Adenosine Receptors and Angiogenesis
2007; Lippincott Williams & Wilkins; Volume: 101; Issue: 11 Linguagem: Inglês
10.1161/circresaha.107.165761
ISSN1524-4571
Autores Tópico(s)Heme Oxygenase-1 and Carbon Monoxide
ResumoHomeCirculation ResearchVol. 101, No. 11Adenosine Receptors and Angiogenesis Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUBAdenosine Receptors and Angiogenesis John A. Auchampach John A. AuchampachJohn A. Auchampach From the Department of Pharmacology & Toxicology, Medical College of Wisconsin, Milwaukee. Originally published26 Nov 2007https://doi.org/10.1161/CIRCRESAHA.107.165761Circulation Research. 2007;101:1075–1077As originally hypothesized by Berne,1 adenosine is formed in the heart during hypoxia or ischemia and serves as a negative feedback signal to maintain oxygen delivery within a normal physiological range. Adenosine is formed by the metabolism of ATP and transported into the extracellular space by various nucleoside transport proteins.2 In a more localized manner that provides the opportunity for coordinated signaling with the diverse P2 purinoreceptor family that recognizes ATP and ADP, adenosine is also formed from the extracellular metabolism of adenine nucleotides released from stored granules (sympathetic nerves, platelets, mast cells) or through hemichannels (neutrophils, endothelial cells, epithelial cells) by ecto-apyrases and ecto-nucleotidases.3–5 Adenosine signals through activation of widely distributed cell surface G protein–coupled receptors, of which 4 different subtypes have been identified designated A1, A2A, A2B, and A3.6 By activating A2A receptors that are abundantly expressed in coronary vascular smooth muscle, adenosine generated under hypoxic conditions produces potent vasodilation thereby increasing nutrient and oxygen delivery.Although less appreciated, adenosine also serves to maintain tissue oxygenation in response to chronic ischemic/hypoxic stress by increasing the formation of new blood vessels; that is, by stimulating angiogenesis.7,8 Using adenosine receptor agonists or modulators of adenosine metabolism, an important role for adenosine has been established in in vivo models of angiogenesis.7,8 In cell culture systems, adenosine stimulates endothelial cell migration, proliferation, and tube formation,7–11 actions required for the formation of new capillary networks. This action occurs at concentrations of adenosine that are reached in hypoxic tissues. Adair7 recently estimated that adenosine can contribute up to 50% to 70% of the angiogenic response in some cases.Adenosine has direct mitogenic effects on vascular cells that may contribute to angiogenesis. However, the main proangiogenic actions of adenosine have been attributed to its ability to regulate the production of pro- and antiangiogenic substances from vascular cells and immune cells within the microenvironment of hypoxic tissues. Adenosine stimulates the release of interleukin-8 (IL-8), basic fibroblast growth factor (bFGF), and vascular endothelial growth factor (VEGF) from endothelial cells via A2B receptors that are dually coupled to Gs and Gq proteins while inhibiting production of the antiangiogenic factor thrombospondin-1, seemingly by the Gs protein–coupled A2A receptor.9,10 Adenosine also stimulates the production of VEGF, IL-8, and angiopoetin-1 from mast cells via A2B and A3 receptors.11 A unique mechanism has been identified by Lebovich and colleagues12 in which adenosine activation of the A2A receptor converts macrophages from a proinflammatory phenotype that generates large amounts of tumor necrosis factor-α and IL-6 to a proangiogenic phenotype that predominantly secretes VEGF. This particular mechanism is likely important in promoting tissue repair following wounding or microbial infection.In this issue of Circulation Research, Clark and colleagues13 demonstrate for the first time that the A1 adenosine receptor also participates in the angiogenic actions of adenosine. The A1 receptor is a Gi protein–coupled receptor that is well-known in the cardiovascular system to mediate the negative chronotropic, negative dromotropic, and antiadrenergic actions of adenosine responsible for reducing oxygen demand during metabolic stress.14 Using the chick chorioallantoic membrane model, Clark et al13 demonstrated that the selective A1 receptor agonist N6-cyclopentyladenosine (CPA) increased membrane vessel number by 40%. This effect produced by CPA was inhibited by the highly selective A1 receptor antagonist WRC-0571 confirming involvement of the A1 receptor. The authors13 need to be commended for devoting substantial effort in cloning and pharmacologically characterizing 3 of the 4 chick adenosine receptors to verify the selectivity of the pharmacological agents used in their study, as the binding affinities of adenosine receptor ligands are well known to differ markedly among species.15,16 A1 adenosine receptor expression has been reported previously in the vasculature,17,18 suggesting that CPA may function through a direct mitogenic action. However, CPA did not promote capillary formation in an aortic ring model of angiogenesis, leading the authors to conclude that the actions of CPA are indirect involving nonvascular cells. Among cells known to be involved in the angiogenic response, monocytes express A1 receptors.19 Acting on this lead, the authors showed that: (1) CPA stimulated VEGF release from isolated peripheral human monocytes through an A1 receptor-mediated mechanism, and (2) conditioned media