Modulation of CaV1.2 calcium channel by neuropeptideW regulates vascularmyogenic tone via G protein-coupled receptor 7

Journal of Hypertension

Volumn 33, Issue 12, 2015, Pages 2431-2442

  Ji, Li ^a   Zhu, Huayuan ^b   Chen, Hong ^a   Fan, Wenyong ^a   Chen, Junjie ^a   Chen, Jing ^a   Zhu, Guoqing ^a   Wang, Juejin ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

CaV1.2 calcium channel; G protein coupled receptor 7; hypertension; neuropeptide W; vascular myogenic tone

Indexed keywords

CALCIUM CHANNEL L TYPE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; DIACYLGLYCEROL; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; NEUROPEPTIDE; NEUROPEPTIDE W; PHOSPHOLIPASE C; PROTEIN KINASE C; UNCLASSIFIED DRUG; L-TYPE CALCIUM CHANNEL ALPHA(1C); NEUROPEPTIDE RECEPTOR; NPBWR1 PROTEIN, HUMAN; NPW PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY MUSCLE; ARTICLE; BLOOD VESSEL TONE; CALCIUM CURRENT; CATALYSIS; CELL ISOLATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENETIC TRANSFECTION; HALF-ACTIVATION VOLTAGE; HUMAN; HUMAN CELL; HYPERTENSION; INTESTINE PRESSURE; MALE; MESENTERIC ARTERY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SECOND MESSENGER; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE CELL; WHOLE CELL PATCH CLAMP; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; BLOOD PRESSURE; CALCIUM CHANNELS, L-TYPE; DIGLYCERIDES; HEK293 CELLS; HUMANS; HYPERTENSION; MALE; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEUROPEPTIDES; PROTEIN KINASE INHIBITORS; RATS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84946728505     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0000000000000723     Document Type: Article

References (49)

