Circulating exosomes induced by cardiac pressure overload contain functional angiotensin II type 1 receptors

Circulation

Volumn 131, Issue 24, 2015, Pages 2120-2130

  Pironti, Gianluigi ^a   Strachan, Ryan T ^a   Abraham, Dennis ^a   Mon Wei Yu, Samuel ^a   Chen, Minyong ^a   Chen, Wei ^a   Hanada, Kenji ^a   Mao, Lan ^a   Watson, Lewis J ^a   Rockman, Howard A ^a,b  

^a Cell Biology   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Beta arrestin; Exosomes; Hypertension; Receptors, angiotensin; Signal transduction

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; BETA ARRESTIN 2; G PROTEIN COUPLED RECEPTOR; RADIOLIGAND; BETA ARRESTIN; RETINA S ANTIGEN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR FUNCTION; CELL STRESS; CONTROLLED STUDY; EXOCYTOSIS; EXOSOME; HEART MUSCLE CELL; HEART VENTRICLE OVERLOAD; IN VITRO STUDY; IN VIVO STUDY; MESENTERY BLOOD VESSEL; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING ASSAY; RESISTANCE BLOOD VESSEL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; DEFICIENCY; ELECTRON MICROSCOPY; FEMALE; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; LIGATION; MALE; MECHANICAL STRESS; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; PROTEIN TRANSPORT; RADIOASSAY; RNA INTERFERENCE; ULTRASTRUCTURE; VASCULAR RESISTANCE;

ANIMALS; ARRESTINS; BLOOD PRESSURE; CONSTRICTION; EXOSOMES; FEMALE; HEK293 CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MUSCLE CELLS; MYOCYTES, CARDIAC; OSMOTIC PRESSURE; PROTEIN TRANSPORT; RADIOLIGAND ASSAY; RECEPTOR, ANGIOTENSIN, TYPE 1; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS, MECHANICAL; VASCULAR RESISTANCE;

EID: 84935449205     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.115.015687     Document Type: Article

References (44)

