A bioluminescence resonance energy transfer 2 (BRET2) assay for monitoring seven transmembrane receptor and insulin receptor crosstalk

References

• Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82–C97.
   PubMed Web of Science ®Google Scholar
• Velloso LA, Folli F, Perego L, et al. The multi-faceted cross-talk between the insulin and angiotensin II signaling systems. Diabetes Metab Res Rev. 2006;22:98–107.
   PubMed Web of Science ®Google Scholar
• Pyne NJ, Pyne S. Sphingosine 1-phosphate, lysophosphatidic acid and growth factor signaling and termination. Biochim Biophys Acta. 2008;1781:467–476.
   PubMed Web of Science ®Google Scholar
• Morel Y, Gadient A, Keller U, et al. Insulin sensitivity in obese hypertensive dyslipidemic patients treated with enalapril or atenolol. J Cardiovasc Pharmacol. 1995;26:306–311.
   PubMed Web of Science ®Google Scholar
• Paolisso G, Gambardella A, Verza M, et al. Ace inhibition improves insulin-sensitivity in aged insulin-resistant hypertensive patients. J Hum Hypertens. 1992;6:175–179.
   PubMed Web of Science ®Google Scholar
• Piedrola G, Novo E, Serrano-Gotarredona J, et al. Evolution of insulin resistance in coronary artery disease patients on four different pharmacological therapies. Postgrad Med J. 1999;75:27–31.
   PubMed Web of Science ®Google Scholar
• Yusuf S, Gerstein H, Hoogwerf B, et al. Ramipril and the development of diabetes. JAMA. 2001;286:1882–1885.
   PubMed Web of Science ®Google Scholar
• Krum H, McMurray JJ, Horton E, et al. Baseline characteristics of the nateglinide and valsartan impaired glucose tolerance outcomes research (navigator) trial population: comparison with other diabetes prevention trials. Cardiovasc Ther. 2010;28:124–132.
   PubMed Web of Science ®Google Scholar
• McMurray JJ, Holman RR, Haffner SM, et al. Effect of valsartan on the incidence of diabetes and cardiovascular events. N Engl J Med. 2010;362:1477–1490.
   PubMed Web of Science ®Google Scholar
• Ahn S, Shenoy SK, Wei H, et al. Differential kinetic and spatial patterns of beta-arrestin and g protein-mediated ERK activation by the angiotensin II receptor. J Biol Chem. 2004;279:35518–35525.
   PubMed Web of Science ®Google Scholar
• Aplin M, Christensen GL, Hansen JL. Pharmacologic perspectives of functional selectivity by the angiotensin II type 1 receptor. Trends Cardiovasc Med. 2008;18:305–312.
   PubMed Web of Science ®Google Scholar
• Hansen JL, Aplin M, Hansen JT, et al. The human angiotensin AT(1) receptor supports G protein-independent extracellular signal-regulated kinase 1/2 activation and cellular proliferation. Eur J Pharmacol. 2008;590:255–263.
   PubMed Web of Science ®Google Scholar
• Avruch J. Insulin signal transduction through protein kinase cascades. Mol Cell Biochem. 1998;182:31–48.
   PubMed Web of Science ®Google Scholar
• Jensen M, De Meyts P. Molecular mechanisms of differential intracellular signaling from the insulin receptor. Vitam Horm. 2009;80:51–75.
   PubMed Web of Science ®Google Scholar
• White MF, Kahn CR. The insulin signaling system. J Biol Chem. 1994;269:1–4.
   PubMed Web of Science ®Google Scholar
• Versteyhe S, Blanquart C, Hampe C, et al. Insulin receptor substrates-5 and -6 are poor substrates for the insulin receptor. Mol Med Rep. 2010;3:189–193.
   PubMed Web of Science ®Google Scholar
• Sesti G, Federici M, Hribal ML, et al. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 2001;15:2099–2111.
   PubMed Web of Science ®Google Scholar
• White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab. 2002;283:E413–E422.
   PubMed Web of Science ®Google Scholar
• Araki E, Lipes MA, Patti ME, et al. Alternative pathway of insulin signalling in mice with targeted disruption of the IRS-1 gene. Nature. 1994;372:186–190.
   PubMed Web of Science ®Google Scholar
• Guo S, Copps KD, Dong X, et al. The IRS1 branch of the insulin signaling cascade plays a dominant role in hepatic nutrient homeostasis. Mol Cell Biol. 2009;29:5070–5083.
   PubMed Web of Science ®Google Scholar
• Withers DJ, Gutierrez JS, Towery H, et al. Disruption of IRS-2 causes type 2 diabetes in mice. Nature. 1998;391:900–904.
   PubMed Web of Science ®Google Scholar
• Lavan BE, Fantin VR, Chang ET, et al. A novel 160-kda phosphotyrosine protein in insulin-treated embryonic kidney cells is a new member of the insulin receptor substrate family. J Biol Chem. 1997;272:21403–21407.
