Insulin augments serotonin-induced contraction via activation of the IR/PI3K/PDK1 pathway in the rat carotid artery

详细信息    查看全文

• 作者：Shun Watanabe ; Takayuki Matsumoto ; Mirai Oda…
• 关键词：Insulin receptor ; Myosin phosphatase target subunit 1 ; Phosphoinositide 3 ; kinase ; Phosphoinositide ; dependent kinase 1 ; Vasoconstriction
• 刊名：Pfl¨¹gers Archiv - European Journal of Physiology
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：468
• 期：4
• 页码：667-677
• 全文大小：807 KB
• 参考文献：1.Abe H, Yamada N, Kamata K, Kuwaki T, Shimada M, Osuga J, Shionoiri F, Yahagi N, Kadowaki T, Tamemoto H, Ishibashi S, Yazaki Y, Makuuchi M (1998) Hypertension, hypertriglyceridemia, and impaired endothelium-dependent vascular dysfunction in mice lacking insulin receptor substrate-1. J Clin Invest 101:1784–1788CrossRef PubMed PubMedCentral
  2.Alessi DR (2001) Discovery of PDK1, one of the missing links in insulin signal transduction. Colworth Medal Lecture. Biochem Soc Trans 29:1–14CrossRef PubMed
  3.Arencibia JM, Pastor-Flores D, Bauer AF, Schulze JO, Biondi RM (2013) AGC protein kinases: from structural mechanism of regulation to allosteric drug development for the treatment of human diseases. Biochim Biophys Acta 1834:1302–1321CrossRef PubMed
  4.Bender SB, Klabunde RE (2007) Altered role of smooth muscle endothelin receptors in coronary endothelin-1 and alpha1-adrenoceptor-mediated vasoconstriction in Type 2 diabetes. Am J Physiol Heart Circ Physiol 293:H2281–H2288CrossRef PubMed
  5.Bender SB, McGraw AP, Jaffe IZ, Sowers JR (2013) Mineralocorticoid receptor-mediated vascular insulin resistance: an early contributor to diabetes-related vascular disease? Diabetes 62:313–319CrossRef PubMed PubMedCentral
  6.Calleja V, Laguerre M, de Las H-MG, Parker PJ, Requejo-Isidro J, Larijani B (2014) Acute regulation of PDK1 by a complex interplay of molecular switches. Biochem Soc Trans 42:1435–1440CrossRef PubMed
  7.Cao YX, He LC, Xu CB, Luo GG, Edvinsson L (2005) Enhanced transcription of contractile 5-hydroxytryptamine 2A receptors via extracellular signal-regulated kinase 1/2 after organ culture of rat mesenteric artery. Basic Clin Pharmacol Toxicol 96:282–288CrossRef PubMed
  8.Cartier-Michaud A, Malo M, Charriere-Bertrand C, Gadea G, Anguille C, Supiramaniam A, Lesne A, Delaplace F, Hutzler G, Roux P, Lawrence DA, Barlovatz-Meimon G (2012) Matrix-bound PAI-1 supports cell blebbing via RhoA/ROCK1 signaling. PLoS One 7:e32204CrossRef PubMed PubMedCentral
  9.Chen X, Zhang Y, Wang Y, Li D, Zhang L, Wang K, Luo X, Yang Z, Wu Y, Liu J (2013) PDK1 regulates platelet activation and arterial thrombosis. Blood 121:3718–3726CrossRef PubMed
  10.Cho JY, Park J (2008) Contribution of natural inhibitors to the understanding of the PI3K/PDK1/PKB pathway in the insulin-mediated intracellular signaling cascade. Int J Mol Sci 9:2217–2230CrossRef PubMed PubMedCentral
  11.DeMarco VG, Aroor AR, Sowers JR (2014) The pathophysiology of hypertension in patients with obesity. Nat Rev Endocrinol 10:364–376CrossRef PubMed PubMedCentral
  12.Didion SP, Lynch CM, Faraci FM (2007) Cerebral vascular dysfunction in TallyHo mice: a new model of Type II diabetes. Am J Physiol Heart Circ Physiol 292:H1579–H1583CrossRef PubMed
  13.Forbes JM, Cooper ME (2013) Mechanisms of diabetic complications. Physiol Rev 93:137–188CrossRef PubMed
  14.Fraer M, Kilic F (2015) Serotonin: a different player in hypertension-associated thrombosis. Hypertension 65:942–948CrossRef PubMed
  15.Gagliardi PA, di Blasio L, Primo L (2015) PDK1: a signaling hub for cell migration and tumor invasion. Biochem Biophys Acta 1856:178–188PubMed
