Novel players in cardioprotection: Insulin like growth factor-1, angiotensin-(1-7) and angiotensin-(1-9)

Pharmacological Research

Volumn 101, Issue , 2015, Pages 41-55

  Westermeier, Francisco ^a   Bustamante, Mario ^a   Pavez, Mario ^a   García, Lorena ^a   Chiong, Mario ^a   Ocaranza, María Paz ^b   Lavandero, Sergio ^a,c  

^a UNIVERSITY OF CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Angiotensin (17); Angiotensin (19); Cardioprotection; Cardiovascular diseases; Growth factor; Insulin like growth factor 1; Renin angiotensin system

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN[1-7]; ANGIOTENSIN[1-9]; PROTECTIVE AGENT; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANGIOTENSIN I (1-9); CARDIOVASCULAR AGENT; G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

BINDING AFFINITY; CARDIOMYOPATHY; CONGESTIVE HEART FAILURE; DRUG EFFECT; HEART DISEASE; HEART FAILURE; HEART INFARCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; ANIMAL; BIOLOGICAL MODEL; CARDIOVASCULAR DISEASES; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; DRUG EFFECTS; PATHOPHYSIOLOGY; PHYSIOLOGY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM;

ANGIOTENSIN I; ANIMALS; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CARDIOVASCULAR SYSTEM; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MODELS, CARDIOVASCULAR; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; RECEPTOR, ANGIOTENSIN, TYPE 2; RECEPTOR, IGF TYPE 1; RECEPTORS, G-PROTEIN-COUPLED; RENIN-ANGIOTENSIN SYSTEM; SIGNAL TRANSDUCTION;

EID: 84945445487     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.06.018     Document Type: Review

References (210)

1. WHO. www.who.int/gho/ncd/en/index.html Global Health Observatory (GHO), 2013.
2. K.K. Proia, A.B. Thota, G.J. Njie, R.K. Finnie, D.P. Hopkins, Q. Mukhtar, N.P. Pronk, D. Zeigler, T.E. Kottke, K.J. Rask, D.T. Lackland, J.F. Brooks, L.T. Braun, and T. Cooksey Team-based care and improved blood pressure control: a community guide systematic review Am. J. Prev. Med. 47 2014 86 99
3. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, M.J. Blaha, S. Dai, E.S. Ford, C.S. Fox, S. Franco, H.J. Fullerton, C. Gillespie, S.M. Hailpern, J.A. Heit, V.J. Howard, M.D. Huffman, S.E. Judd, B.M. Kissela, S.J. Kittner, D.T. Lackland, J.H. Lichtman, L.D. Lisabeth, R.H. Mackey, D.J. Magid, G.M. Marcus, A. Marelli, D.B. Matchar, D.K. McGuire, E.R. Mohler 3rd, C.S. Moy, M.E. Mussolino, R.W. Neumar, G. Nichol, D.K. Pandey, N.P. Paynter, M.J. Reeves, P.D. Sorlie, J. Stein, A. Towfighi, T.N. Turan, S.S. Virani, N.D. Wong, D. Woo, and M.B. Turner Heart disease and stroke statistics - 2014 update: a report from the American Heart Association Circulation 129 2014 e28 e292
4. C.M. Lawes, H. Vander, S. oorn, and A. Rodgers Global burden of blood-pressure-related disease, 2001 Lancet 371 2008 1513 1518
5. D. Susic, and E.D. Frohlich Hypertensive cardiovascular and renal disease and target organ damage: lessons from animal models Cardiorenal Med. 1 2011 139 146
6. A.V. Chobanian, G.L. Bakris, H.R. Black, W.C. Cushman, L.A. Green, J.L.J. Izzo, D.W. Jones, B.J. Materson, S. Oparil, J.T.J. Wright, and E.J. Roccella Seventh report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure Hypertension 42 2003 1206 1252
7. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, W.B. Borden, D.M. Bravata, S. Dai, E.S. Ford, C.S. Fox, S. Franco, H.J. Fullerton, C. Gillespie, S.M. Hailpern, J.A. Heit, V.J. Howard, M.D. Huffman, B.M. Kissela, S.J. Kittner, D.T. Lackland, J.H. Lichtman, L.D. Lisabeth, D. Magid, G.M. Marcus, A. Marelli, D.B. Matchar, D.K. McGuire, E.R. Mohler, C.S. Moy, M.E. Mussolino, G. Nichol, N.P. Paynter, P.J. Schreiner, P.D. Sorlie, J. Stein, T.N. Turan, S.S. Virani, N.D. Wong, D. Woo, and M.B. Turner Heart disease and stroke statistics-2013 update: a report from the American Heart Association Circulation 127 2013 e6 e245
8. A.S. Greenstein, A. Price, K. Sonoyama, A. Paisley, K. Khavandi, S. Withers, L. Shaw, O. Paniagua, R.A. Malik, and A.M. Heagerty Eutrophic remodeling of small arteries in type 1 diabetes mellitus is enabled by metabolic control: a 10-year follow-up study Hypertension 54 2009 134 141
9. M. De, J.G. ey, P.M. Schiffers, R.H. Hilgers, and M.M. Sanders Toward functional genomics of flow-induced outward remodeling of resistance arteries Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1022 H1027
10. K. Sonoyama, A. Greenstein, A. Price, K. Khavandi, and T. Heagerty Vascular remodeling: implications for small artery function and target organ damage Ther. Adv. Cardiovasc. Dis. 1 2007 129 137
11. D. Rizzoni, E. Porteri, G. Bettoni, A. Piccoli, M. Castellano, M.L. Muiesan, G. Pasini, D. Guelfi, and E.A. Rosei Effects of candesartan cilexetil and enalapril on structural alterations and endothelial function in small resistance arteries of spontaneously hypertensive rats J. Cardiovasc. Pharmacol. 32 1998 798 806
12. D. Rizzoni, E. Porteri, A. Piccoli, M. Castellano, G. Bettoni, M.L. Muiesan, G. Pasini, D. Guelfi, M.J. Mulvany, R. Agabiti, and E. osei Effects of losartan and enalapril on small artery structure in hypertensive rats Hypertension 32 1998 305 310
13. N.K. Thybo, N. Stephens, A. Cooper, C. Aalkjaer, A.M. Heagerty, and M.J. Mulvany Effect of antihypertensive treatment on small arteries of patients with previously untreated essential hypertension Hypertension 25 1995 474 481
14. E.L. Schiffrin, J.B. Park, H.D. Intengan, and R.M. Touyz Correction of arterial structure and endothelial dysfunction in human essential hypertension by the angiotensin receptor antagonist losartan Circulation 101 2000 1653 1659
15. E. Porteri, D. Rizzoni, A. Piccoli, M. Castellano, G. Bettoni, M.L. Muiesan, G. Pasini, D. Guelfi, R. Zulli, and E.A. Rosei Effects of hypotensive and non-hypotensive doses of manidipine on structure, responses to endothelin-1 and ICAM-1 production in mesenteric small resistance arteries of spontaneously hypertensive rats Blood Pressure 7 1998 324 330
16. J.N. Cohn, R. Ferrari, and N. Sharpe Cardiac remodeling-concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an international forum on cardiac remodeling J. Am. Coll. Cardiol. 35 2000 569 582
17. G.W. Dorn, R. 2nd, J. obbins, and P.H. Sugden Phenotyping hypertrophy: eschew obfuscation Circ. Res. 92 2003 1171 1175