   PubMed Web of Science ®Google Scholar
• Fantin VR, Keller SR, Lienhard GE, et al. Insulin receptor substrate 4 supports insulin- and interleukin 4-stimulated proliferation of hematopoietic cells. Biochem Biophys Res Commun. 1999;260:718–723.
   PubMed Web of Science ®Google Scholar
• Hoxhaj G, Dissanayake K, MacKintosh C. Effect of IRS4 levels on PI 3-kinase signalling. PLoS One. 2013;8:e73327.
   PubMed Web of Science ®Google Scholar
• Qu BH, Karas M, Koval A, et al. Insulin receptor substrate-4 enhances insulin-like growth factor-I-induced cell proliferation. J Biol Chem. 1999;274:31179–31184.
   PubMed Web of Science ®Google Scholar
• Carvalheira JB, Calegari VC, Zecchin HG, et al. The cross-talk between angiotensin and insulin differentially affects phosphatidylinositol 3-kinase- and mitogen-activated protein kinase-mediated signaling in rat heart: implications for insulin resistance. Endocrinology. 2003;144:5604–5614.
   PubMed Web of Science ®Google Scholar
• Diamond-Stanic MK, Henriksen EJ. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch Physiol Biochem. 2010;116:88–95.
   PubMedGoogle Scholar
• Izawa Y, Yoshizumi M, Fujita Y, et al. ERK1/2 activation by angiotensin II inhibits insulin-induced glucose uptake in vascular smooth muscle cells. Exp Cell Res. 2005;308:291–299.
   PubMed Web of Science ®Google Scholar
• Motley ED, Eguchi K, Gardner C, et al. Insulin-induced Akt activation is inhibited by angiotensin II in the vasculature through protein kinase c-alpha. Hypertension. 2003;41:775–780.
   PubMed Web of Science ®Google Scholar
• Taniyama Y, Hitomi H, Shah A, et al. Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II. Arterioscler Thromb Vasc Biol. 2005;25:1142–1147.
   PubMed Web of Science ®Google Scholar
• Folli F, Kahn CR, Hansen H, et al. Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J Clin Invest. 1997;100:2158–2169.
   PubMed Web of Science ®Google Scholar
• Kulahin N, Sanni SJ, Slaaby R, et al. A bret assay for monitoring insulin receptor interactions and ligand pharmacology. J Receptor Signal Transd Res. 2012;32:57–64.
   PubMed Web of Science ®Google Scholar
• Hansen JL, Hansen JT, Speerschneider T, et al. Lack of evidence for at1r/b2r heterodimerization in cos-7, hek293, and nih3t3 cells: how common is the at1r/b2r heterodimer? J Biol Chem. 2009;284:1831–1839.
   PubMed Web of Science ®Google Scholar
• Loening AM, Fenn TD, Wu AM, et al. Consensus guided mutagenesis of renilla luciferase yields enhanced stability and light output. Protein Eng Des Sel. 2006;19:391–400.
   PubMed Web of Science ®Google Scholar
• Poulsen H, Jorgensen R, Heding A, et al. Dimerization of adar2 is mediated by the double-stranded RNA binding domain. RNA. 2006;12:1350–1360.
   PubMed Web of Science ®Google Scholar
• Sanni SJ, Hansen JT, Bonde MM, et al. Beta-arrestin 1 and 2 stabilize the angiotensin II type I receptor in distinct high-affinity conformations. Br J Pharmacol. 2010;161:150–161.
   PubMed Web of Science ®Google Scholar
• Copps KD, White MF. Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia. 2012;55:2565–2582.
   PubMed Web of Science ®Google Scholar
• Clauser E, Curnow KM, Davies E, et al. Angiotensin II receptors: protein and gene structures, expression and potential pathological involvements. Eur J Endocrinol. 1996;134:403–411.
   PubMed Web of Science ®Google Scholar
• Johnston AP, Baker J, De Lisio M, et al. Skeletal muscle myoblasts possess a stretch-responsive local angiotensin signalling system. J Renin Angiotensin Aldosterone Syst. 2011;12:75–84.
   Google Scholar
• Serrano R, Villar M, Martinez C, et al. Differential gene expression of insulin receptor isoforms a and b and insulin receptor substrates 1, 2 and 3 in rat tissues: modulation by aging and differentiation in rat adipose tissue. J Mol Endocrinol. 2005;34:153–161.
   PubMed Web of Science ®Google Scholar
• Richey JM, Ader M, Moore D, et al. Angiotensin II induces insulin resistance independent of changes in interstitial insulin. Am J Physiol. 1999;277:E920–E926.
   PubMed Web of Science ®Google Scholar
• Wei Y, Sowers JR, Clark SE, et al. Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-kappab activation via NADPH oxidase. Am J Physiol Endocrinol Metab. 2008;294:E345–E351.