  16.Gamoh S, Hisa H, Yamamoto R (2013) 5-hydroxytryptamine receptors as targets for drug therapies of vascular-related diseases. Biol Pharm Bull 36:1410–1415CrossRef PubMed
  17.Goulopoulou S, Webb RC (2014) Symphony of vascular contraction: how smooth muscle lose harmony to signal increased vascular resistance in hypertension. Hypertension 63:e33–39CrossRef PubMed PubMedCentral
  18.Guo Z, Su W, Allen S, Pang H, Daugherty A, Smart E, Gong MC (2005) COX-2 up-regulation and vascular smooth muscle contractile hyperreactivity in spontaneous diabetic db/db mice. Cardiovasc Res 67:723–735CrossRef PubMed
  19.Hindie V, Stroba A, Zhang H, Lopez-Garcia LA, Idrissova L, Zeuzem S, Hirschberg D, Schaeffer F, Jorgensen TJ, Engel M, Alzari PM, Biondi RM (2009) Structure and allosteric effects of low-molecular-weight activators on the protein kinase PDK1. Nat Chem Biol 5:758–764CrossRef PubMed
  20.Ito K, Akazawa H, Tamagawa M, Furukawa K, Ogawa W, Yasuda N, Kudo Y, Liao CH, Yamamoto R, Sato T, Molkentin JD, Kasuga M, Noda T, Nakaya H, Komuro I (2009) PDK1 coordinates survival pathways and beta-adrenergic response in the heart. Proc Natl Acad Sci U S A 106:8689–8694CrossRef PubMed PubMedCentral
  21.Iwabayashi M, Taniyama Y, Sanada F, Azuma J, Iekushi K, Kusunoki H, Chatterjee A, Okayama K, Rakugi H, Morishita R (2012) Role of serotonin in angiogenesis: induction of angiogenesis by sarpogrelate via endothelial 5-HT1B/Akt/eNOS pathway in diabetic mice. Atherosclerosis 220:337–342CrossRef PubMed
  22.Kanagy NL, Webb RC (1996) Increased responsiveness and decreased expression of G proteins in deoxycorticosterone hypertension. Hypertension 27:740–745CrossRef PubMed
  23.Kaumann AJ, Levy FO (2006) 5-hydroxytryptamine receptors in the human cardiovascular system. Pharmacol Ther 111:674–706CrossRef PubMed
  24.Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904CrossRef PubMed
  25.Kobayashi T, Kaneda A, Kamata K (2003) Possible involvement of IGF-1 receptor and IGF-binding protein in insulin-induced enhancement of noradrenaline response in diabetic rat aorta. Br J Pharmacol 140:285–294CrossRef PubMed PubMedCentral
  26.Kobayashi T, Matsumoto T, Kamata K (2005) IGF-1-induced enhancement of contractile response in organ-cultured aortae from diabetic rats is mediated by sustained thromboxane A2 release from endothelial cells. J Endocrinol 186:367–376CrossRef PubMed
  27.Kobayashi T, Nogami T, Taguchi K, Matsumoto T, Kamata K (2008) Diabetic state, high plasma insulin and angiotensin II combine to augment endothelin-1-induced vasoconstriction via ETA receptors and ERK. Br J Pharmacol 155:974–983CrossRef PubMed PubMedCentral
  28.Kobayashi T, Taguchi K, Nemoto S, Nogami T, Matsumoto T, Kamata K (2009) Activation of the PDK-1/Akt/eNOS pathway involved in aortic endothelial function differs between hyperinsulinemic and insulin-deficient diabetic rats. Am J Physiol Heart Circ Physiol 297:H1767–H1775CrossRef PubMed
  29.Kobayashi T, Taguchi K, Takenouchi Y, Matsumoto T, Kamata K (2007) Insulin-induced impairment via peroxynitrite production of endothelium-dependent relaxation and sarco/endoplasmic reticulum Ca(2+)-ATPase function in aortas from diabetic rats. Free Radic Biol Med 43:431–443CrossRef PubMed
  30.Kubota T, Kubota N, Moroi M, Terauchi Y, Kobayashi T, Kamata K, Suzuki R, Tobe K, Namiki A, Aizawa S, Nagai R, Kadowaki T, Yamaguchi T (2003) Lack of insulin receptor substrate-2 causes progressive neointima formation in response to vessel injury. Circulation 107:3073–3080CrossRef PubMed
  31.Laakso M, Kuusisto J (2014) Insulin resistance and hyperglycaemia in cardiovascular disease development. Nat Rev Endocrinol 10:293–302CrossRef PubMed