18. R. Troncoso, C. Ibarra, J.M. Vicencio, E. Jaimovich, and S. Lavandero New insights into IGF-1 signaling in the heart Trends Endocrinol. Metab. 25 2014 128 137
19. L.H. Opie, P.J. Commerford, B.J. Gersh, and M.A. Pfeffer Controversies in ventricular remodelling Lancet 367 2006 356 367
20. H.D. Intengan, and E.L. Schiffrin Structure and mechanical properties of resistance arteries in hypertension: role of adhesion molecules and extracellular matrix determinants Hypertension 36 2000 312 318
21. M.J. Davies A macro and micro view of coronary vascular insult in ischemic heart disease Circulation 82 1990 II38 46
22. M.P. Ocaranza, L. Michea, M. Chiong, C.F. Lagos, S. Lavandero, and J.E. Jalil Recent insights and therapeutic perspectives of angiotensin-(1-9) in the cardiovascular system Clin. Sci. (Lond.) 127 2014 549 557
23. M. De, P. eyts, and J. Whittaker Structural biology of insulin and IGF receptors: implications for drug design Nat. Rev. Drug Discovery 1 2002 769 783
24. A. Colao The GH-IGF-I axis and the cardiovascular system: clinical implications Clin. Endocrinol. (Oxf) 69 2008 347 358
25. J.A. Janssen, and A.J. Varewijck IGF-IR targeted therapy: past, present and future Front. Endocrinol. (Lausanne) 5 2014 224
26. S. Watanabe, T. Tamura, K. Ono, H. Horiuchi, T. Kimura, T. Kita, and Y. Furukawa Insulin-like growth factor axis (insulin-like growth factor-I/insulin-like growth factor-binding protein-3) as a prognostic predictor of heart failure: association with adiponectin Eur. J. Heart Fail 12 2010 1214 1222
27. A. Ullrich, A. Gray, A.W. Tam, T. Yang-Feng, M. Tsubokawa, C. Collins, W. Henzel, T. Le Bon, S. Kathuria, E. Chen, and et al. Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity EMBO J. 5 1986 2503 2512
28. A. Belfiore, F. Frasca, G. Pandini, L. Sciacca, and R. Vigneri Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease Endocr. Rev. 30 2009 586 623
29. T.E. Adams, V.C. Epa, T.P. Garrett, and C.W. Ward Structure and function of the type 1 insulin-like growth factor receptor Cell. Mol. Life Sci. 57 2000 1050 1093
30. A.J. Varewijck, and J.A. Janssen Insulin and its analogues and their affinities for the IGF1 receptor Endocr. Relat. Cancer 19 2012 F63 F75
31. R. Slaaby, L. Schaffer, I. Lautrup-Larsen, A.S. Andersen, A.C. Shaw, I.S. Mathiasen, and J. Brandt Hybrid receptors formed by insulin receptor (IR) and insulin-like growth factor I receptor (IGF-IR) have low insulin and high IGF-1 affinity irrespective of the IR splice variant J. Biol. Chem. 281 2006 25869 25874
32. F. Morgillo, J.K. Woo, E.S. Kim, W.K. Hong, and H.Y. Lee Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib Cancer Res. 66 2006 10100 10111
33. J. van der Veeken, S. Oliveira, R.M. Schiffelers, G. Storm, P.M. van Bergen En Henegouwen, and R.C. Roovers Crosstalk between epidermal growth factor receptor- and insulin-like growth factor-1 receptor signaling: implications for cancer therapy Curr. Cancer Drug Targets 9 2009 748 760
34. S. Benyoucef, K.H. Surinya, D. Hadaschik, and K. Siddle Characterization of insulin/IGF hybrid receptors: contributions of the insulin receptor L2 and Fn1 domains and the alternatively spliced exon 11 sequence to ligand binding and receptor activation Biochem. J. 403 2007 603 613
35. G. Pandini, F. Frasca, R. Mineo, L. Sciacca, R. Vigneri, and A. Belfiore Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved J. Biol. Chem. 277 2002 39684 39695
36. L. Sciacca, M.F. Cassarino, M. Genua, G. Pandini, R. Le Moli, S. Squatrito, and R. Vigneri Insulin analogues differently activate insulin receptor isoforms and post-receptor signalling Diabetologia 53 2010 1743 1753
37. M.R. Sommerfeld, G. Muller, G. Tschank, G. Seipke, P. Habermann, R. Kurrle, and N. Tennagels In vitro metabolic and mitogenic signaling of insulin glargine and its metabolites PLoS One 5 2010 e9540
38. C.W. Ward, T.P. Garrett, N.M. McKern, M. Lou, L.J. Cosgrove, L.G. Sparrow, M.J. Frenkel, P.A. Hoyne, T.C. Elleman, T.E. Adams, G.O. Lovrecz, L.J. Lawrence, and P.A. Tulloch The three dimensional structure of the type I insulin-like growth factor receptor Mol. Pathol. 54 2001 125 132
39. J. Kim, A.R. Wende, S. Sena, H.A. Theobald, J. Soto, C. Sloan, B.E. Wayment, S.E. Litwin, M. Holzenberger, D. LeRoith, and E.D. Abel Insulin-like growth factor I receptor signaling is required for exercise-induced cardiac hypertrophy Mol. Endocrinol. 22 2008 2531 2543
40. J.R. McMullen, T. Shioi, W.Y. Huang, L. Zhang, O. Tarnavski, E. Bisping, M. Schinke, S. Kong, M.C. Sherwood, J. Brown, L. Riggi, P.M. Kang, and S. Izumo The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway J. Biol. Chem. 279 2004 4782 4793
41. R. Foncea, A. Galvez, V. Perez, M.P. Morales, A. Calixto, J. Melendez, F. Gonzalez-Jara, G. Diaz-Araya, M. Sapag-Hagar, P.H. Sugden, D. LeRoith, and S. Lavandero Extracellular regulated kinase, but not protein kinase C, is an antiapoptotic signal of insulin-like growth factor-1 on cultured cardiac myocytes Biochem. Biophys. Res. Commun. 273 2000 736 744
42. Y.C. Kim, and K.L. Guan mTOR: a pharmacologic target for autophagy regulation J. Clin. Invest. 125 2015 25 32
43. S. Lavandero, M. Chiong, B.A. Rothermel, and J.A. Hill Autophagy in cardiovascular biology J. Clin. Invest. 125 2015 55 64
44. R. Troncoso, J.M. Vicencio, V. Parra, A. Nemchenko, Y. Kawashima, C. Del, A. ampo, B. Toro, P.K. Battiprolu, P. Aranguiz, M. Chiong, S. Yakar, T.G. Gillette, J.A. Hill, E.D. Abel, D. Leroith, and S. Lavandero Energy-preserving effects of IGF-1 antagonize starvation-induced cardiac autophagy Cardiovasc. Res. 93 2012 320 329
45. R. Troncoso, J. Diaz-Elizondo, S.P. Espinoza, M.F. Navarro-Marquez, A.P. Oyarzun, J.A. Riquelme, I. Garcia-Carvajal, G. Diaz-Araya, L. Garcia, J.A. Hill, and S. Lavandero Regulation of cardiac autophagy by insulin-like growth factor 1 IUBMB Life 65 2013 593 601
46. A.J. Muslin Akt2: a critical regulator of cardiomyocyte survival and metabolism Pediatr. Cardiol. 32 2011 317 322
47. V. Parra, H.E. Verdejo, M. Iglewski, A. Del Campo, R. Troncoso, D. Jones, Y. Zhu, J. Kuzmicic, C. Pennanen, C. Lopez-Crisosto, F. Jana, J. Ferreira, E. Noguera, M. Chiong, D.A. Bernlohr, A. Klip, J.A. Hill, B.A. Rothermel, E.D. Abel, A. Zorzano, and S. Lavandero Insulin stimulates mitochondrial fusion and function in cardiomyocytes via the Akt-mTOR-NFkappaB-Opa-1 signaling pathway Diabetes 63 2014 75 88