from CPA-treated monocytes promoted vessel growth in the aortic ring model, which was blocked by the addition of an anti-VEGF antibody. Collectively, these results suggest that A1 receptor-mediated angiogenesis may involve the release of VEGF from monocytes. This study is important to our understanding of mechanisms of angiogenesis and the identification of the A1 receptor as a new therapeutic target. This is also the first study to demonstrate that A1 receptor activation promotes the release of a proangiogenic substance from an immune cell population. Previously, the only known function of the A1 receptor in the immune system is to promote migration of neutrophils and dendritic cells.20Clark and colleagues13 are careful to emphasize that the 2 major findings in their study may not be interrelated. That is, it is possible that A1 receptor–mediated angiogenesis in the chick chorioallantoic membrane model may involve other mechanisms that do not involve the release of VEGF from monocytes. Considering that A1 receptors facilitate migration of some immune cells,8 one interesting possibility is that CPA increased vasculogenesis. After wounding, adenosine has been implicated in mediating recruitment of endothelial progenitor cells to sites of neovascular formation.21 The authors13 also note that the importance of the A1 receptor in angiogenesis needs to be demonstrated in mammalian models. This work will be facilitated by the availability of mice with global deletion of adenosine receptor genes as well as mice with tissue-specific deletion of adenosine receptors. If confirmed, the exciting possibility will exist that pharmacological therapies targeting A1 receptor function may provide a basis for treating coronary artery disease, cancer, or other diseases in which the underlying basis is exaggerated or limited angiogenesis. Of note, the clinical use of direct A1 agonists as proangiogenic agents would face several obstacles, such as the potential to produce undesirable cardiovascular effects including bradycardia, atrioventricular block, and hypotension. Small molecule allosteric enhancers of the A1 receptor, which do not directly activate the receptor but instead enhance the actions of endogenous adenosine by increasing coupling efficiency to G proteins, may prove to be more useful.22,23 These agents could theoretically lead to angiogenesis in those tissue areas where hypoxia is greatest without affecting systemic hemodynamic parameters. Cardiovascular side-effects may also be minimized by using partial A1 receptor agonists that elicit submaximal responses even when administered at high doses.24,25 The use of A1 receptor antagonists to reduce angiogenesis may be less problematic. Afzal and colleagues26 recently reported that intraocular injection of a ribozyme specific for the A2B receptor reduced preretinal neovascularization in a neonatal mouse model of oxygen-induced retinopathy, highlighting the feasibility of using genetic approaches to modulate adenosine-mediated angiogenesis.In summary, Clark et al13 have made the novel discovery that A1 adenosine receptor activation can stimulate angiogenesis in an established experimental model. Combined with previous work conducted by others, it now appears that all 4 adenosine receptor subtypes participate in mediating the angiogenic actions of adenosine, working in a coordinated fashion involving indirect and direct actions on endothelial cells, smooth muscle cells, fibroblasts, and resident immune cells including monocytes, macrophages, and mast cells (see Figure 7 in Clark et al13). The relative importance of each adenosine receptor subtype awaits further investigation.The opinions expressed in this editorial are not necessarily those of the editors or of the American Heart Association.Sources of FundingThe author is supported by NIH R01 grants HL60051 and HL077707.DisclosuresNone.FootnotesCorrespondence to John A. Auchampach, PhD, Department of Pharmacology & Toxicology, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226. E-mail [email protected] References 1 Feigl EO. Berne's adenosine hypothesis of coronary blood flow control. Am J Physiol. 2004; 287: H1891–H1894.Google Scholar2 Thorn JA, Jarvis SM. Adenosine transporters. Gen Pharmacol. 1996; 27: 613–620.CrossrefMedlineGoogle Scholar3 Burnstock G. Purinergic signalling–an overview. Novartis Foundation Symposium. 2006; 276: 26–48.MedlineGoogle Scholar4 Eltzschig HK, Eckle T, Mager A, Kuper N, Karcher C, Weissmuller T, Boengler K, Schulz R, Robson SC, Colgan SP. 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Am J Pathol. 2004; 164: 1887–1892.CrossrefMedlineGoogle Scholar22 Chordia MD, Zigler M, Murphree LJ, Figler H, Macdonald TL, Olsson RA, Linden J. 6-aryl-8H-indeno[1,2-d]thiazol-2-ylamines: A1 adenosine receptor agonist allosteric enhancers having improved potency. J Med Chem. 2005; 48: 5131–5139.CrossrefMedlineGoogle Scholar23 Figler H, Olsson RA, Linden J. Allosteric enhancers of A1 adenosine receptors increase receptor-G protein coupling and counteract Guanine nucleotide effects on agonist binding. Mol Pharmacol. 2003; 64: 1557–1564.CrossrefMedlineGoogle Scholar24 Dhalla AK, Wong MY, Voshol PJ, Belardinelli L, Reaven GM. A1 adenosine receptor partial agonist lowers plasma FFA and improves insulin resistance induced by high-fat diet in rodents. Am J Physiol Endocrinol Metab. 2007; 292: E1358–E1363.CrossrefMedlineGoogle Scholar25 Zablocki JA, Wu L, Shryock J, Belardinelli L. 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