   PubMed Web of Science ®Google Scholar
• Wei Y, Whaley-Connell AT, Chen K, et al. NADPH oxidase contributes to vascular inflammation, insulin resistance, and remodeling in the transgenic (MREN2) rat. Hypertension. 2007;50:384–391.
   PubMed Web of Science ®Google Scholar
• Gotoh N, Toyoda M, Shibuya M. Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from RAS/mitogen-activated protein kinase activation. Mol Cell Biol. 1997;17:1824–1831.
   PubMed Web of Science ®Google Scholar
• Sasaoka T, Draznin B, Leitner JW, et al. Shc is the predominant signaling molecule coupling insulin receptors to activation of guanine nucleotide releasing factor and p21ras-GTP formation. J Biol Chem. 1994;269:10734–10738.
   PubMed Web of Science ®Google Scholar
• Takahashi Y, Tobe K, Kadowaki H, et al. Roles of insulin receptor substrate-1 and Shc on insulin-like growth factor I receptor signaling in early passages of cultured human fibroblasts. Endocrinology. 1997;138:741–750.
   PubMed Web of Science ®Google Scholar
• Christensen GL, Kelstrup CD, Lyngso C, et al. Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol Cell Proteomics. 2010;9:1540–1553.
   PubMed Web of Science ®Google Scholar
• Beard KM, Lu H, Ho K, et al. Bradykinin augments insulin-stimulated glucose transport in rat adipocytes via endothelial nitric oxide synthase-mediated inhibition of Jun NH2-terminal kinase. Diabetes. 2006;55:2678–2687.
   PubMed Web of Science ®Google Scholar
• Hutchinson DS, Bengtsson T. Alpha1a-adrenoceptors activate glucose uptake in l6 muscle cells through a phospholipase c-, phosphatidylinositol-3 kinase-, and atypical protein kinase c-dependent pathway. Endocrinology. 2005;146:901–912.
   PubMed Web of Science ®Google Scholar
• Jain S, Ruiz de Azua I, Lu H, et al. Chronic activation of a designer g(q)-coupled receptor improves beta cell function. J Clin Invest. 2013;123:1750–1762.
   PubMed Web of Science ®Google Scholar
• Li JH, Jain S, McMillin SM, et al. novel experimental strategy to assess the metabolic effects of selective activation of a g(q)-coupled receptor in hepatocytes in vivo. Endocrinology. 2013;154:3539–3551.
   PubMed Web of Science ®Google Scholar
• Cipolletta E, Campanile A, Santulli G, et al. The g protein coupled receptor kinase 2 plays an essential role in beta-adrenergic receptor-induced insulin resistance. Cardiovasc Res. 2009;84:407–415.
   PubMed Web of Science ®Google Scholar
• Jensen J, Gronning-Wang LM, Jebens E, et al. Adrenaline potentiates insulin-stimulated PKB activation in the rat fast-twitch epitrochlearis muscle without affecting IRS-1-associated PI 3-kinase activity. Pflugers Arch. 2008;456:969–978.
   PubMed Web of Science ®Google Scholar
• Boura-Halfon S, Zick Y. Serine kinases of insulin receptor substrate proteins. Vitam Horm. 2009;80:313–349.
   PubMed Web of Science ®Google Scholar
• Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab. 2009;296:E581–E591.
   PubMed Web of Science ®Google Scholar
• Ishizuka T, Kajita K, Natsume Y, et al. Protein kinase c (PKC) beta modulates serine phosphorylation of insulin receptor substrate-1 (IRS-1) – effect of overexpression of PKCbeta on insulin signal transduction. Endocr Res. 2004;30:287–299.
   PubMed Web of Science ®Google Scholar
• Kellerer M, Mushack J, Seffer E, et al. Protein kinase c isoforms alpha, delta and theta require insulin receptor substrate-1 to inhibit the tyrosine kinase activity of the insulin receptor in human kidney embryonic cells (HEK 293 cells). Diabetologia. 1998;41:833–838.
   PubMed Web of Science ®Google Scholar
• Lee S, Lynn EG, Kim JA, et al. Protein kinase c-zeta phosphorylates insulin receptor substrate-1, -3, and -4 but not -2: isoform specific determinants of specificity in insulin signaling. Endocrinology. 2008;149:2451–2458.
   PubMed Web of Science ®Google Scholar
• Moeschel K, Beck A, Weigert C, et al. Protein kinase c-zeta-induced phosphorylation of ser318 in insulin receptor substrate-1 (IRS-1) attenuates the interaction with the insulin receptor and the tyrosine phosphorylation of IRS-1. J Biol Chem. 2004;279:25157–25163.
   PubMed Web of Science ®Google Scholar
• Oriente F, Andreozzi F, Romano C, et al. Protein kinase c-alpha regulates insulin action and degradation by interacting with insulin receptor substrate-1 and 14-3-3 epsilon. J Biol Chem. 2005;280:40642–40649.
   PubMed Web of Science ®Google Scholar