Recent Developments in Vascular Biology
2014; Lippincott Williams & Wilkins; Volume: 115; Issue: 12 Linguagem: Inglês
10.1161/circresaha.114.305639
ISSN1524-4571
Autores Tópico(s)Cardiovascular, Neuropeptides, and Oxidative Stress Research
ResumoHomeCirculation ResearchVol. 115, No. 12Recent Developments in Vascular Biology Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessResearch ArticlePDF/EPUBRecent Developments in Vascular Biology Daniel J. Conklin Daniel J. ConklinDaniel J. Conklin Originally published5 Dec 2014https://doi.org/10.1161/CIRCRESAHA.114.305639Circulation Research. 2014;115:e79–e82The field of vascular biology has transformed dramatically in recent years as new research has elucidated complex roles of novel proteins, stem/progenitor/hematopoietic cells, and miRNAs as well as redox signaling in vascular development, vascular tone regulation and disease in preclinical models and clinical settings. Review of this body of work highlights seminal findings and new developments that emphasize and illuminate underlying principles and historical connections. In the 1980s, there was the frenzied search for the identity of the Endothelium-Derived Relaxing Factor (EDRF; ie, NO).1,2 In the 1990s, the elucidation of myriad EDHFs (hyperpolarizing factors, eg, H2O2, K+, arachidonic acid metabolites) expanded endothelial cell complexity beyond NO.3–5 In the 2000s, the endothelial cell generation and overall cardiovascular effects of H2S were hotly pursued.6,7 In the 2010s, the role of the perivascular adipose tissue (PVAT) derived relaxing and contractile factors in vascular regulation under physiological and disease promoting conditions (eg, diet-induced obesity, metabolic syndrome) has emerged as a new integrative vascular issue of import because of the obesity epidemic.8Vasodilation Mechanisms – Still RelevantCritically important mechanisms continue to be sources of interest and renewed research. Indeed, the panoply of endothelium-derived factors that regulate vascular tone continues to grow, and identifying new ones will only enhance our understanding of the diverse factors that regulate vascular tone and blood flow in context-dependent ways. As elucidated in the article by Zhang et al, entitled "H2O2-induced dilation in human coronary arterioles: role of protein kinase G dimerization and large-conductance Ca2+-activated K+ channel activation," redox-mediated VSMC K+-channel opening ultimately leads to relaxation and dilation in coronary blood vessels.9 Similarly, PPAR-γ stimulated Regulatory G-protein S 5 (RGS5)-control of Protein Kinase C-mediated opening of calcium-activated BKCa channels also leads to VSMC relaxation in arterioles.10 If that is not enough, K+, BKCa or inward rectifying K+-channels along with the Na+/K+-ATPase are effector targets of acidosis11 or reactive hyperemia12 in arteriolar dilation, respectively. Thus, there has been a resurgence of research into the largely metabolism-driven (such as in exercise)13 and K+-channel-mediated regulation of arterial smooth muscle tone abounds. In another study, "Vascular bioactivation of nitroglycerin is catalyzed by cytosolic aldehyde dehydrogenase-2," Beretta et al,14 shed new light on a long-standing controversy regarding the mechanism of nitroglycerin (GTN) bioactivation in VSMC. Superseding the historic roles of both aortic GSTs15 and mitochondrial ALDH2,16 their findings suggest that cytoplasmic ALDH2 is the important player in blood vessels, a fresh perspective that could provide a new biochemical target with the potential to combat nitrate tolerance – the major limitation to continual use of organic nitrates.17Vascular Imaging – Not your Father's (or Galileo Galilei's) MicroscopeNot to be outdone by detailed vasoregulatory mechanisms, increased attention has been given to vascular imaging, and in recent years, several articles describing new vascular imaging approaches and their applications in a variety of physiological and pathophysiological settings have been published. For example, one of the more difficult tasks of imaging coronary blood flow (especially in mice) is accomplished by Krueger et al in "Visualizing regional myocardial blood flow in the mouse"—a straightforward title for a not so ordinary feat that involves the use of 15-μm fluorescent microspheres with unprecedented spatial and temporal resolution.18 Second, a "Novel genetic approach for in vivo vascular imaging in mice" by Bartelle et al19 is quite simply amazing as mice expressing the Biotag-BirA transgene are injected with various 'avidinated' probes and then imaged with near infrared, ultrasound, and