48. A. Abbas, H. Imrie, H. Viswambharan, P. Sukumar, A. Rajwani, R.M. Cubbon, M. Gage, J. Smith, S. Galloway, N. Yuldeshava, M. Kahn, S. Xuan, P.J. Grant, K.M. Channon, D.J. Beech, S.B. Wheatcroft, and M.T. Kearney The insulin-like growth factor-1 receptor is a negative regulator of nitric oxide bioavailability and insulin sensitivity in the endothelium Diabetes 60 2011 2169 2178
49. H. Imrie, H. Viswambharan, P. Sukumar, A. Abbas, R.M. Cubbon, N. Yuldasheva, M. Gage, J. Smith, S. Galloway, A. Skromna, S.T. Rashid, T.S. Futers, S. Xuan, V.K. Gatenby, P.J. Grant, K.M. Channon, D.J. Beech, S.B. Wheatcroft, and M.T. Kearney Novel role of the IGF-1 receptor in endothelial function and repair: studies in endothelium-targeted IGF-1 receptor transgenic mice Diabetes 61 2012 2359 2368
50. H. Cai, and D.G. Harrison Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress Circ. Res. 87 2000 840 844
51. V.K. Gatenby, H. Imrie, and M. Kearney The IGF-1 receptor and regulation of nitric oxide bioavailability and insulin signalling in the endothelium Pflugers Arch. 465 2013 1065 1074
52. H. Tsukahara, D.V. Gordienko, B. Tonshoff, M.C. Gelato, and M.S. Goligorsky Direct demonstration of insulin-like growth factor-I-induced nitric oxide production by endothelial cells Kidney Int. 45 1994 598 604
53. R. Muniyappa, M.F. Walsh, J.S. Rangi, R.M. Zayas, P.R. Standley, J.L. Ram, and J.R. Sowers Insulin like growth factor 1 increases vascular smooth muscle nitric oxide production Life Sci. 61 1997 925 931
54. G. Zeng, and M.J. Quon Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells J. Clin. Invest. 98 1996 894 898
55. S. Dimmeler, I. Fleming, B. Fisslthaler, C. Hermann, R. Busse, and A.M. Zeiher Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation Nature 399 1999 601 605
56. M.A. Potenza, F. Addabbo, and M. Montagnani Vascular actions of insulin with implications for endothelial dysfunction Am. J. Physiol. Endocrinol. Metab. 297 2009 E568 E577
57. S.Y. Shai, S. Sukhanov, Y. Higashi, C. Vaughn, C.J. Rosen, and P. Delafontaine Low circulating insulin-like growth factor I increases atherosclerosis in ApoE-deficient mice Am. J. Physiol. Heart Circ. Physiol. 300 2011 H1898 H1906
58. J. Wang, A. Razuvaev, L. Folkersen, E. Hedin, J. Roy, K. Brismar, and U. Hedin The expression of IGFs and IGF binding proteins in human carotid atherosclerosis, and the possible role of IGF binding protein-1 in the regulation of smooth muscle cell proliferation Atherosclerosis 220 2012 102 109
59. S. Dalle, W. Ricketts, T. Imamura, P. Vollenweider, and J.M. Olefsky Insulin and insulin-like growth factor I receptors utilize different G protein signaling components J. Biol. Chem. 276 2001 15688 15695
60. H. Hallak, A.E. Seiler, J.S. Green, B.N. Ross, and R. Rubin Association of heterotrimeric G(i) with the insulin-like growth factor-I receptor. Release of G(betagamma) subunits upon receptor activation J. Biol. Chem. 275 2000 2255 2258
61. J.F. Kuemmerle, and K.S. Murthy Coupling of the insulin-like growth factor-I receptor tyrosine kinase to Gi2 in human intestinal smooth muscle: Gbetagamma -dependent mitogen-activated protein kinase activation and growth J. Biol. Chem. 276 2001 7187 7194
62. L.M. Luttrell, T. van Biesen, B.E. Hawes, W.J. Koch, K. Touhara, and R.J. Lefkowitz G beta gamma subunits mediate mitogen-activated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor J. Biol. Chem. 270 1995 16495 16498
63. R. Perrault, and P. Zahradka Identification of novel signalling roles and targets for G(alpha) and G(betagamma) downstream of the insulin-like growth factor 1 receptor in vascular smooth muscle cells Biochem. J. 450 2013 209 219
64. C. Ibarra, J.M. Vicencio, M. Estrada, Y. Lin, P. Rocco, P. Rebellato, J.P. Munoz, J. Garcia-Prieto, A.F. Quest, M. Chiong, S.M. Davidson, I. Bulatovic, K.H. Grinnemo, O. Larsson, G. Szabadkai, P. Uhlen, E. Jaimovich, and S. Lavandero Local control of nuclear calcium signaling in cardiac myocytes by perinuclear microdomains of sarcolemmal insulin-like growth factor 1 receptors Circ. Res. 112 2013 236 245
65. C. Ibarra, M. Estrada, L. Carrasco, M. Chiong, J.L. Liberona, C. Cardenas, G. Diaz-Araya, E. Jaimovich, and S. Lavandero Insulin-like growth factor-1 induces an inositol 1,4,5-trisphosphate-dependent increase in nuclear and cytosolic calcium in cultured rat cardiac myocytes J. Biol. Chem. 279 2004 7554 7565
66. L. Carrasco, P. Cea, P. Rocco, D. Pena-Oyarzun, P. Rivera-Mejias, C. Sotomayor-Flores, C. Quiroga, A. Criollo, C. Ibarra, M. Chiong, and S. Lavandero Role of heterotrimeric G protein and calcium in cardiomyocyte hypertrophy induced by IGF-1 J. Cell. Biochem. 115 2014 712 720
67. H. Ito, M. Hiroe, Y. Hirata, M. Tsujino, S. Adachi, M. Shichiri, A. Koike, A. Nogami, and F. Marumo Insulin-like growth factor-I induces hypertrophy with enhanced expression of muscle specific genes in cultured rat cardiomyocytes Circulation 87 1993 1715 1721
68. C. Crocini, R. Coppini, C. Ferrantini, P. Yan, L.M. Loew, C. Tesi, E. Cerbai, C. Poggesi, F.S. Pavone, and L. Sacconi Defects in T-tubular electrical activity underlie local alterations of calcium release in heart failure Proc. Natl. Acad. Sci. U. S. A. 111 2014 15196 15201
69. D.J. Crossman, A.A. Young, P.N. Ruygrok, G.P. Nason, D. Baddelely, C. Soeller, and M.B. Cannell T-tubule disease: relationship between t-tubule organization and regional contractile performance in human dilated cardiomyopathy J. Mol. Cell. Cardiol. 84 2015 170 178
70. S. Wei, A. Guo, B. Chen, W. Kutschke, Y.P. Xie, K. Zimmerman, R.M. Weiss, M.E. Anderson, H. Cheng, and L.S. Song T-tubule remodeling during transition from hypertrophy to heart failure Circ. Res. 107 2010 520 531
71. G. Takemura, M. Kanoh, S. Minatoguchi, and H. Fujiwara Cardiomyocyte apoptosis in the failing heart-a critical review from definition and classification of cell death Int. J. Cardiol. 167 2013 2373 2386
72. Z. Ungvari, and A. Csiszar The emerging role of IGF-1 deficiency in cardiovascular aging: recent advances J. Gerontol. A Biol. Sci. Med. Sci. 67 2012 599 610