  32.Luo G, Xu CB, Cao YX, Edvinsson L (2004) Transcriptional up-regulation in expression of 5-hydroxytryptamine2A and transcriptional down-regulation of angiotensin II type 1 receptors during organ culture of rat mesenteric artery. Basic Clin Pharmacol Toxicol 95:280–287CrossRef PubMed
  33.Matsumoto T, Goulopoulou S, Taguchi K, Tostes RC, Kobayashi T (2015) Constrictor prostanoids and uridine adenosine tetraphosphate: vascular mediators and therapeutic targets in hypertension and diabetes. Br J Pharmacol 172:3980–4001CrossRef PubMed
  34.Matsumoto T, Ishida K, Nakayama N, Kobayashi T, Kamata K (2009) Involvement of NO and MEK/ERK pathway in enhancement of endothelin-1-induced mesenteric artery contraction in later-stage type 2 diabetic Goto-Kakizaki rat. Am J Physiol Heart Circ Physiol 296:H1388–H1397CrossRef PubMed
  35.Matsumoto T, Kakami M, Noguchi E, Kobayashi T, Kamata K (2007) Imbalance between endothelium-derived relaxing and contracting factors in mesenteric arteries from aged OLETF rats, a model of Type 2 diabetes. Am J Physiol Heart Circ Physiol 293:H1480–H1490CrossRef PubMed
  36.Matsumoto T, Kobayashi T, Ishida K, Taguchi K, Kamata K (2010) Enhancement of mesenteric artery contraction to 5-HT depends on Rho kinase and Src kinase pathways in the ob/ob mouse model of type 2 diabetes. Br J Pharmacol 160:1092–1104CrossRef PubMed PubMedCentral
  37.Matsumoto T, Noguchi E, Ishida K, Kobayashi T, Yamada N, Kamata K (2008) Metformin normalizes endothelial function by suppressing vasoconstrictor prostanoids in mesenteric arteries from OLETF rats, a model of type 2 diabetes. Am J Physiol Heart Circ Physiol 295:H1165–H1176CrossRef PubMed
  38.Matsumoto T, Watanabe S, Kawamura R, Taguchi K, Kobayashi T (2014) Enhanced uridine adenosine tetraphosphate-induced contraction in renal artery from type 2 diabetic Goto-Kakizaki rats due to activated cyclooxygenase/thromboxane receptor axis. Pflugers Arch 466:331–342CrossRef PubMed
  39.Matsumoto T, Watanabe S, Kawamura R, Taguchi K, Kobayashi T (2014) Epigallocatechin gallate attenuates ET-1-induced contraction in carotid artery from type 2 diabetic OLETF rat at chronic stage of disease. Life Sci 118:200–205CrossRef PubMed
  40.Matsumoto T, Watanabe S, Taguchi K, Kobayashi T (2014) Mechanisms underlying increased serotonin-induced contraction in carotid arteries from chronic type 2 diabetic Goto-Kakizaki rats. Pharmacol Res 87:123–132CrossRef PubMed
  41.Muniyappa R, Montagnani M, Koh KK, Quon MJ (2007) Cardiovascular actions of insulin. Endocr Rev 28:463–491CrossRef PubMed
  42.Najafov A, Sommer EM, Axten JM, Deyoung MP, Alessi DR (2011) Characterization of GSK2334470, a novel and highly specific inhibitor of PDK1. Biochem J 433:357–369CrossRef PubMed
  43.Nakazawa T, Chiba T, Kaneko E, Yui K, Yoshida M, Shimokado K (2005) Insulin signaling in arteries prevents smooth muscle apoptosis. Arterioscler Thromb Vasc Biol 25:760–765CrossRef PubMed
  44.Nelson PM, Harrod JS, Lamping KG (2012) 5HT(2A) and 5HT(2B) receptors contribute to serotonin-induced vascular dysfunction in diabetes. Exp Diabetes Res 2012:398406CrossRef PubMed PubMedCentral
  45.Nemoto S, Matsumoto T, Taguchi K, Kobayashi T (2014) Relationships among protein tyrosine phosphatase 1B, angiotensin II, and insulin-mediated aortic responses in type 2 diabetic Goto-Kakizaki rats. Atherosclerosis 233:64–71CrossRef PubMed
  46.Nemoto S, Taguchi K, Matsumoto T, Kamata K, Kobayashi T (2012) Pravastatin normalizes ET-1-induced contraction in the aorta of type 2 diabetic OLETF rats by suppressing the KSR1/ERK complex. Am J Physiol Heart Circ Physiol 303:H893–H902CrossRef PubMed