1. Robbins PD, Morelli AE., Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014; 14: 195-208. doi: 10.1038/nri3622.
2. Johnstone RM, Mathew A, Mason AB, Teng K., Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J Cell Physiol 1991; 147: 27-36. doi: 10.1002/jcp.1041470105.
3. Yellon DM, Davidson SM., Exosomes: nanoparticles involved in cardioprotection? Circ Res 2014; 114: 325-332. doi: 10.1161/CIRCRESAHA.113.300636.
4. Waldenström A, Ronquist G., Role of exosomes in myocardial remodeling. Circ Res 2014; 114: 315-324. doi: 10.1161/CIRCRESAHA.114.300584.
5. Février B, Raposo G., Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 2004; 16: 415-421. doi: 10.1016/j.ceb.2004.06.003.
6. Estelles A, Sperinde J, Roulon T, Aguilar B, Bonner C, LePecq JB, Delcayre A., Exosome nanovesicles displaying G protein-coupled receptors for drug discovery. Int J Nanomedicine 2007; 2: 751-760.
7. Lakkaraju A, Rodriguez-Boulan E., Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 2008; 18: 199-209. doi: 10.1016/j.tcb.2008.03.002.
8. Mederos y Schnitzler M, Storch U, Meibers S, Nurwakagari P, Breit A, Essin K, Gollasch M, Gudermann T., Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J 2008; 27: 3092-103.
9. Zou Y, Akazawa H, Qin Y, Sano M, Takano H, Minamino T, Makita N, Iwanaga K, Zhu W, Kudoh S, Toko H, Tamura K, Kihara M, Nagai T, Fukamizu A, Umemura S, Iiri T, Fujita T, Komuro I., Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat Cell Biol 2004; 6: 499-506. doi: 10.1038/ncb1137.
10. Rakesh K, Yoo B, Kim IM, Salazar N, Kim KS, Rockman HA., β-Arrestin-biased agonism of the angiotensin receptor induced by mechanical stress. Sci Signal 2010 3 ra46. doi: 10.1126/scisignal.2000769.
11. Tang W, Strachan RT, Lefkowitz RJ, Rockman HA., Allosteric modulation of beta-arrestin-biased angiotensin II type 1 receptor signaling by membrane stretch. J Biol Chem 2014; 289: 28271-28283.
12. Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, Ponimaskin E, Schmiedl A, Yin X, Mayr M, Halder R, Fischer A, Engelhardt S, Wei Y, Schober A, Fiedler J, Thum T., Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest 2014; 124: 2136-2146. doi: 10.1172/JCI70577.
13. Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJ, Zeiher AM, Scheffer MP, Frangakis AS, Yin X, Mayr M, Braun T, Urbich C, Boon RA, Dimmeler S., Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012; 14: 249-256. doi: 10.1038/ncb2441.
14. Savina A, Furlán M, Vidal M, Colombo MI., Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 2003; 278: 20083-20090. doi: 10.1074/jbc.M301642200.
15. Dragovic RA, Gardiner C, Brooks AS, Tannetta DS, Ferguson DJ, Hole P, Carr B, Redman CW, Harris AL, Dobson PJ, Harrison P, Sargent IL., Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis. Nanomedicine 2011; 7: 780-788. doi: 10.1016/j.nano.2011.04.003.
16. Strachan RT, Sun JP, Rominger DH, Violin JD, Ahn S, Rojas Bie Thomsen A, Zhu X, Kleist A, Costa T, Lefkowitz RJ., Divergent transducer-specific molecular efficacies generate biased agonism at a G protein-coupled receptor (GPCR). J Biol Chem 2014; 289: 14211-14224. doi: 10.1074/jbc.M114.548131.
17. Ito M, Oliverio MI, Mannon PJ, Best CF, Maeda N, Smithies O, Coffman TM., Regulation of blood pressure by the type 1A angiotensin II receptor gene. Proc Natl Acad Sci U S A 1995; 92: 3521-3525.
18. Conner DA, Mathier MA, Mortensen RM, Christe M, Vatner SF, Seidman CE, Seidman JG., beta-Arrestin1 knockout mice appear normal but demonstrate altered cardiac responses to beta-adrenergic stimulation. Circ Res 1997; 81: 1021-1026.
19. Walters RW, Shukla AK, Kovacs JJ, Violin JD, DeWire SM, Lam CM, Chen JR, Muehlbauer MJ, Whalen EJ, Lefkowitz RJ., β-Arrestin1 mediates nicotinic acid-induced flushing, but not its antilipolytic effect, in mice. J Clin Invest 2009; 119: 1312-1321. doi: 10.1172/JCI36806.
20. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT., Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 1999; 286: 2495-2498.
21. Chen M, Hegde A, Choi YH, Theriot BS, Premont RT, Chen W, Walker JK., Genetic deletion of beta-arrestin-2 mitigates established airway hyperresponsiveness in a murine asthma model [published online ahead of print January 8, 2015]. Am J Respir Cell Mol Biol. doi: 10.1165/rcmb.2014-0231OC. http://www.atsjournals.org/doi/abs/10.1165/rcmb.2014-0231OC?url-ver=Z39.88-2003&rfr-id=ori:rid:crossref.org&rfr-dat=cr-pub%3dpubmed#.VTVPGpOd4xI. Accessed January 8, 2015.
22. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD., Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 2001; 89: 20-25.
23. György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A, Nagy G, Falus A, Buzás EI., Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 2011; 68: 2667-2688. doi: 10.1007/s00018-011-0689-3.
24. Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JE, Gould SJ., Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 2006; 172: 923-935. doi: 10.1083/jcb.200508014.
25. Halkein J, Tabruyn SP, Ricke-Hoch M, Haghikia A, Nguyen NQ, Scherr M, Castermans K, Malvaux L, Lambert V, Thiry M, Sliwa K, Noel A, Martial JA, Hilfiker-Kleiner D, Struman I., MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J Clin Invest 2013; 123: 2143-2154. doi: 10.1172/JCI64365.
26. Shenoy SK, Lefkowitz RJ., β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 2011; 32: 521-533.
27. Ahn S, Nelson CD, Garrison TR, Miller WE, Lefkowitz RJ., Desensitization, internalization, and signaling functions of beta-arrestins demonstrated by RNA interference. Proc Natl Acad Sci U S A 2003; 100: 1740-1744. doi: 10.1073/pnas.262789099.
28. Mittelbrunn M, Sánchez-Madrid F., Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 2012; 13: 328-335. doi: 10.1038/nrm3335.
29. Villarroya-Beltri C, Baixauli F, Gutiérrez-Vázquez C, Sánchez-Madrid F, Mittelbrunn M., Sorting it out: regulation of exosome loading. Semin Cancer Biol 2014; 28: 3-13. doi: 10.1016/j.semcancer.2014.04.009.
30. Fauré J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, Kirchhoff F, Raposo G, Garin J, Sadoul R., Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 2006; 31: 642-648. doi: 10.1016/j.mcn.2005.12.003.
31. Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ, Santambrogio L., Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol 2005; 175: 2237-2243.
32. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO., Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10: 1470-1476. doi: 10.1038/ncb1800.
33. Wang X, Huang W, Liu G, Cai W, Millard RW, Wang Y, Chang J, Peng T, Fan GC., Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol 2014; 74: 139-150. doi: 10.1016/j.yjmcc.2014.05.001.
34. Rajagopal S, Rajagopal K, Lefkowitz RJ., Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nat Rev Drug Discov 2010; 9: 373-386. doi: 10.1038/nrd3024.
35. Momen-Heravi F, Balaj L, Alian S, Tigges J, Toxavidis V, Ericsson M, Distel RJ, Ivanov AR, Skog J, Kuo WP., Alternative methods for characterization of extracellular vesicles. Front Physiol 2012 3 354. doi: 10.3389/fphys.2012.00354.
36. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J., Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008; 10: 619-624. doi: 10.1038/ncb1725.
37. Little KM, Smalley DM, Harthun NL, Ley K., The plasma microparticle proteome. Semin Thromb Hemost 2010; 36: 845-856. doi: 10.1055/s-0030-1267038.
38. Barry OP, Praticò D, Savani RC, FitzGerald GA., Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 1998; 102: 136-144. doi: 10.1172/JCI2592.
39. Janowska-Wieczorek A, Majka M, Kijowski J, Baj-Krzyworzeka M, Reca R, Turner AR, Ratajczak J, Emerson SG, Kowalska MA, Ratajczak MZ., Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood 2001; 98: 3143-3149.
40. Burger D, Montezano AC, Nishigaki N, He Y, Carter A, Touyz RM., Endothelial microparticle formation by angiotensin II is mediated via Ang II receptor type I/NADPH oxidase/ Rho kinase pathways targeted to lipid rafts. Arterioscler Thromb Vasc Biol 2011; 31: 1898-1907. doi: 10.1161/ATVBAHA.110.222703.
41. Guescini M, Leo G, Genedani S, Carone C, Pederzoli F, Ciruela F, Guidolin D, Stocchi V, Mantuano M, Borroto-Escuela DO, Fuxe K, Agnati LF., Microvesicle and tunneling nanotube mediated intercellular transfer of g-protein coupled receptors in cell cultures. Exp Cell Res 2012; 318: 603-613. doi: 10.1016/j.yexcr.2012.01.005.
42. Drake MT, Shenoy SK, Lefkowitz RJ., Trafficking of G protein-coupled receptors. Circ Res 2006; 99: 570-582. doi: 10.1161/01.RES.0000242563.47507.ce.
43. Williams SK, Greener DA, Solenski NJ., Endocytosis and exocytosis of protein in capillary endothelium. J Cell Physiol 1984; 120: 157-162. doi: 10.1002/jcp.1041200208.
44. Quah BJ, Barlow VP, McPhun V, Matthaei KI, Hulett MD, Parish CR., Bystander B cells rapidly acquire antigen receptors from activated B cells by membrane transfer. Proc Natl Acad Sci U S A 2008; 105: 4259-4264. doi: 10.1073/pnas.0800259105.