Beta3-adrenergic receptors modulate vascular endothelial growth factor release in response to hypoxia through the nitric oxide pathway in mouse retinal explants

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 386, Issue 4, 2013, Pages 269-278

  Dal Monte, Massimo ^a   Filippi, Luca ^b   Bagnoli, Paola ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

3 AR agonists antagonists; Angiogenesis; NO VEGF relationships; Retinal explants; RNA silencing

Indexed keywords

BETA 3 ADRENERGIC RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SMALL INTERFERING RNA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLORIMETRY; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; EXPLANT; GENE SILENCING; HYPOXIA; MOUSE; NONHUMAN; RETINA EXPLANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STUDENT T TEST; WESTERN BLOTTING;

ANIMALS; ANOXIA; MICE; MICE, INBRED C57BL; NITRIC OXIDE; RECEPTORS, ADRENERGIC, BETA-3; RETINA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84876419366     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-012-0828-x     Document Type: Article

References (58)

1. Aragón JP, Condit ME, Bhushan S, Predmore BL, Patel SS, Grinsfelder DB, Gundewar S, Jha S, Calvert JW, Barouch LA, Lavu M, Wright HM, Lefer DJ (2011) Beta3-adrenoreceptor stimulation ameliorates myocardial ischemia-reperfusion injury via endothelial nitric oxide synthase and neuronal nitric oxide synthase activation. J Am Coll Cardiol 58:2683-2691
2. Arden GB, Sivaprasad S (2011) Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr Diabetes Rev 7:291-304
3. Ballester C, Sarriá B, García-Granero E, Mata M, Milara J, Morcillo EJ, Lledó S, Cortijo J (2010) Relaxation by beta 3-adrenoceptor agonists of the isolated human internal anal sphincter. Life Sci 86:358-364
4. Breit A, Lagacé M, Bouvier M (2004) Hetero-oligomerization between beta2- and beta3-adrenergic receptors generates a beta-adrenergic signaling unit with distinct functional properties. J Biol Chem 279:28756-28765
5. Bryan NS, Bian K, Murad F (2009) Discovery of the nitric oxide signaling pathway and targets for drug development. Front Biosci 14:1-18
6. Candelore MR, Deng L, Tota L, Guan XM, Amend A, Liu Y, Newbold R, Cascieri MA, Weber AE (1999) Potent and selective human beta(3)-adrenergic receptor antagonists. J Pharmacol Exp Ther 290:649-655
7. Carpéné C, Galitzky J, Fontana E, Atgié C, Lafontan M, Berlan M (1999) Selective activation of beta3-adrenoceptors by octopamine: comparative studies in mammalian fat cells. Naunyn Schmiedebergs Arch Pharmacol 359:310-321
8. Cawley SM, Kolodziej S, Ichinose F, Brouckaert P, Buys ES, Bloch KD (2011) sGC{alpha}1 mediates the negative inotropic effects of NO in cardiac myocytes independent of changes in calcium handling. Am J Physiol Heart Circ Physiol 301:H157-H163
9. Chen J, Smith LE (2007) Retinopathy of prematurity. Angiogenesis 10:133-140
10. Chen H, Ikeda U, Shimpo M, Ikeda M, Minota S, Shimada K (2000) Fluvastatin upregulates inducible nitric oxide synthase expression in cytokine-stimulated vascular smooth muscle cells. Hypertension 36:923-928
11. Chen J, Joyal JS, Hatton CJ, Juan AM, Pei DT, Hurst CG, Xu D, Stahl A, Hellstrom A, Smith LE (2012) Propranolol inhibition of β-adrenergic receptor does not suppress pathologic neovascularization in oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 53:2968-2977
12. Curatola AM, Moscatelli D, Norris A, Hendricks-Munoz K (2005) Retinal blood vessels develop in response to local VEGF-A signals in the absence of blood flow. Exp Eye Res 81:147-158
13. Dal Monte M, Ristori C, Cammalleri M, Bagnoli P (2009) Effects of somatostatin analogues on retinal angiogenesis in a mouse model of oxygen-induced retinopathy: involvement of the somatostatin receptor subtype 2. Invest Ophthalmol Vis Sci 50:3596-3606
14. Dal Monte M, Ristori C, Videau C, Loudes C, Martini D, Casini G, Epelbaum J, Bagnoli P (2010) Expression, localization, and functional coupling of the somatostatin receptor subtype 2 in a mouse model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 51:1848-1856
15. Dal Monte M, Martini D, Latina V, Pavan B, Filippi L, Bagnoli P (2012) Beta-adrenoreceptor agonism influences retinal responses to hypoxia in a model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 53:2181-2192