  47.Nunes KP, Rigsby CS, Webb RC (2010) RhoA/Rho-kinase and vascular diseases: what is the link? Cell Mol Life Sci 67:3823–3836CrossRef PubMed PubMedCentral
  48.Nuno DW, Harrod JS, Lamping KG (2009) Sex-dependent differences in Rho activation contribute to contractile dysfunction in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 297:H1469–1477CrossRef PubMed
  49.Okada A, Yaguchi T, Kanno T, Gotoh A, Nakano T, Nishizaki T (2012) PDGF-D/PDGF-ββ receptor-regulated chemotaxis of malignant mesothelioma cells. Cell Physiol Biochem 29:241–250CrossRef PubMed
  50.Olivares-Reyes JA, Arellano-Plancarte A, Castillo-Hernandez JR (2009) Angiotensin II and the development of insulin resistance: implications for diabetes. Mol Cell Endocrinol 302:128–139CrossRef PubMed
  51.Ozaki H, Karaki H (2002) Organ culture as a useful method for studying the biology of blood vessels and other smooth muscle tissues. Jpn J Pharmacol 89:93–100CrossRef PubMed
  52.Paneni F, Beckman JA, Creager MA, Cosentino F (2013) Diabetes and vascular disease: pathophysiology, clinical concequences, and medical therapy: part I. Eur Heart J 34:2436–2443CrossRef PubMed PubMedCentral
  53.Porter KE, Riches K (2013) The vascular smooth muscle cell: a therapeutic target in Type 2 diabetes? Clin Sci 125:167–182CrossRef PubMed
  54.Pullen N, Dennis PB, Andjelkovic M, Dufner A, Kozma SC, Hemmings BA, Thomas S (1998) Phosphorylation and activation of p70s6k by PDK1. Science 279:707–710CrossRef PubMed
  55.Ramage AG, Villalon CM (2008) 5-hydroxytryptamine and cardiovascular regulation. Trends Pharmacol Sci 29:472–481CrossRef PubMed
  56.Sabbatini P, Korenchuk S, Rowand JL, Groy A, Liu Q, Leperi D, Atkins C, Dumble M, Yang J, Anderson K, Kruger RG, Gontarek RR, Maksimchuk KR, Suravajjala S, Lapierre RR, Shotwell JB, Wilson JW, Chamberlain SD, Rabindran SK, Kumar R (2009) GSK1838705A inhibits the insulin-like growth factor-1 receptor and anaplastic lymphoma kinase and shows antitumor activity in experimental models of human cancers. Mol Cancer Ther 8:2811–2820CrossRef PubMed
  57.Sachidanandam K, Elgebaly MM, Harris AK, Hutchinson JR, Mezzetti EM, Portik-Dobos V, Ergul A (2008) Effect of chronic and selective endothelin receptor antagonism on microvascular function in type 2 diabetes. Am J Physiol Heart Circ Physiol 294:H2743–H2749CrossRef PubMed PubMedCentral
  58.Sadowsky JD, Burlingame MA, Wolan DW, McClendon CL, Jacobson MP, Wells JA (2011) Turning a protein kinase on or off from a single allosteric site via disulfide trapping. Proc Natl Acad Sci U S A 108:6056–6061CrossRef PubMed PubMedCentral
  59.Scortegagna M, Lau E, Zhang T, Feng Y, Sereduk C, Yin H, De SK, Meeth K, Platt JT, Langdon CG, Halaban R, Pellecchia M, Davies MA, Brown K, Stern DF, Bosenberg M, Ronai ZA (2015) PDK1 and SGK3 contribute to the growth of BRAF-mutant Melanomas and are potential therapeutic targets. Cancer Res 75:1399–1412CrossRef PubMed
  60.Seok YM, Azam MA, Okamoto Y, Sato A, Yoshioka K, Maeda M, Kim I, Takuwa Y (2010) Enhanced Ca2 + −dependent activation of phosphoinositide 3-kinase class IIα isoform-Rho axis in blood vessels of spontaneously hypertensive rats. Hypertension 56:934–941CrossRef PubMed
  61.Sowers JR (2004) Insulin resistance and hypertension. Am J Physiol Heart Circ Physiol 286:H1597–H1602CrossRef PubMed
  62.Taguchi K, Matsumoto T, Kobayashi T (2015) G-protein-coupled receptor kinase 2 and endothelial dysfunction: molecular insights and pathophysiological mechanisms. J Smooth Muscle Res in press
  63.Tawaramoto K, Kotani K, Hashiramoto M, Kanda Y, Nagare T, Sakaue H, Ogawa W, Emoto N, Yanagisawa M, Noda T, Kasuka M, Kaku K (2012) Ablation of 3-phosphoinositide-dependent protein kinase 1 (PDK1) in vascular endothelial cells enhances insulin sensitivity by reducing visceral fat and suppressing angiogenesis. Mol Endocrinol 26:95–109CrossRef PubMed