MRI as appropriate. Similarly, Thuneman et al20 took the advice of Bartelle et al, to heart by making transgenic mice that express a cGMP sensor (cGi500) that when bound elicits fluorescence resonance energy transfer (FRET) for visualization of blood vessels in vivo. This technical accomplishment could be used, for example, in visual assessment of true nitrate tolerance that is a result of impaired GTN bioactivation in VSMC. Nanotechnology has also gained an imaging foothold via two like-minded articles featuring potent nuclear imaging methods for cell-type–specific targeting in atherosclerotic plaques.21 These were: "Nanobodies targeting mouse/human vcam1 for the nuclear imaging of atherosclerotic lesions" by Broisat et al, which utilized technetium-99 m (99 m)Tc-labeled, anti-VCAM1 nanobody for noninvasive detection of mouse and human VCAM122; and, "Polymeric nanoparticle PET/MR imaging allows macrophage detection in atherosclerotic plaques" by Majmudar et al, where 13-nm polymeric nanoparticles consisting of crosslinked-dextran radiolabeled with zirconium-89 are imaged and colocalized with CD11b+ cells in plaques.23 These new applications are powerful techniques that will not only revolutionize the way we visualize and interpret changes in vascular wall dynamics that regulate blood flow and vascular wall remodeling, but could also better our understanding of the early, causal, and deleterious modifications that ultimately promote endothelium dysfunction, atherosclerosis and aneurysm.Atherosclerosis to Aneurysm: Acts of RemodelingSince Virchow's day, our model of atherosclerosis is continually updating and recent articles add more of the same.24 From the works, "Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice"25; "Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis"26; and, "Deficiency of ATP-binding cassette transporters A1 and G1 in macrophages increases inflammation and accelerates atherosclerosis in mice",27 we see important roles for specific proteins expressed in bone marrow-derived hematopoietic (and inflammatory) cells that dramatically alter the progression of atherosclerosis, and as such, these are potentially new targets for suppression of atherosclerotic growth. Moreover, 'remodeling of the vascular wall' is a frequently used catch-all phrase; however, current studies are attempting to more precisely define the temporal and spatial relationships (eg, "outside in" versus "inside out")28 between critical events such as VSMC phenotypic switching and proliferation (eg, see "MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation"29; "MAPK phosphorylation of connexin 43 promotes binding of cyclin E and smooth muscle cell proliferation"30; "Quaking, an RNA-binding protein, is a critical regulator of vascular smooth muscle cell phenotype"31) and calcification (eg, "Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification"32; "Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells"33) that lead to development of atherosclerotic plaques and/or aneurysm formation. The latter pathology is associated with a new circulating biomarker that could be useful for aneurysm prognosis34 to aid more directed treatment35 as described by Marshall et al in "Thoracic aortic aneurysm frequency and dissection are associated with fibrillin-fragment concentrations in circulation." Similarly, a potential role of a miRNA is explored in "miR-29b participates in early aneurysm development in Marfan syndrome" by Merk et al with miR-29b suppressing elastin gene and augmenting apoptosis and MMP2.36 Finally, the article "Transient exposure of neonatal female mice to testosterone abrogates the sexual dimorphism of abdominal aortic aneurysms" by Zhang et al37 offers an especially compelling reminder of the powerful influence sex hormones have on cardiovascular disease risk.38Angiogenesis/Arteriogenesis — From EPCs to miRNAAlthough treatments to stop and reverse pathogenic growth processes are certainly crucial, methods that can promote new vascular growth, ie, angiogenesis and arteriogenesis, without tumorigenesis, are equally useful in tissue/organ recovery following ischemia-reperfusion–related injury. Many excellent works have addressed this topic, and it is no surprise that several of these have highlighted mechanisms that influence stem/progenitor cell biology and function. For example, "β2-Adrenergic receptor stimulation improves endothelial progenitor cell-mediated ischemic neoangiogenesis"39 shows EPCs have intact β2 adrenergic receptors that not only promote EPC migration, proliferation, and tube formation but also augment