73. J. Guevara-Aguirre, P. Balasubramanian, M. Guevara-Aguirre, M. Wei, F. Madia, C.W. Cheng, D. Hwang, A. Martin-Montalvo, J. Saavedra, S. Ingles, R. de Cabo, P. Cohen, and V.D. Longo Growth hormone receptor deficiency is associated with a major reduction in pro-aging signaling, cancer, and diabetes in humans Sci. Transl. Med. 3 2011 70ra13
74. M. Scheinowitz, M.S. Feinberg, and Z. Laron IGF-I replacement therapy in children with congenital IGF-I deficiency (Laron syndrome) maintains heart dimension and function Growth Horm. IGF Res. 19 2009 280 282
75. L. Groban, M. Lin, K.A. Kassik, R.L. Ingram, and W.E. Sonntag Early-onset growth hormone deficiency results in diastolic dysfunction in adult-life and is prevented by growth hormone supplementation Growth Horm. IGF Res. 21 2011 81 88
76. F. Feihl, L. Liaudet, B.I. Levy, and B. Waeber Hypertension and microvascular remodelling Cardiovasc. Res. 78 2008 274 285
77. M. Scharin Tang, B. Redfors, M. Lindbom, J. Svensson, T. Ramunddal, C. Ohlsson, Y. Shao, and E. Omerovic Importance of circulating IGF-1 for normal cardiac morphology, function and post infarction remodeling Growth Horm. IGF Res. 22 2012 206 211
78. R. Malaguarnera, and A. Belfiore The emerging role of insulin and insulin-like growth factor signaling in cancer stem cells Front. Endocrinol. (Lausanne) 5 2014 10
79. E.J. Gallagher, and D. LeRoith The proliferating role of insulin and insulin-like growth factors in cancer Trends Endocrinol. Metab. 21 2010 610 618
80. M. Vinciguerra, M.P. Santini, W.C. Claycomb, A.G. Ladurner, and N. Rosenthal Local IGF-1 isoform protects cardiomyocytes from hypertrophic and oxidative stresses via SirT1 activity Aging (Albany NY) 2 2010 43 62
81. M. Vinciguerra, M.P. Santini, C. Martinez, V. Pazienza, W.C. Claycomb, A. Giuliani, and N. Rosenthal mIGF-1/JNK1/SirT1 signaling confers protection against oxidative stress in the heart Aging Cell 11 2012 139 149
82. K. Huynh, J.R. McMullen, T.L. Julius, J.W. Tan, J.E. Love, N. Cemerlang, H. Kiriazis, X.J. Du, and R.H. Ritchie Cardiac-specific IGF-1 receptor transgenic expression protects against cardiac fibrosis and diastolic dysfunction in a mouse model of diabetic cardiomyopathy Diabetes 59 2010 1512 1520
83. Y. Zhang, M. Yuan, K.M. Bradley, F. Dong, P. Anversa, and J. Ren Insulin-like growth factor 1 alleviates high-fat diet-induced myocardial contractile dysfunction: role of insulin signaling and mitochondrial function Hypertension 59 2012 680 693
84. N.S. Freestone, S. Ribaric, and W.T. Mason The effect of insulin-like growth factor-1 on adult rat cardiac contractility Mol. Cell. Biochem. 163-164 1996 223 229
85. S. Kinugawa, H. Tsutsui, T. Ide, R. Nakamura, K. Arimura, K. Egashira, and A. Takeshita Positive inotropic effect of insulin-like growth factor-1 on normal and failing cardiac myocytes Cardiovasc. Res. 43 1999 157 164
86. S.J. Kim, M. Abdellatif, S. Koul, and G.J. Crystal Chronic treatment with insulin-like growth factor I enhances myocyte contraction by upregulation of Akt-SERCA2a signaling pathway Am. J. Physiol. Heart Circ. Physiol. 295 2008 H130 H135
87. 2+ in myocyte contractile dysfunction in heart failure Cardiovasc. Res. 44 1999 398 406
88. U.M. Steckelings, and T. Unger Angiotensin II type 2 receptor agonists-where should they be applied Expert Opin. Invest. Drugs 21 2012 763 766
89. D. Mozaffarian, E.J. Benjamin, A.S. Go, D.K. Arnett, M.J. Blaha, M. Cushman, S. de Ferranti, J.P. Despres, H.J. Fullerton, V.J. Howard, M.D. Huffman, S.E. Judd, B.M. Kissela, D.T. Lackland, J.H. Lichtman, L.D. Lisabeth, S. Liu, R.H. Mackey, D.B. Matchar, D.K. McGuire, E.R. Mohler 3rd, C.S. Moy, P. Muntner, M.E. Mussolino, K. Nasir, R.W. Neumar, G. Nichol, L. Palaniappan, D.K. Pandey, M.J. Reeves, C.J. Rodriguez, P.D. Sorlie, J. Stein, A. Towfighi, T.N. Turan, S.S. Virani, J.Z. Willey, D. Woo, R.W. Yeh, and M.B. Turner Heart disease and stroke statistics-2015 update: a report from the American Heart Association Circulation 131 2015 e29 e322
90. A.J. Ferreira, and R.A. Santos Cardiovascular actions of angiotensin-(1-7) Braz. J. Med. Biol. Res. 38 2005 499 507
91. M. Flores-Munoz, N.J. Smith, C. Haggerty, G. Milligan, and S.A. Nicklin Angiotensin1-9 antagonises pro-hypertrophic signalling in cardiomyocytes via the angiotensin type 2 receptor J. Physiol. 589 2011 939 951
92. R.A. Santos, Simoes, S. e, A.C. ilva, C. Maric, D.M. Silva, R.P. Machado, B. de, I. uhr, S. Heringer-Walther, S.V. Pinheiro, M.T. Lopes, M. Bader, E.P. Mendes, V.S. Lemos, M.J. Campagnole-Santos, H.P. Schultheiss, R. Speth, and T. Walther Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas Proc. Natl. Acad. Sci. U. S. A. 100 2003 8258 8263
93. M. Sharif, N. Sasakawa, and M.R. Hanley Malignant transformation by G protein-coupled hormone receptors Mol. Cell. Endocrinol. 100 1994 115 119
94. D. Young, G. Waitches, C. Birchmeier, O. Fasano, and M. Wigler Isolation and characterization of a new cellular oncogene encoding a protein with multiple potential transmembrane domains Cell 45 1986 711 719
95. R. Metzger, M. Bader, T. Ludwig, C. Berberich, B. Bunnemann, and D. Ganten Expression of the mouse and rat mas proto-oncogene in the brain and peripheral tissues FEBS Lett. 357 1995 27 32
96. D. Young, K. O'Neill, T. Jessell, and M. Wigler Characterization of the rat mas oncogene and its high-level expression in the hippocampus and cerebral cortex of rat brain Proc. Natl. Acad. Sci. U. S. A. 85 1988 5339 5342
97. M. Bader, N. Alenina, M.A. Andrade-Navarro, and R.A. Santos MAS and its related G protein-coupled receptors, Mrgprs Pharmacol. Rev. 66 2014 1080 1105
98. R.Q. Lautner, D.C. Villela, R.A. Fraga-Silva, N. Silva, T. Verano-Braga, F. Costa-Fraga, J. Jankowski, V. Jankowski, F. Sousa, A. Alzamora, E. Soares, C. Barbosa, F. Kjeldsen, A. Oliveira, J. Braga, S. Savergnini, G. Maia, A.B. Peluso, D. Passos-Silva, A. Ferreira, F. Alves, A. Martins, M. Raizada, R. Paula, D. Motta-Santos, F. Klempin, A. Pimenta, N. Alenina, R. Sinisterra, M. Bader, M.J. Campagnole-Santos, and R.A. Santos Discovery and characterization of alamandine: a novel component of the renin-angiotensin system Circ. Res. 112 2013 1104 1111
99. N. Alenina, P. Xu, B. Rentzsch, E.L. Patkin, and M. Bader Genetically altered animal models for Mas and angiotensin-(1-7) Exp. Physiol. 93 2008 528 537