  64.Toker A, Newton AC (2000) Cellular signaling: pivoting around PDK-1. Cell 103:185–188CrossRef PubMed
  65.Wang Y, Yoshioka K, Azam MA, Takuwa N, Sakurada S, Kayaba Y, Sugimoto N, Inoki I, Kimura T, Kuwaki T, Takuwa Y (2006) Class II phosphoinositide 3-kinase alpha-isoform regulates Rho, myosin phosphatase and contraction in vascular smooth muscle. Biochem J 394:581–592CrossRef PubMed PubMedCentral
  66.Watts SW, Davis RP (2011) 5-hydroxytryptamine receptors in systemic hypertension: an arterial focus. Cardiovasc Ther 29:54–67CrossRef PubMed PubMedCentral
  67.Watts SW, Morrison SF, Davis RP, Barman SM (2012) Serotonin and blood pressure regulation. Pharmacol Rev 64:359–388CrossRef PubMed PubMedCentral
  68.Weber DS, Taniyama Y, Rocic P, Seshiah PN, Dechert MA, Gerthoffer WT, Griendling KK (2004) Phosphoinositide-dependent kinase 1 and p21-activated protein kinase mediate reactive oxygen species-dependent regulation of platelet-derived growth factor-induced smooth muscle cell migration. Circ Res 94:1219–1226CrossRef PubMed
  69.Wick KL, Liu F (2001) A new molecular target of insulin action: regulating the pivotal PDK1. Curr Drug Targets Immune Endocr Metabol Disord 1:209–221CrossRef PubMed
  70.Yamada T, Katagiri H, Asano T, Tsuru H, Inukai K, Ono H, Kodama T, Kikuchi M, Oka Y (2002) Role of PDK1 in insulin-signaling pathway for glucose metabolism in 3T3-L1 adipocytes. Am J Physiol Endocrinol Metab 282:E1385–E1394CrossRef PubMed
  
• 作者单位：Shun Watanabe (1)
  Takayuki Matsumoto (1)
  Mirai Oda (1)
  Kosuke Yamada (1)
  Junya Takagi (1)
  Kumiko Taguchi (1)
  Tsuneo Kobayashi (1)
  
  1. Department of Physiology and Morphology, Institute of Medicinal Chemistry, Hoshi University, 2-4-41 Ebara, Shinagawa-ku, Tokyo, 142-8501, Japan
  
• 刊物主题：Human Physiology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1432-2013

文摘

Hyperinsulinemia associated with type 2 diabetes may contribute to the development of vascular diseases. Although we recently reported that enhanced contractile responses to serotonin (5-hydroxytryptamine, 5-HT) are observed in the arteries of type 2 diabetes models, the causative factors and detailed signaling pathways involved remain unclear. The purpose of this study was to investigate whether high insulin would be an amplifier of 5-HT-induced contraction in rat carotid arteries and whether the contraction involves phosphoinositide 3-kinase (PI3K)/3-phosphoinositide-dependent protein kinase 1 (PDK1) signaling, an insulin-mediated signaling pathway. In rat carotid arteries organ-cultured with insulin (for 24 h), (1) the contractile responses to 5-HT were significantly greater (vs. vehicle), (2) the insulin-induced enhancement of 5-HT-induced contractions was largely suppressed by inhibitors of the insulin receptor (IR) (GSK1838705A), PI3K (LY294002), and PDK1 (GSK2334470), and (3) the levels of phosphorylated forms of both PDK1 and myosin phosphatase target subunit 1 (MYPT1) were greater upon 5-HT stimulation. In addition, in rat carotid arteries organ-cultured with an activator of PDK1 (PS48), the 5-HT-induced contraction was greater, and this was suppressed by PDK1 inhibition but not PI3K inhibition. In addition, MYPT1 and PDK1 phosphorylation upon 5-HT stimulation was enhanced (vs. vehicle). These results suggest that high insulin levels amplify 5-HT-induced contraction. Moreover, the present results indicated the direct linkage between IR/PI3K/PDK1 activation and 5-HT-induced contraction in rat carotid arteries for the first time.