16. DeNiro M, Alsmadi O, Al-Mohanna F (2009) Modulating the hypoxia-inducible factor signaling pathway as a therapeutic modality to regulate retinal angiogenesis. Exp Eye Res 89:700-717
17. Dessy C, Balligand JL (2010) Beta3-adrenergic receptors in cardiac and vascular tissues emerging concepts and therapeutic perspectives. Adv Pharmacol 59:1351-1363
18. Dessy C, Moniotte S, Ghisdal P, Havaux X, Noirhomme P, Balligand JL (2004) Endothelial beta3-adrenoceptors mediate vasorelaxation of human coronary microarteries through nitric oxide and endothelium-dependent hyperpolarization. Circulation 110:948-954
19. Dulak J, Józkowicz A (2003) Regulation of vascular endothelial growth factor synthesis by nitric oxide: facts and controversies. Antioxid Redox Signal 5:123-132
20. Fredriksson JM, Lindquist JM, Bronnikov GE, Nedergaard J (2000) Norepinephrine induces vascular endothelial growth factor gene expression in brown adipocytes through a beta-adrenoreceptor/cAMP/protein kinase A pathway involving Src but independently of Erk1/2. J Biol Chem 275:13802-13811
21. He T, Xing YQ, Zhao XH, Ai M (2007) Interaction between iNOS and COX-2 in hypoxia-induced retinal neovascularization in mice. Arch Med Res 38:807-815
22. Hodis J, Vaclavíková R, Farghali H (2011) Beta-3 agonist-induced lipolysis and nitric oxide production: relationship to PPARgamma agonist/antagonist and AMP kinase modulation. Gen Physiol Biophys 30:90-99
23. Ignarro LJ, Sisodia M, Trinh K, Bedrood S, Wu G, Wei LH, Buga GM (2002) Nebivolol inhibits vascular smooth muscle cell proliferation by mechanisms involving nitric oxide but not cyclic GMP. Nitric Oxide 7:83-90
24. Joussen AM, Poulaki V, Qin W, Kirchhof B, Mitsiades N, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP (2002) Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol 160:501-509
25. Kaempf S, Walter P, Salz AK, Thumann G (2008) Novel organotypic culture model of adult mammalian neurosensory retina in co-culture with retinal pigment epithelium. J Neurosci Methods 173:47-58
26. Kanie S, Otsuka A, Yoshikawa S, Morimoto T, Hareyama N, Okazaki S, Kobayashi R, Hasebe K, Nakao K, Hayashi R, Mochizuki H, Matsumoto R, Ozono S (2012) Pharmacological effect of TRK-380, a novel selective human β3-adrenoceptor agonist, on mammalian detrusor strips. Urology 79:744, e1-7
27. Kaur C, Foulds WS, Ling EA (2008) Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog Retin Eye Res 27:622-647
28. Kaur C, Sivakumar V, Foulds WS, Luu CD, Ling EA (2009) Cellular and vascular changes in the retina of neonatal rats after an acute exposure to hypoxia. Invest Ophthalmol Vis Sci 50:5364-5374
29. Kubota Y, Nakahara T, Yunoki M, Mitani A, Maruko T, Sakamoto K, Ishii K (2002) Inhibitory mechanism of BRL37344 on muscarinic receptor-mediated contractions of the rat urinary bladder smooth muscle. Naunyn Schmiedebergs Arch Pharmacol 366:198-203
30. Leblais V, Pourageaud F, Ivorra MD, Marthan R, Muller B (2005) Comparison of the alpha-adrenoceptor-mediated effects of beta3-adrenoceptor ligands in rat pulmonary artery. Naunyn Schmiedebergs Arch Pharmacol 371:535-539
31. Li SY, Fu ZJ, Lo ACY (2012) Hypoxia-induced oxidative stress in ischemic retinopathy. Oxid Med Cell Longev 2012:426769
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408
33. Martini D, Dal Monte M, Ristori C, Cupisti E, Mei S, Fiorini P, Filippi L, Bagnoli P (2011) Antiangiogenic effects of β2 -adrenergic receptor blockade in a mouse model of oxygen-induced retinopathy. J Neurochem 119:1317-1329
34. Massion PB, Dessy C, Desjardins F, Pelat M, Havaux X, Belge C, Moulin P, Guiot Y, Feron O, Janssens S, Balligand JL (2004) Cardiomyocyte-restricted overexpression of endothelial nitric oxide synthase (NOS3) attenuates beta-adrenergic stimulation and reinforces vagal inhibition of cardiac contraction. Circulation 110:2666-2672
35. Mazumder B, Sampath P, Seshadri V, Maitra RK, DiCorleto PE, Fox PL (2003) Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115:187-198
36. Meda C, Plank C, Mykhaylyk O, Schmidt K, Mayer B (2010) Effects of statins on nitric oxide/cGMP signaling in human umbilical vein endothelial cells. Pharmacol Rep 62:100-112