100. M.F. Dias-Peixoto, A.J. Ferreira, P.W. Almeida, V.B. Braga, D.C. Coutinho, D.S. Melo, F. Gomes, A. ilho, M.B. Melo, L. Greco, M.J. Campagnole-Santos, R.F. Lima, R.A. Santos, and S. Guatimosim The cardiac expression of Mas receptor is responsive to different physiological and pathological stimuli Peptides 35 2012 196 201
101. T.R. Jackson, L.A. Blair, J. Marshall, M. Goedert, and M.R. Hanley The mas oncogene encodes an angiotensin receptor Nature 335 1988 437 440
102. S.Q. Savergnini, D. Ianzer, M.B. Carvalho, A.J. Ferreira, G.A. Silva, F.D. Marques, A.A. Peluso, M. Beiman, G. Cojocaru, Y. Cohen, A.P. Almeida, G. Rotman, and R.A. Santos The novel Mas agonist, CGEN-856S, attenuates isoproterenol-induced cardiac remodeling and myocardial infarction injury in rats PLoS One 8 2013 e57757
103. R.A. Santos, M.J. Campagnole-Santos, N.C. Baracho, M.A. Fontes, L.C. Silva, L.A. Neves, D.R. Oliveira, S.M. Caligiorne, A.R. Rodrigues, C. Gropen Junior, and et al. Characterization of a new angiotensin antagonist selective for angiotensin-(1-7): evidence that the actions of angiotensin-(1-7) are mediated by specific angiotensin receptors Brain Res. Bull. 35 1994 293 298
104. W.O. Sampaio, Souza, S. dos, R.A. antos, R. Faria-Silva, M. da, M. ata, L.T. achado, E.L. Schiffrin, and R.M. Touyz Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways Hypertension 49 2007 185 192
105. J. Zhao, E. Liu, G. Li, L. Qi, J. Li, and W. Yang Effects of the angiotensin- (1-7)/Mas/PI3K/Akt/nitric oxide axis and the possible role of atrial natriuretic peptide in an acute atrial tachycardia canine model J. Renin Angiotensin Aldosterone Syst. 2014
106. S. Zheng, Y. Yang, R. Song, X. Yang, H. Liu, Q. Ma, L. Yang, R. Meng, T. Tao, S. Wang, and J. He Ang-(1-7) promotes the migration and invasion of human renal cell carcinoma cells via Mas-mediated AKT signaling pathway Biochem. Biophys. Res. Commun. 460 2015 333 340
107. F. Cisternas, M.G. Morales, C. Meneses, F. Simon, E. Brandan, J. Abrigo, Y. Vazquez, and C. Cabello-Verrugio Angiotensin-(1-7) decreases skeletal muscle atrophy induced by angiotensin II through a Mas receptor-dependent mechanism Clin. Sci. (Lond.) 128 2015 307 319
108. A. Than, M.K. Leow, and P. Chen Control of adipogenesis by the autocrine interplays between angiotensin 1-7/Mas receptor and angiotensin II/AT1 receptor signaling pathways J. Biol. Chem. 288 2013 15520 15531
109. J.F. Giani, M.M. Gironacci, M.C. Munoz, C. Pena, D. Turyn, and F.P. Dominici Angiotensin-(1-7) stimulates the phosphorylation of JAK2, IRS-1 and Akt in rat heart in vivo: role of the AT1 and Mas receptors Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1154 H1163
110. M.C. Munoz, J.F. Giani, and F.P. Dominici Angiotensin-(1-7) stimulates the phosphorylation of Akt in rat extracardiac tissues in vivo via receptor Mas Regul. Pept. 161 2010 1 7
111. T. Verano-Braga, V. Schwammle, M. Sylvester, D.G. Passos-Silva, A.A. Peluso, G.M. Etelvino, R.A. Santos, and P. Roepstorff Time-resolved quantitative phosphoproteomics: new insights into Angiotensin-(1-7) signaling networks in human endothelial cells J. Proteome Res. 11 2012 3370 3381
112. F.P. Dominici, V. Burghi, M.C. Munoz, and J.F. Giani Modulation of the action of insulin by angiotensin-(1-7) Clin. Sci. (Lond.) 126 2014 613 630
113. M. Canals, L. Jenkins, E. Kellett, and G. Milligan Up-regulation of the angiotensin II type 1 receptor by the MAS proto-oncogene is due to constitutive activation of Gq/G11 by MAS J. Biol. Chem. 281 2006 16757 16767
114. E.R. Gomes, R.A. Santos, and S. Guatimosim Angiotensin-(1-7)-mediated signaling in cardiomyocytes Int. J. Hypertens 2012 2012 493129
115. K.C. Tirupula, R. Desnoyer, R.C. Speth, and S.S. Karnik Atypical signaling and functional desensitization response of MAS receptor to peptide ligands PLoS One 9 2014 e103520
116. L. Wang, D. Luo, X. Liao, J. He, C. Liu, C. Yang, and H. Ma Ang-(1-7) offers cytoprotection against ischemia-reperfusion injury by restoring intracellular calcium homeostasis J. Cardiovasc. Pharmacol. 63 2014 259 264
117. T. Kenakin, and A. Christopoulos Signalling bias in new drug discovery: detection, quantification and therapeutic impact Nat. Rev. Drug Discovery 12 2013 205 216
118. R.A. Santos, J.M. Brum, K.B. Brosnihan, and C.M. Ferrario The renin-angiotensin system during acute myocardial ischemia in dogs Hypertension 15 1990 I121 127
119. C. Peiro, S. Vallejo, F. Gembardt, V. Azcutia, S. Heringer-Walther, L. Rodriguez-Manas, H.P. Schultheiss, C.F. Sanchez-Ferrer, and T. Walther Endothelial dysfunction through genetic deletion or inhibition of the G protein-coupled receptor Mas: a new target to improve endothelial function J. Hypertens 25 2007 2421 2425
120. C.H. Castro, R.A. Santos, A.J. Ferreira, M. Bader, N. Alenina, and A.P. Almeida Effects of genetic deletion of angiotensin-(1-7) receptor Mas on cardiac function during ischemia/reperfusion in the isolated perfused mouse heart Life Sci. 80 2006 264 268
121. Y. Wang, C. Qian, A.J. Roks, D. Westermann, S.M. Schumacher, F. Escher, R.G. Schoemaker, T.L. Reudelhuber, W.H. van Gilst, H.P. Schultheiss, C. Tschope, and T. Walther Circulating rather than cardiac angiotensin-(1-7) stimulates cardioprotection after myocardial infarction Circ. Heart Fail 3 2010 286 293
122. L.T. McCollum, P.E. Gallagher, and E. Ann Tallant Angiotensin-(1-7) attenuates angiotensin II-induced cardiac remodeling associated with upregulation of dual-specificity phosphatase 1 Am. J. Physiol. Heart Circ. Physiol. 302 2012 H801 810
123. V.B. Patel, S. Bodiga, D. Fan, S.K. Das, Z. Wang, W. Wang, R. Basu, J. Zhong, Z. Kassiri, and G.Y. Oudit Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1-7 in experimental heart failure in angiotensin-converting enzyme 2-null mice Hypertension 59 2012 1195 1203
124. W.C. De Mello Angiotensin (1-7) re-establishes impulse conduction in cardiac muscle during ischaemia-reperfusion. The role of the sodium pump J. Renin Angiotensin Aldosterone Syst. 5 2004 203 208
125. A.E. Loot, A.J. Roks, R.H. Henning, R.A. Tio, A.J. Suurmeijer, F. Boomsma, G. van, and W.H. ilst Angiotensin-(1-7) attenuates the development of heart failure after myocardial infarction in rats Circulation 105 2002 1548 1550
126. C. Mercure, A. Yogi, G.E. Callera, A.B. Aranha, M. Bader, A.J. Ferreira, R.A. Santos, T. Walther, R.M. Touyz, and T.L. Reudelhuber Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart Circ. Res. 103 2008 1319 1326