1. O'Dowd BF, Scheideler MA, Nguyen T, Cheng R, Rasmussen JS, Marchese A, et al. The cloning and chromosomal mapping of two novel human opioid-somatostatin-like receptor genes, GPR7 and GPR8, expressed in discrete areas of the brain. Genomics 1995; 28:84-91.
2. Tanaka H, Yoshida T, Miyamoto N, Motoike T, Kurosu H, Shibata K, et al. Characterization of a family of endogenous neuropeptide ligands for the G protein-coupled receptors GPR7 and GPR8. Proc Natl Acad Sci USA 2003; 100:6251-6256.
3. Fujii R, Yoshida H, Fukusumi S, Habata Y, Hosoya M, Kawamata Y, et al. Identification of a neuropeptide modified with bromine as an endogenous ligand for GPR7. J Biol Chem 2002; 277:34010-34016.
4. Lee DK, Nguyen T, Porter CA, Cheng R, George SR, O'Dowd BF. Two related G protein-coupled receptors: the distribution of GPR7 in rat brain and the absence of GPR8 in rodents. Brain Res Mol Brain Res 1999; 71:96-103.
5. Shimomura Y, Harada M, Goto M, Sugo T, Matsumoto Y, Abe M, et al. Identification of neuropeptide Was the endogenous ligand for orphan G-protein-coupled receptors GPR7 and GPR8. J Biol Chem 2002; 277:35826-35832.
6. Caminos JE, Bravo SB, Garcia-Rendueles ME, Ruth Gonzalez C, Garces MF, Cepeda LA, et al. Expression of neuropeptide W in rat stomach mucosa: regulation by nutritional status, glucocorticoids and thyroid hormones. Regul Pept 2008; 146:106-111.
7. Dezaki K, Kageyama H, Seki M, Shioda S, Yada T. Neuropeptide W in the rat pancreas: potentiation of glucose-induced insulin release and Ca2 influx through L-type Ca2 channels in beta-cells and localization in islets. Regul Pept 2008; 145:153-158.
8. Skrzypski M, Pruszynska-Oszmalek E, Rucinski M, Szczepankiewicz D, Sassek M, Wojciechowicz T, et al. Neuropeptide B and W regulate leptin and resistin secretion, and stimulate lipolysis in isolated rat adipocytes. Regul Pept 2012; 176:51-56.
9. Brezillon S, Lannoy V, Franssen JD, Le Poul E, Dupriez V, Lucchetti J, et al. Identification of natural ligands for the orphan G protein-coupled receptors GPR7 and GPR8. J Biol Chem 2003; 278:776-783.
10. Baker JR, Cardinal K, Bober C, Taylor MM, Samson WK. Neuropeptide W acts in brain to control prolactin, corticosterone, and growth hormone release. Endocrinology 2003; 144:2816-2821.
11. Levine AS, Winsky-Sommerer R, Huitron-Resendiz S, Grace MK, de Lecea L. Injection of neuropeptide W into paraventricular nucleus of hypothalamus increases food intake. Am J Physiol Regul Integr Comp Physiol 2005; 288:R1727-R1732.
12. Mondal MS, Yamaguchi H, Date Y, Shimbara T, Toshinai K, Shimomura Y, et al. A role for neuropeptide W in the regulation of feeding behavior. Endocrinology 2003; 144:4729-4733.
13. Yamamoto T, Saito O, Shono K, Tanabe S. Anti-hyperalgesic effects of intrathecally administered neuropeptide W-23, and neuropeptide B, in tests of inflammatory pain in rats. Brain Res 2005; 1045:97-106.
14. Nagata-Kuroiwa R, Furutani N, Hara J, Hondo M, Ishii M, Abe T, et al. Critical role of neuropeptides B/W receptor 1 signaling in social behavior and fear memory. PLoS One 2011; 6:e16972.
15. Hill MA, Zou H, Potocnik SJ, Meininger GA, Davis MJ. Invited review: arteriolar smooth muscle mechanotransduction: Ca2 signaling pathways underlying myogenic reactivity. J Appl Physiol 2001; 91:973-983.
16. Moosmang S, Schulla V, Welling A, Feil R, Feil S, Wegener JW, et al. Dominant role of smooth muscle L-type calcium channel Cav1. 2 for blood pressure regulation. EMBO J 2003; 22:6027-6034.
17. Ohya Y, Abe I, Fujii K, Takata Y, Fujishima M. Voltage-dependent Ca2 channels in resistance arteries from spontaneously hypertensive rats. Circ Res 1993; 73:1090-1099.
18. Lozinskaya IM, Cox RH. Effects of age on Ca2 currents in small mesenteric artery myocytes from Wistar-Kyoto and spontaneously hypertensive rats. Hypertension 1997; 29:1329-1336.
19. Cox RH, Fromme S. Expression of calcium channel subunit variants in small mesenteric arteries of WKY and SHR. Am J Hypertens 2015; doi: 10. 1093/ajh/hpv024.
20. Gui P, Wu X, Ling S, Stotz SC, Winkfein RJ, Wilson E, et al. Integrin receptor activation triggers converging regulation of Cav1. 2 calcium channels by c-Src and protein kinase A pathways. J Biol Chem 2006; 281:14015-14025.
21. Hulme JT, Lin TW, Westenbroek RE, Scheuer T, Catterall WA. Betaadrenergic regulation requires direct anchoring of PKA to cardiac CaV1. 2 channels via a leucine zipper interaction with A kinase-anchoring protein 15. Proc Natl Acad Sci USA 2003; 100:13093-13098.
22. Wu C, Li J, Bo L, Gao Q, Zhu Z, Li D, et al. High-sucrose diets in pregnancy alter angiotensin II-mediated pressor response and microvessel tone via the PKC/Cav1. 2 pathway in rat offspring. Hypertens Res 2014; 37:818-823.
23. Wang J, Thio SS, Yang SS, Yu D, Yu CY, Wong YP, et al. Splice variant specific modulation of CaV1. 2 calcium channel by galectin-1 regulates arterial constriction. Circ Res 2011; 109:1250-1258.
