β-Arrestin mediates the Frank-Starling mechanism of cardiac contractility

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 50, 2016, Pages 14426-14431

  Abraham, Dennis M ^a   Davis, Robert T ^b   Warren, Chad M ^b   Mao, Lan ^a   Wolska, Beata M ^b   Solaro, R John ^b   Rockman, Howard A ^a   Semenza, Gregg L ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin II type I receptor; Cardiac function; Hemodynamics; Mechanotransduction; arrestin

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; BETA ARRESTIN 1; BETA ARRESTIN 2; CALCIUM; LOSARTAN; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ARRB1 PROTEIN, MOUSE; ARRB2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; CONFERENCE PAPER; CONTROLLED STUDY; HEART CYCLE; HEART HEMODYNAMICS; HEART MUSCLE COMPLIANCE; HEART MUSCLE CONTRACTILITY; HEART VOLUME; MOUSE; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKINNED MUSCLE FIBER; STARLING LAW; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CALCIUM SIGNALING; DEFICIENCY; DRUG EFFECTS; GENETICS; HEART CONTRACTION; IN VITRO STUDY; KNOCKOUT MOUSE; MALE; PHYSIOLOGY;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BETA-ARRESTIN 1; BETA-ARRESTIN 2; CALCIUM SIGNALING; IN VITRO TECHNIQUES; LOSARTAN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION; RECEPTOR, ANGIOTENSIN, TYPE 1; SIGNAL TRANSDUCTION;

EID: 85006062429     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1609308113     Document Type: Article

References (49)