127. E.A. Tallant, C.M. Ferrario, and P.E. Gallagher Angiotensin-(1-7) inhibits growth of cardiac myocytes through activation of the mas receptor Am. J. Physiol. Heart Circ. Physiol. 289 2005 H1560 H1566
128. J.G. He, S.L. Chen, Y.Y. Huang, Y.L. Chen, Y.G. Dong, and H. Ma The nonpeptide AVE0991 attenuates myocardial hypertrophy as induced by angiotensin II through downregulation of transforming growth factor-beta1/Smad2 expression Heart Vessels 25 2010 438 443
129. B. Liang, Y. Li, Z. Han, J. Xue, Y. Zhang, S. Jia, and C. Wang CE2-Ang (1-7) axis is induced in pressure overloaded rat model Int. J. Clin. Exp. Pathol. 8 2015 1443 1450
130. M.P. Ocaranza, I. Godoy, J.E. Jalil, M. Varas, P. Collantes, M. Pinto, M. Roman, C. Ramirez, M. Copaja, G. Diaz-Araya, P. Castro, and S. Lavandero Enalapril attenuates downregulation of Angiotensin-converting enzyme 2 in the late phase of ventricular dysfunction in myocardial infarcted rat Hypertension 48 2006 572 578
131. J. Xing, J. Lu, and J. Li Role of angiotensin-(1-7) and Mas-R-nNOS pathways in amplified neuronal activity of dorsolateral periaqueductal gray after chronic heart failure Neurosci. Lett. 563 2014 6 11
132. E. Kaschina, and T. Unger Angiotensin AT1/AT2 receptors: regulation, signalling and function Blood Pressure 12 2003 70 88
133. Y. Kambayashi, S. Bardhan, K. Takahashi, S. Tsuzuki, H. Inui, T. Hamakubo, and T. Inagami Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition J. Biol. Chem. 268 1993 24543 24546
134. H. Funke-Kaiser, J. Reinemund, U.M. Steckelings, and T. Unger Adapter proteins and promoter regulation of the angiotensin AT2 receptor-implications for cardiac pathophysiology J. Renin Angiotensin Aldosterone Syst. 11 2010 7 17
135. S.H. Padia, and R.M. Carey AT2 receptors: beneficial counter-regulatory role in cardiovascular and renal function Pflugers Arch. 465 2013 99 110
136. M. Horiuchi, M. Akishita, and V.J. Dzau Recent progress in angiotensin II type 2 receptor research in the cardiovascular system Hypertension 33 1999 613 621
137. G. Faria-Costa, A. Leite-Moreira, and T. Henriques-Coelho Cardiovascular effects of the angiotensin type 2 receptor Rev. Port. Cardiol. 33 2014 439 449
138. C. Savoia, F. Tabet, G. Yao, E.L. Schiffrin, and R.M. Touyz Negative regulation of RhoA/Rho kinase by angiotensin II type 2 receptor in vascular smooth muscle cells: role in angiotensin II-induced vasodilation in stroke-prone spontaneously hypertensive rats J. Hypertens 23 2005 1037 1045
139. C. Hu, A. Dandapat, J. Chen, Y. Liu, P.L. Hermonat, R.M. Carey, and J.L. Mehta Over-expression of angiotensin II type 2 receptor (agtr2) reduces atherogenesis and modulates LOX-1, endothelial nitric oxide synthase and heme-oxygenase-1 expression Atherosclerosis 199 2008 288 294
140. R.M. Touyz, and E.L. Schiffrin Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells Pharmacol. Rev. 52 2000 639 672
141. D. Henrion, N. Kubis, and B.I. Levy Physiological and pathophysiological functions of the AT(2) subtype receptor of angiotensin II: from large arteries to the microcirculation Hypertension 38 2001 1150 1157
142. Y. Li, X.H. Li, and H. Yuan Angiotensin II type-2 receptor-specific effects on the cardiovascular system Cardiovasc. Diagn. Ther. 2 2012 56 62
143. F.M. Tavares, I.B. da Silva, D.A. Gomes, and M.L. Barreto-Chaves Angiotensin II type 2 receptor (AT2R) is associated with increased tolerance of the hyperthyroid heart to ischemia-reperfusion Cardiovasc. Drugs Ther. 27 2013 393 402
144. J. Varagic, S. Ahmad, S. Nagata, and C.M. Ferrario ACE2: angiotensin II/angiotensin-(1-7) balance in cardiac and renal injury Curr. Hypertens Rep. 16 2014 420
145. M.P. Ocaranza, L. Michea, M. Chiong, S. Lavandero, J.E.R. Jalil, and eply dissociating angiotensin 1-9 anticardiovascular remodeling effects from those on blood pressure J. Hypertens 32 2014 1719 1721
146. M.P. Ocaranza, J. Moya, V. Barrientos, R. Alzamora, D. Hevia, C. Morales, M. Pinto, N. Escudero, L. Garcia, U. Novoa, P. Ayala, G. Diaz-Araya, I. Godoy, M. Chiong, S. Lavandero, J.E. Jalil, and L. Michea Angiotensin-(1-9) reverses experimental hypertension and cardiovascular damage by inhibition of the angiotensin converting enzyme/Ang II axis J. Hypertens 32 2014 771 783
147. P.M. Abadir, R.M. Carey, and H.M. Siragy Angiotensin AT2 receptors directly stimulate renal nitric oxide in bradykinin B2-receptor-null mice Hypertension 42 2003 600 604
148. C. Savoia, T. Ebrahimian, Y. He, J.P. Gratton, E.L. Schiffrin, and R.M. Touyz Angiotensin II/AT2 receptor-induced vasodilation in stroke-prone spontaneously hypertensive rats involves nitric oxide and cGMP-dependent protein kinase J. Hypertens 24 2006 2417 2422
149. A. Dandapat, C.P. Hu, J. Chen, Y. Liu, J.A. Khan, F. Remeo, R.M. Carey, P.L. Hermonat, and J.L. Mehta Over-expression of angiotensin II type 2 receptor (agtr2) decreases collagen accumulation in atherosclerotic plaque Biochem. Biophys. Res. Commun. 366 2008 871 877
150. P. Brassard, F. Amiri, and E.L. Schiffrin Combined angiotensin II type 1 and type 2 receptor blockade on vascular remodeling and matrix metalloproteinases in resistance arteries Hypertension 46 2005 598 606
151. C. Dimitropoulou, R.E. White, L. Fuchs, H. Zhang, J.D. Catravas, G.O. Carrier, and I.I. Angiotensin relaxes microvessels via the AT(2) receptor and Ca(2+)-activated K(+) (BK(Ca)) channels Hypertension 37 2001 301 307
152. M. Horiuchi, W. Hayashida, T. Kambe, T. Yamada, and V.J. Dzau Angiotensin type 2 receptor dephosphorylates Bcl-2 by activating mitogen-activated protein kinase phosphatase-1 and induces apoptosis J. Biol. Chem. 272 1997 19022 19026
153. K. Bedecs, N. Elbaz, M. Sutren, M. Masson, C. Susini, A.D. Strosberg, and C. Nahmias Angiotensin II type 2 receptors mediate inhibition of mitogen-activated protein kinase cascade and functional activation of SHP-1 tyrosine phosphatase Biochem. J. 325 Pt 2 1997 449 454
154. S. Nouet, N. Amzallag, J.M. Li, S. Louis, I. Seitz, T.X. Cui, A.M. Alleaume, B. Di, M. enedetto, C. Boden, M. Masson, A.D. Strosberg, M. Horiuchi, P.O. Couraud, and C. Nahmias Trans-inactivation of receptor tyrosine kinases by novel angiotensin II AT2 receptor-interacting protein, ATIP J. Biol. Chem. 279 2004 28989 28997
