats. Am J Physiol Heart Circ Physiol 2010; 299: H624-H633.
32. Yu Y, Fantozzi I, Remillard CV, Landsberg JW, Kunichika N, Platoshyn O et al. Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc Natl Acad Sci USA 2004; 101: 13861-13866.
33. Nelson MT, Standen NB, Brayden JE, Worley JF III. Noradrenaline contracts arteries by activating voltage-dependent calcium channels. Nature 1988; 336: 382-385.
34. Reading SA, Earley S, Waldron BJ, Welsh DG, Brayden JE. TRPC3 mediates pyrimidine receptor-induced depolarization of cerebral arteries. Am J Physiol Heart Circ Physiol 2005; 288: H2055-H2061.
35. Watts SW. Serotonin-induced contraction in mesenteric resistance arteries: signaling and changes in deoxycorticosterone acetate-salt hypertension. Hypertension 2002; 39: 825-829.
36. Chan KY, De Vries R, Leijten FP, Pfannkuche HJ, van den Bogaerdt AJ, Danser AH et al. Functional characterization of contractions to tegaserod in human isolated proximal and distal coronary arteries. Eur J Pharmacol 2009; 619: 61-67.
37. Al-Judaibi B, Chande N, Gregor J. Safety and efficacy of tegaserod therapy in patients with irritable bowel syndrome or chronic constipation. Can J Clin Pharmacol 2010; 17: 194-200.
38. Loughlin J, Quinn S, Rivero E, Wong J, Huang J, Kralstein J et al. Tegaserod and the risk of cardiovascular ischemic events: an observational cohort study. J Cardiovasc Pharmacol Ther 2010; 15: 151-157.
39. Banes AK, Watts SW. Arterial expression of 5-HT2B and 5-HT1B receptors during development of DOCA-salt hypertension. BMC Pharmacol 2003; 3: 1-15.
40. Joseph BK, Thakali KM, Moore CL, Rhee SW. Ion channel remodeling in vascular smooth muscle during hypertension: implications for novel therapeutic approaches. Pharmacol Res 2013; 70: 126-138.
41. Lu Y, Hanna ST, Tang G, Wang R. Contributions of Kv1.2, Kv1.5 and Kv2.1 subunits to the native delayed rectifier K(+) current in rat mesenteric artery smooth muscle cells. Life Sci 2002; 71: 1465-1473.
42. Choi WS, Khurana A, Mathur R, Viswanathan V, Steele DF, Fedida D. Kv1.5 surface expression is modulated by retrograde trafficking of newly endocytosed channels by the dynein motor. Circ Res 2005; 97: 363-371.
43. Nitabach MN, Llamas DA, Thompson IJ, Collins KA, Holmes TC. Phosphorylation-dependent and phosphorylation-independent modes of modulation of shaker family voltage-gated potassium channels by SRC family protein tyrosine kinases. J Neurosci 2002; 22: 7913-7922.
44. D'Adamo MC, Servettini I, Guglielmi L, Di Matteo V, Di Maio R, Di Giovanni G et al. 5-HT2 receptors-mediated modulation of voltagegated K+ channels and neurophysiopathological correlates. Exp Brain Res (e-pub ahead of print 24 May 2013).
45. Lambe EK, Aghajanian GK. The role of Kv1.2-containing potassium channels in serotonin-induced glutamate release from thalamocortical terminals in rat frontal cortex. J Neurosci 2001; 21: 9955-9963.
46. Lambe EK, Goldman-Rakic PS, Aghajanian GK. Serotonin induces EPSCs preferentially in layer V pyramidal neurons of the frontal cortex in the rat. Cereb Cortex 2000; 10: 974-980.