24. Nystoriak MA, Murakami K, Penar PL, Wellman GC. Ca(v)1. 2 splice variant with exon 9- is critical for regulation of cerebral artery diameter. Am J Physiol Heart Circ Physiol 2009; 297:H1820-H1828.
25. Earley S, Straub SV, Brayden JE. Protein kinase C regulates vascular myogenic tone through activation of TRPM4. Am J Physiol Heart Circ Physiol 2007; 292:H2613-H2622.
26. Mazzocchi G, Rebuffat P, Ziolkowska A, Rossi GP, Malendowicz LK, Nussdorfer GG. G protein receptors 7 and 8 are expressed in human adrenocortical cells, and their endogenous ligands neuropeptides B and w enhance cortisol secretion by activating adenylate cyclase-and phospholipase C-dependent signaling cascades. J Clin Endocrinol Metab 2005; 90:3466-3471.
27. Ungvari Z, Pacher P, Kecskemeti V, Papp G, Szollar L, Koller A. Increased myogenic tone in skeletal muscle arterioles of diabetic rats. Possible role of increased activity of smooth muscle Ca2channels and protein kinase C. Cardiovasc Res 1999; 43:1018-1028.
28. Ishii M, Fei H, Friedman JM. Targeted disruption of GPR7, the endogenous receptor for neuropeptides B and W, leads to metabolic defects and adult-onset obesity. Proc Natl Acad Sci USA 2003; 100:10540-10545.
29. Li H, Kentish SJ, Kritas S, Young RL, Isaacs NJ, O'Donnell TA, et al. Modulation of murine gastric vagal afferent mechanosensitivity by neuropeptide W. Acta Physiol (Oxf) 2013; 209:179-191.
30. Davare MA, Avdonin V, Hall DD, Peden EM, Burette A, Weinberg RJ, et al. A beta2 adrenergic receptor signaling complex assembled with the Ca2 channel Cav1. 2. Science 2001; 293:98-101.
31. Hulme JT, Westenbroek RE, Scheuer T, Catterall WA. Phosphorylation of serine 1928 in the distal C-terminal domain of cardiac CaV1. 2 channels during beta1-adrenergic regulation. Proc Natl Acad Sci USA 2006; 103:16574-16579.
32. Le Menuet D, Munier M, Meduri G, Viengchareun S, Lombes M. Mineralocorticoid receptor overexpression in embryonic stem cellderived cardiomyocytes increases their beating frequency. Cardiovasc Res 2010; 87:467-475.
33. Park HW, Jung H, Choi KH, Baik JH, Rhim H. Direct interaction and functional coupling between voltage-gated CaV1. 3 Ca2 channel and GABAB receptor subunit 2. FEBS Lett 2010; 584:3317-3322.
34. Yang L, Liu G, Zakharov SI, Bellinger AM, Mongillo M, Marx SO. Protein kinase G phosphorylates Cav1. 2 alpha1c and beta2 subunits. Circ Res 2007; 101:465-474.
35. Vandael DH, Mahapatra S, Calorio C, Marcantoni A, Carbone E. Cav1. 3 and Cav1. 2 channels of adrenal chromaffin cells: emerging views on cAMP/cGMP-mediated phosphorylation and role in pacemaking. Biochim Biophys Acta 2013; 1828:1608-1618.
36. Keranen LM, Dutil EM, Newton AC. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr Biol 1995; 5:1394-1403.
37. Newton AC. Protein kinase C: poised to signal. Am J Physiol Endocrinol Metab 2010; 298:E395-E402.
38. Amberg GC, Navedo MF, Nieves-Cintron M, Molkentin JD, Santana LF. Calcium sparklets regulate local and global calcium in murine arterial smooth muscle. J Physiol 2007; 579:187-201.
39. Yang L, Liu G, Zakharov SI, Morrow JP, Rybin VO, Steinberg SF, et al. Ser1928 is a common site for Cav1. 2 phosphorylation by protein kinase C isoforms. J Biol Chem 2005; 280:207-214.
40. Bayliss WM. On the local reactions of the arterial wall to changes of internal pressure. J Physiol 1902; 28:220-231.
41. 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.
42. Pratt PF, Bonnet S, Ludwig LM, Bonnet P, Rusch NJ. Upregulation of L-type Ca2 channels in mesenteric and skeletal arteries of SHR. Hypertension 2002; 40:214-219.
43. Pesic A, Madden JA, Pesic M, Rusch NJ. High blood pressure upregulates arterial L-type Ca2 channels: is membrane depolarization the signal? Circ Res 2004; 94:e97-e104.
44. Ohya Y, Tsuchihashi T, Kagiyama S, Abe I, Fujishima M. Single L-type calcium channels in smooth muscle cells from resistance arteries of spontaneously hypertensive rats. Hypertension 1998; 31:1125-1129.
45. Rainbow RD, Norman RI, Everitt DE, Brignell JL, Davies NW, Standen NB. Endothelin-I and angiotensin II inhibit arterial voltage-gated K channels through different protein kinase C isoenzymes. Cardiovasc Res 2009; 83:493-500.
46. Straub SV, Girouard H, Doetsch PE, Hannah RM, Wilkerson MK, Nelson MT. Regulation of intracerebral arteriolar tone by K(v) channels: effects of glucose and PKC. Am J Physiol Cell Physiol 2009; 297:C788-C796.
47. Yu N, Chu C, Kunitake T, Kato K, Nakazato M, Kannan H. Cardiovascular actions of central neuropeptide W in conscious rats. Regul Pept 2007; 138:82-86.
48. Pate AT, Yosten GL, Samson WK. Neuropeptide W increases mean arterial pressure as a result of behavioral arousal. Am J Physiol Regul Integr Comp Physiol 2013; 305:R804-R810.
49. Pate AT, Yosten GL, Samson WK. Compromise of endogenous neuropeptide W production abrogates the dipsogenic and pressor effects of angiotensin II in adult male rats. J Neuroendocrinol 2013; 25:1290-1297.