155. C.J. Wruck, H. Funke-Kaiser, T. Pufe, H. Kusserow, M. Menk, J.H. Schefe, M.L. Kruse, M. Stoll, and T. Unger Regulation of transport of the angiotensin AT2 receptor by a novel membrane-associated Golgi protein Arterioscler. Thromb. Vasc. Biol. 25 2005 57 64
156. B. Di, M. enedetto, I. Bieche, F. Deshayes, S. Vacher, S. Nouet, V. Collura, I. Seitz, S. Louis, P. Pineau, D. Amsellem-Ouazana, P.O. Couraud, A.D. Strosberg, D. Stoppa-Lyonnet, R. Lidereau, and C. Nahmias Structural organization and expression of human MTUS1, a candidate 8p22 tumor suppressor gene encoding a family of angiotensin II AT2 receptor-interacting proteins, ATIP Gene 380 2006 127 136
157. M.A. Krezel, L.A. Rezmann, N. Varghayee, J. Pete, A.G. Frauman, and S.N. Louis Gene sequencing and tissue expression of unknown isoforms of an angiotensin II type 2 receptor interacting protein, ATIP, in the rat Biosci. Biotechnol. Biochem. 75 2011 414 418
158. T. Kinjo, M. Isomura, T. Iwamasa, and Y. Nakamura Molecular cloning and characterization of two novel genes on chromosome 8p21.3 J. Hum. Genet. 45 2000 12 17
159. S. Seibold, C. Rudroff, M. Weber, J. Galle, C. Wanner, and M. Marx Identification of a new tumor suppressor gene located at chromosome 8p21. 3-22 FASEB J. 17 2003 1180 1182
160. M.P. Ocaranza, S. Lavandero, J.E. Jalil, J. Moya, M. Pinto, U. Novoa, F. Apablaza, L. Gonzalez, C. Hernandez, M. Varas, R. Lopez, I. Godoy, H. Verdejo, and M. Chiong Angiotensin-(1-9) regulates cardiac hypertrophy in vivo and in vitro J. Hypertens 28 2010 1054 1064
161. M. Flores-Munoz, B.M. Godinho, A. Almalik, and S.A. Nicklin Adenoviral delivery of angiotensin-(1-7) or angiotensin-(1-9) inhibits cardiomyocyte hypertrophy via the mas or angiotensin type 2 receptor PLoS One 7 2012 e45564
162. S.A. Cha, B.M. Park, S. Gao, and S.H. Kim Stimulation of ANP by angiotensin-(1-9) via the angiotensin type 2 receptor Life Sci. 93 2013 934 940
163. M. Flores-Munoz, L.M. Work, K. Douglas, L. Denby, A.F. Dominiczak, D. Graham, and S.A. Nicklin Angiotensin-(1-9) attenuates cardiac fibrosis in the stroke-prone spontaneously hypertensive rat via the angiotensin type 2 receptor Hypertension 59 2012 300 307
164. M.P. Ocaranza, P. Rivera, U. Novoa, M. Pinto, L. Gonzalez, M. Chiong, S. Lavandero, and J.E. Jalil Rho kinase inhibition activates the homologous angiotensin-converting enzyme-angiotensin-(1-9) axis in experimental hypertension J. Hypertens 29 2011 706 715
165. E.G. Erdos, H.L. Jackman, V. Brovkovych, F. Tan, and P.A. Deddish Products of angiotensin I hydrolysis by human cardiac enzymes potentiate bradykinin J. Mol. Cell. Cardiol. 34 2002 1569 1576
166. H.L. Jackman, M.G. Massad, M. Sekosan, F. Tan, V. Brovkovych, B.M. Marcic, and E.G. Erdos Angiotensin 1-9 and 1-7 release in human heart: role of cathepsin A Hypertension 39 2002 976 981
167. R. Ray, C.E. Murdoch, M. Wang, C.X. Santos, M. Zhang, S. Alom-Ruiz, N. Anilkumar, A. Ouattara, A.C. Cave, S.J. Walker, D.J. Grieve, R.L. Charles, P. Eaton, A.C. Brewer, and A.M. Shah Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo Arterioscler. Thromb. Vasc. Biol. 31 2011 1368 1376
168. Z. Chen, F. Tan, E.G. Erdos, and P.A. Deddish Hydrolysis of angiotensin peptides by human angiotensin I-converting enzyme and the resensitization of B2 kinin receptors Hypertension 46 2005 1368 1373
169. M. Flores-Munoz, N.J. Smith, C. Haggerty, G. Milligan, and S.A. Nicklin Angiotensin1-9 antagonises pro-hypertrophic signalling in cardiomyocytes via the angiotensin type 2 receptor J. Physiol. 589 2011 939 951
170. H. Zheng, S.Y. Pu, X.F. Fan, X.S. Li, Y. Zhang, J. Yuan, Y.F. Zhang, and J.L. Yang Treatment with angiotensin-(1-9) alleviates the cardiomyopathy in streptozotocin-induced diabetic rats Biochem. Pharmacol. 95 2015 38 45
171. D. Fintini, C. Brufani, and M. Cappa Profile of mecasermin for the long-term treatment of growth failure in children and adolescents with severe primary IGF-1 deficiency Ther. Clin. Risk Manag. 5 2009 553 559
172. R.G. Rosenfeld IGF-I therapy in growth disorders Eur. J. Endocrinol. 157 Suppl. 1 2007 S57 S60
173. S.F. Kemp, J.L. Fowlkes, and K.M. Thrailkill Efficacy and safety of mecasermin rinfabate Expert Opin. Biol. Ther. 6 2006 533 538
174. Hoeybye C., Metabolic effects of GH and IGF-I in growth hormone deficient (GHD) and diabetes and impaired glucose tolerance (IGT). https://wwwclinicaltrialsgov/ct2/show/NCT01020955?term=IGF-1&rank=30 2009.
175. FDA Office of Orphan Products Development. Study of recombinant human insulin-like growth factor I in patients with severe insulin resistance. https://wwwclinicaltrialsgov/ct2/show/NCT00004419?term=IGF-1&rank=140 1999.
176. FDA Office of Orphan Products Development. Short term study of recombinant human insulin-like growth factor I in children with hyperinsulinism. https://wwwclinicaltrialsgov/ct2/show/NCT00004825?term=IGF-1&rank=120 2000.
177. FDA Office of Orphan Products Development. Dose ranging study of recombinant human insulin-like growth factor I in children with hyperinsulinism. https://wwwclinicaltrialsgov/ct2/show/NCT00004699?term=IGF-1&rank=135 2000.
178. FDA Office of Orphan Products Development. Phase II long term, randomized study of recombinant human insulin-like growth factor I in children with hyperinsulinism. https://wwwclinicaltrialsgov/ct2/show/NCT00004700?term=IGF-1&rank=136 2000.
179. Mayo Clinic Insulin-like growth factor-1 in amyotrophic lateral sclerosis (ALS) trial. https://wwwclinicaltrialsgov/ct2/show/NCT00035815?term=IGF-1&rank=38 2002.
180. Kim R. Effects of IGF-I in HIV metabolic disease. https://wwwclinicaltrialsgov/ct2/show/NCT01329744?term=IGF-1&rank=139 2011.
181. NIAID NIoAaID. Treatment for growth failure in patients with X-linked severe combined immunodeficiency: Phase 2 study of insulin-like growth factor-1. https://wwwclinicaltrialsgov/ct2/show/NCT00490100?term=IGF-1&rank=9 2007.
182. Kaufmann W. Treatment of Rett syndrome with recombinant human IGF-1. https://wwwclinicaltrialsgov/ct2/show/NCT01777542?term=IGF-1&rank=18 2013.
183. Kaufmann W. Treatment of Rett syndrome with rhIGF-1 (Mecasermin [rDNA] injection). https://wwwclinicaltrialsgov/ct2/show/NCT01253317?term=IGF-1&rank=28 2010.
184. Shire IGF-1/IGFBP3 prevention of retinopathy of prematurity. https://wwwclinicaltrialsgov/ct2/show/NCT01096784?term=IGF-1&rank=23 2010.