1. Katz AM (2002) Ernest Henry Starling, his predecessors, and the "Law of the Heart." Circulation 106(23):2986-2992.
2. Adhikari BB, Regnier M, Rivera A.J., Kreutziger KL, Martyn D.A. (2004) Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling. Biophys J 87(3):1784-1794.
3. Pearson JT, et al (2007) Effects of sustained length-dependent activation on in situ cross-bridge dynamics in rat hearts. Biophys J 93(12):4319-4329.
4. + by phos-phorylating troponin I on threonine-144. J Mol Cell Cardiol 41(5):823-833.
5. + sensitivity and ATPase activity in the mouse myocardium. J Physiol 552(Pt 3):845-857.
6. Kirk JA, et al (2009) Left ventricular and myocardial function in mice expressing constitutively pseudophosphorylated cardiac troponin I. Circ Res 105(12):1232-1239.
7. Buscemi N, Foster DB, Neverova I, Van Eyk JE (2002) p21-activated kinase increases the calcium sensitivity of rat triton-skinned cardiac muscle fiber bundles via a mechanism potentially involving novel phosphorylation of troponin I. Circ Res 91(6):509-516.
8. Burkart EM, et al (2003) Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J Biol Chem 278(13):11265-11272.
9. Chen PP, Patel JR, Rybakova I.N., Walker JW, Moss R.L. (2010) Protein kinase A-induced myofilament desensitization to Ca(2+) as a result of phosphorylation of cardiac myosin-binding protein C. J Gen Physiol 136(6):615-627.
10. Sadayappan S, et al (2011) A critical function for Ser-282 in cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ Res 109(2):141-150.
11. + sensitivity of force is enhanced in failing human hearts. Cardiovasc Res 57(2): 505-514.
12. Solaro RJ (2007) Mechanisms of the Frank-Starling law of the heart: The beat goes on. Biophys J 93(12):4095-4096.
13. Kobayashi T, Solaro R.J. (2005) Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu Rev Physiol 67:39-67.
14. Reiter E, Ahn S, Shukla A.K., Lefkowitz R.J. (2012) Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu Rev Pharmacol Toxicol 52:179-197.
15. Noma T, et al (2007) Beta-arrestin-mediated beta1-adrenergic receptor trans-activation of the EGFR confers cardioprotection. J Clin Invest 117(9):2445-2458.
16. Kim KS, et al (2012) β-Arrestin-biased AT1R stimulation promotes cell survival during acute cardiac injury. Am J Physiol Heart Circ Physiol 303(8):H1001-H1010.
17. Rajagopal K, et al (2006) Beta-arrestin 2-mediated inotropic effects of the angiotensin II type 1A receptor in isolated cardiac myocytes. Proc Natl Acad Sci USA 103(44): 16284-16289.
18. Violin JD, et al (2010) Selectively engaging β-arrestins at the angiotensin II type 1 receptor reduces blood pressure and increases cardiac performance. J Pharmacol Exp Ther 335(3):572-579.
19. Rakesh K, et al (2010) Beta-arrestin-biased agonism of the angiotensin receptor induced by mechanical stress. Sci Signal 3(125):ra46.
20. Kim J, Ahn S, Rajagopal K., Lefkowitz R.J. (2009) Independent beta-arrestin 2 and Gq/ protein kinase Czeta pathways for ERK stimulated by angiotensin type 1A receptors in vascular smooth muscle cells converge on transactivation of the epidermal growth factor receptor. J Biol Chem 284(18):11953-11962.
21. Baan J, et al (1984) Continuous measurement of left ventricular volume in animals and humans by conductance catheter. Circulation 70(5):812-823.
22. Tang W, Strachan RT, Lefkowitz R.J., Rockman H.A. (2014) Allosteric modulation of β-arrestin-biased angiotensin II type 1 receptor signaling by membrane stretch. J Biol Chem 289(41):28271-28283.
23. Noland TA, Jr, et al. (1995) Cardiac troponin I mutants: Phosphorylation by protein kinases C and A and regulation of Ca(2+)-stimulated MgATPase of reconstituted actomyosin S-1. J Biol Chem 270(43):25445-25454.
24. Abedi H, Rozengurt E, Zachary I. (1998) Rapid activation of the novel serine/threonine protein kinase, protein kinase D by phorbol esters, angiotensin II and PDGF-BB in vascular smooth muscle cells. FEBS Lett 427(2):209-212.
25. Andersen GO, et al (2002) Alpha(1)-AR-induced positive inotropic response in heart is dependent on myosin light chain phosphorylation. Am J Physiol Heart Circ Physiol 283(4):H1471-H1480.
26. + sensitivity in ventricular myocytes. Circ Res 100(6):864-873.
27. Hinken AC, et al (2012) Protein kinase C depresses cardiac myocyte power output and attenuates myofilament responses induced by protein kinase A. J Muscle Res Cell Motil 33(6):439-448.
28. Rajagopal S, Rajagopal K, Lefkowitz R.J. (2010) Teaching old receptors new tricks: Biasing seven-transmembrane receptors. Nat Rev Drug Discov 9(5):373-386.
29. Arteaga GM, Palmiter KA, Leiden J.M., Solaro R.J. (2000) Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol 526(Pt 3):541-549.
30. Tachampa K, Wang H, Farman G.P., de Tombe PP (2007) Cardiac troponin I threonine 144: Role in myofilament length-dependent activation. Circ Res 101(11):1081-1083.
31. + activation of cardiac myofilaments and the end-systolic pressure-volume relation. J Muscle Res Cell Motil 28(7-8):415-419.
32. Mamidi R, Gresham KS, Stelzer J.E. (2014) Length-dependent changes in contractile dynamics are blunted due to cardiac myosin binding protein-C ablation. Front Physiol 5:461.
33. Fukuda N, Granzier H.L. (2005) Titin/connectin-based modulation of the Frank-Starling mechanism of the heart. J Muscle Res Cell Motil 26(6-8):319-323.
34. Hanft LM, Greaser ML, McDonald K.S. (2014) Titin-mediated control of cardiac myo-fibrillar function. Arch Biochem Biophys 552-553:83-91.
35. Kirk JA, et al (2014) Cardiac resynchronization sensitizes the sarcomere to calcium by reactivating GSK-3β. J Clin Invest 124(1):129-138.
36. Pyle WG, Solaro R.J. (2004) At the crossroads of myocardial signaling: The role of Z-discs in intracellular signaling and cardiac function. Circ Res 94(3):296-305.
37. Pernigo S, et al (2010) Structural insight into M-band assembly and mechanics from the titin-obscurin-like-1 complex. Proc Natl Acad Sci USA 107(7):2908-2913.
38. Yasuda N, et al (2008) Conformational switch of angiotensin II type 1 receptor underlying mechanical stress-induced activation. EMBO Rep 9(2):179-186.
39. Cingolani HE, Pérez NG, Cingolani O.H., Ennis I.L. (2013) The Anrep effect: 100 years later. Am J Physiol Heart Circ Physiol 304(2):H175-H182.
40. von Anrep G (1912) On the part played by the suprarenals in the normal vascular reactions of the body. J Physiol 45(5):307-317.
41. + exchange after myocardial stretch: Underlying mechanism of the slow force response. Circ Res 88(4):376-382.
42. Villa-Abrille M.C., et al (2010) The Anrep effect requires transactivation of the epidermal growth factor receptor. J Physiol 588(Pt 9):1579-1590.
43. Granger CB, et al; CHARM Investigators and Committees (2003) Effects of cande-sartan in patients with chronic heart failure and reduced left-ventricular systolic function intolerant to angiotensin-converting-enzyme inhibitors: The CHARM-Alternative trial. Lancet 362 (9386):772-776.
44. Cheung BM, Cheung GT, Lauder I.J., Lau CP, Kumana C.R. (2006) Meta-analysis of large outcome trials of angiotensin receptor blockers in hypertension. J Hum Hypertens 20(1):37-43.
45. Strauss MH, Hall A.S. (2006) Angiotensin receptor blockers may increase risk of myo-cardial infarction: Unraveling the ARB-MI paradox. Circulation 114(8):838-854.
46. Monasky MM, et al (2013) The β-arrestin-biased ligand TRV120023 inhibits angio-tensin II-induced cardiac hypertrophy while preserving enhanced myofilament response to calcium. Am J Physiol Heart Circ Physiol 305(6):H856-H866.
47. Layland J, et al (2005) Protection against endotoxemia-induced contractile dysfunction in mice with cardiac-specific expression of slow skeletal troponin I. FASEB J 19(9): 1137-1139.
48. Warren CM, et al (2008) Use of 2-D DIGE analysis reveals altered phosphorylation in a tropomyosin mutant (Glu54Lys) linked to dilated cardiomyopathy. Proteomics 8(1): 100-105.
49. Warren CM, Krzesinski PR, Greaser M.L. (2003) Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis 24(11):1695-1702.