37. Mei S, Cammalleri M, Azara D, Casini G, Bagnoli P, Dal Monte M (2012) Mechanisms underlying somatostatin receptor 2 down-regulation of vascular endothelial growth factor expression in response to hypoxia in mouse retinal explants. J Pathol 226:519-533
38. Mori A, Miwa T, Sakamoto K, Nakahara T, Ishii K (2010) Pharmacological evidence for the presence of functional beta(3)-adrenoceptors in rat retinal blood vessels. Naunyn Schmiedebergs Arch Pharmacol 382:119-126
39. Nakagawa T, Sato W, Sautin YY, Glushakova O, Croker B, Atkinson MA, Tisher CC, Johnson RJ (2006) Uncoupling of vascular endothelial growth factor with nitric oxide as a mechanism for diabetic vasculopathy. J Am Soc Nephrol 17:736-745
40. 3- adrenoceptor in human urinary bladder, comparison with rat and mouse: implications for drug discovery. Eur J Pharmacol 690:202-206
41. Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F, Diz PG, Gándara Rey JM, García-García A (2010) Beta-adrenergic receptors in cancer: therapeutic implications. Oncol Res 19:45-54
42. Perrone MG, Scilimati A (2011) β(3)-Adrenoceptor ligand development history through patent review. Expert Opin Ther Pat 21:505-536
43. Pott C, Brixius K, Bundkirchen A, Bölck B, Bloch W, Steinritz D, Mehlhorn U, Schwinger RH (2003) The preferential beta3-adrenoceptor agonist BRL 37344 increases force via beta1-/beta2-adrenoceptors and induces endothelial nitric oxide synthase via beta3-adrenoceptors in human atrial myocardium. Br J Pharmacol 138:521-529
44. Ristori C, Filippi L, Dal Monte M, Martini D, Cammalleri M, Fortunato P, la Marca G, Fiorini P, Bagnoli P (2011) Role of the adrenergic system in a mouse model of oxygen-induced retinopathy: antiangiogenic effects of beta-adrenoreceptor blockade. Invest Ophthalmol Vis Sci 52:155-170
45. Sapieha P, Hamel D, Shao Z, Rivera JC, Zaniolo K, Joyal JS, Chemtob S (2010) Proliferative retinopathies: angiogenesis that blinds. Int J Biochem Cell Biol 42:5-12
46. Steinle JJ, Booz GW, Meininger CJ, Day JN, Granger HJ (2003) Beta 3-adrenergic receptors regulate retinal endothelial cell migration and proliferation. J Biol Chem 278:20681-20686
47. Steinle JJ, Zamora DO, Rosenbaum JT, Granger HJ (2005) Beta 3-adrenergic receptors mediate choroidal endothelial cell invasion, proliferation, and cell elongation. Exp Eye Res 80:83-91
48. Storch CH, Hoeger PH (2010) Propranolol for infantile haemangiomas: insights into the molecular mechanisms of action. Br J Dermatol 163:269-274
49. Tremolada G, Del Turco C, Lattanzio R, Maestroni S, Maestroni A, Bandello F, Zerbini G (2012) The role of angiogenesis in the development of proliferative diabetic retinopathy: impact of intravitreal anti-VEGF treatment. Exp Diabetes Res 2012:728325
50. Trochu JN, Leblais V, Rautureau Y, Bévérelli F, Le Marec H, Berdeaux A, Gauthier C (1999) Beta 3-adrenoceptor stimulation induces vasorelaxation mediated essentially by endothelium-derived nitric oxide in rat thoracic aorta. Br J Pharmacol 128:69-76
51. Tugues S, Koch S, Gualandi L, Li X, Claesson-Welsh L (2011) Vascular endothelial growth factors and receptors: anti-angiogenic therapy in the treatment of cancer. Mol Aspects Med 32:88-111
52. van der Wijk T, Blanchetot C, den Hertog J (2005) Regulation of receptor protein-tyrosine phosphatase dimerization. Methods 35:73-79
53. Vrydag W, Michel MC (2007) Tools to study beta3-adrenoceptors. Naunyn Schmiedebergs Arch Pharmacol 374:385-398
54. West MB, Hill BG, Xuan YT, Bhatnagar A (2006) Protein glutathiolation by nitric oxide: an intracellular mechanism regulating redox protein modification. FASEB J 20:1715-1717
55. Wilkinson-Berka JL (2004) Vasoactive factors and diabetic retinopathy: vascular endothelial growth factor, cycoloxygenase-2 and nitric oxide. Curr Pharm Des 10:3331-3348
56. Wuest M, Eichhorn B, Grimm MO, Wirth MP, Ravens U, Kaumann AJ (2009) Catecholamines relax detrusor through beta 2-adrenoceptors in mouse and beta 3-adrenoceptors in man. J Pharmacol Exp Ther 328:213-222
57. Zhang Q, Zhang J, Guan Y, Zhang S, Zhu C, Xu GT, Wang L (2009) Suppression of retinal neovascularization by the iNOS inhibitor aminoguanidine in mice of oxygen-induced retinopathy. Graefes Arch Clin Exp Ophthalmol 247:919-927
58. Ziche M, Morbidelli L (2009) Molecular regulation of tumour angiogenesis by nitric oxide. Eur Cytokine Netw 20:164-170