185. The University of Texas Medical Branch G. Assessment of mechanisms of improved wound healing. https://wwwclinicaltrialsgov/ct2/show/NCT00673309?term=IGF-1&rank=50 2007.
186. Moxley RT. Effects of SomatoKine (Iplex) recombinant human insulin-like growth factor-1/recombinant human insulin-like growth factor-binding protein-3 (rhIGF-I/rhIGFBP-3) in myotonic dystrophy type 1 (DM1). https://wwwclinicaltrialsgov/ct2/show/NCT00233519?term=IGF-1&rank=33 2005.
187. Insmed Incorporated Safety and efficacy study of recombinant human insulin-like growth factor-I/recombinant human insulin-like growth factor binding protein-3 (rhIGF-I/rhIGFBP-3) in myotonic dystrophy type 1. https://wwwclinicaltrialsgov/ct2/show/NCT00577577?term=IGF-1&rank=200 2007.
188. Children's Hospital Medical Center C. Safety and efficacy study of IGF-1 in Duchenne muscular dystrophy. https://wwwclinicaltrialsgov/ct2/show/NCT01207908?term=IGF-1&rank=3 2012.
189. National Institutes of Health Clinical Center (CC). A 48-week (24-week baseline followed by a 24-week treatment) phase II pilot study of the tolerability and effect/efficacy of subcutaneously administered insulin-like growth factor-1 (rhIGF) (CEP-151) in multiple sclerosis (MS) patients. https://wwwclinicaltrialsgov/ct2/show/NCT00001669?term=IGF-1&rank=199 1999.
190. [190] Nationwide Children's Hospital. Effect of Increlex® on children with Crohn disease. https://wwwclinicaltrialsgov/ct2/show/NCT00764699?term=IGF-1&rank=301 2008.
191. Insmed Incorporated IGF-I/IGFBP-3 therapy in children and adolescents with growth hormone insenitivity syndrome (GHIS) such as Laron syndrome. https://wwwclinicaltrialsgov/ct2/show/NCT00368173?term=IGF-1&rank=326 2006.
192. Klibanski A. Effects of anorexia nervosa on peak bone mass. https://wwwclinicaltrialsgov/ct2/show/NCT01301183?term=IGF-1&rank=66 2011.
193. Misra M. Effects of rhIGF-1 on bone metabolism in adolescent girls with anorexia nervosa (814). https://wwwclinicaltrialsgov/ct2/show/NCT00720122?term=IGF-1&rank=116 2008.
194. Hansen M. Patellar tendinopathy - effect of training and enhancement of the collagen synthesis by insulin-like growth factor-I (IGF-I). https://wwwclinicaltrialsgov/ct2/show/NCT01834989?term=IGF-1&rank=59 2013.
195. Wilson TA. IGF-1 therapy in patients with cystic fibrosis. https://wwwclinicaltrialsgov/ct2/show/NCT00566241?term=IGF-1&rank=4 2007.
196. Kolevzon A. A pilot treatment study of insulin-like growth factor-1 (IGF-1) in autism spectrum disorder. https://wwwclinicaltrialsgov/ct2/show/NCT01970345?term=IGF-1&rank=2 2013.
197. Caplice N. Evaluation of the safety and efficacy of using insulin-like growth factor-1 in patients with a heart attack (RESUS-AMI). https://wwwclinicaltrialsgov/ct2/show/NCT01438086?term=IGF-1&rank=44 2011.
198. Columbia University Differential effects of rhGH vs. rhIGF-1 on cardiovascular risk factors. https://wwwclinicaltrialsgov/ct2/show/NCT00684957?term=IGF-1&rank=60 2008.
199. C. Werner, M. Baumhakel, K.K. Teo, R. Schmieder, J. Mann, T. Unger, S. Yusuf, and M. Bohm RAS blockade with ARB and ACE inhibitors: current perspective on rationale and patient selection Clin. Res. Cardiol. 97 2008 418 431
200. Y. Wan, C. Wallinder, B. Plouffe, H. Beaudry, A.K. Mahalingam, X. Wu, B. Johansson, M. Holm, M. Botoros, A. Karlen, A. Pettersson, F. Nyberg, L. Fandriks, N. Gallo-Payet, A. Hallberg, and M. Alterman Design, synthesis, and biological evaluation of the first selective nonpeptide AT2 receptor agonist J. Med. Chem. 47 2004 5995 6008
201. G.T. Wagenaar, Laghmani, H. el, M. Fidder, R.M. Sengers, V. de, Y.P. isser, V. de, L. ries, R. Rink, A.J. Roks, G. Folkerts, and F.J. Walther Agonists of MAS oncogene and angiotensin II type 2 receptors attenuate cardiopulmonary disease in rats with neonatal hyperoxia-induced lung injury Am. J. Physiol. Lung Cell. Mol. Physiol. 305 2013 L341 L351
202. E.S. Jones, M.P. Del Borgo, J.F. Kirsch, D. Clayton, S. Bosnyak, I. Welungoda, N. Hausler, S. Unabia, P. Perlmutter, W.G. Thomas, M.I. Aguilar, and R.E. Widdop A single beta-amino acid substitution to angiotensin II confers AT2 receptor selectivity and vascular function Hypertension 57 2011 570 576
203. R. Shemesh, A. Toporik, Z. Levine, I. Hecht, G. Rotman, A. Wool, D. Dahary, E. Gofer, Y. Kliger, M.A. Soffer, A. Rosenberg, D. Eshel, and Y. Cohen Discovery and validation of novel peptide agonists for G-protein-coupled receptors J. Biol. Chem. 283 2008 34643 34649
204. G. Wiemer, L.W. Dobrucki, F.R. Louka, T. Malinski, and H. Heitsch AVE 0991, a nonpeptide mimic of the effects of angiotensin-(1-7) on the endothelium Hypertension 40 2002 847 852
205. A.C. Mendes, A.J. Ferreira, S.V. Pinheiro, and R.A. Santos Chronic infusion of angiotensin-(1-7) reduces heart angiotensin II levels in rats Regul. Pept. 125 2005 29 34
206. N.M. Santiago, P.S. Guimaraes, R.A. Sirvente, L.A. Oliveira, M.C. Irigoyen, R.A. Santos, and M.J. Campagnole-Santos Lifetime overproduction of circulating Angiotensin-(1-7) attenuates deoxycorticosterone acetate-salt hypertension-induced cardiac dysfunction and remodeling Hypertension 55 2010 889 896
207. A.M. Papinska, N.M. Mordwinkin, C.J. Meeks, S.S. Jadhav, and K.E. Rodgers Angiotensin-(1-7) administration benefits cardiac, renal, and progenitor cell function in db/db mice Br. J. Pharmacol. 2015
208. X.X. Liao, R.X. Guo, H. Ma, L.C. Wang, Z.H. Chen, C.T. Yang, and J.Q. Feng Effects of angiotensin-(1-7) on oxidative stress and functional changes of isolated rat hearts induced by ischemia-reperfusion Nan Fang Yi Ke Da Xue Xue Bao 28 2008 1345 1348
209. R. Faria-Silva, F.V. Duarte, and R.A. Santos Short-term angiotensin(1-7) receptor MAS stimulation improves endothelial function in normotensive rats Hypertension 46 2005 948 952
210. H.Z. Liu, C.Y. Gao, X.Q. Wang, H.X. Fu, H.H. Yang, X.P. Wang, Y.H. Liu, M.W. Li, Z.M. Niu, G.Y. Dai, D.T. Qi, and Y. Zhang Angiotensin(1-7) attenuates left ventricular dysfunction and myocardial apoptosis on rat model of adriamycin-induced dilated cardiomyopathy Zhonghua Xin Xue Guan Bing Za Zhi 40 2012 219 224