blood flow restoration in murine models of hindlimb ischemia. The intact endothelium itself is no passive partner in new blood vessel growth40 as shown by Sweet et al41 in "Endothelial Shc regulates arteriogenesis through dual control of arterial specification and inflammation via the notch and nuclear factor-κ-light-chain-enhancer of activated B-cell pathways"; and likewise by Yin et al42 in "Induction of vascular progenitor cells from endothelial cells stimulates coronary collateral growth". Additionally, a series of reports implicate one or more miRNAs in regulating angiogenesis such as miR-10 in zebrafish43; antagonistic action of miRNA-22344; as well as miR-10A* and miRNA-21 in EPCs,45 which identify potential targets of shRNA, antagomirs, etc... Finally, in additional integrative works that emphasize cellular interdependence and crosstalk in angiogenesis, two articles by Renault et al,46,47 "Gli3 regulation of myogenesis is necessary for ischemia-induced angiogenesis" and "Desert hedgehog promotes ischemia-induced angiogenesis by ensuring peripheral nerve survival" reveal that within the complex milieu of injury and regeneration, proangiogenic factors derive inputs including cardiomyocytes and peripheral neuron Schwann cells, to promote proper and efficient revascularization.Summary – A Few Good YearsThere are nearly 60,000 miles of blood vessels in the human body and their function, or dysfunction, can have long-lasting implications for the quality and quantity of life. In the wake of the diabetes and obesity epidemics, it becomes especially important that we better understand vascular dysfunction because these diseases have a particularly profound effect on cardiovascular health. In fact, vascular insulin resistance is one of the earliest events to occur in metabolic syndrome and precedes both endothelial dysfunction and atherosclerosis as well as other vascular defects.48 Several recent studies stand out in this regard and have identified promising vascular targets for intervention in diabetes and obesity. For example, Estrada et al show in "STIM1 restores coronary endothelial function in type 1 diabetic mice" that hyperglycemia-induced endothelium injury can be reversed by overexpressing the ER protein STIM1 to regulate ER calcium flux.49 On a more holistic level, Spinetti et al in "Global remodeling of the vascular stem cell niche in bone marrow of diabetic patients: implication of the microRNA-155/FOXO3a signaling pathway"50 implicate bone marrow-derived stem/progenitor cells as targets of diabetes (an effect reversed by miR-155) that may ultimately limit vascular repair and regeneration. Bringing us full circle is Sansbury et al51 who show that overexpression of eNOS (and subsequent NO effects) offsets diet-induced obesity in mice ultimately indicating that the 'antique EDRF' still has a place in the 21st century.Recent Developments in Cardiovascular Research: The goal of "Recent Developments" is to provide a concise but comprehensive overview of new advances in cardiovascular research, which we hope will keep our readers abreast of recent scientific discoveries and facilitate discussion, interpretation, and integration of the findings. This will enable readers who are not experts in a particular field to grasp the significance and effect of work performed in other fields. It is our hope and expectation that these "Recent Development" articles will help readers to gain a broader awareness and a deeper understanding of the status of research across the vast landscape of cardiovascular research—The Editors.Sources of FundingThis work supported by NIH grants: GM103492 and HL89380 (D.J.C.).FootnotesCorrespondence to Daniel J. Conklin, Diabetes and Obesity Center and Institute of Molecular Cardiology, University of Louisville, KY 40292.References1. Ignarro LJ, Byrns RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical.Circ Res. 1987; 61:866–879.LinkGoogle Scholar2. Loscalzo J. The identification of nitric oxide as endothelium-derived relaxing factor.Circ Res. 2013; 113:100–103. doi: 10.1161/CIRCRESAHA.113.301577.LinkGoogle Scholar3. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors.Circ Res. 1996; 78:415–423.LinkGoogle Scholar4. Liu Y, Bubolz AH, Mendoza S, Zhang DX, Gutterman DD. H2O2 is the transferrable factor mediating flow-induced dilation in human coronary arterioles.Circ Res. 2011; 108:566–573. doi: 10.1161/CIRCRESAHA.110.237636.LinkGoogle Scholar5. Adeagbo AS, Triggle CR. Varying extracellular [K+]: a functional approach to separating EDHF- and EDNO-related mechanisms in perfused rat mesenteric arterial bed.J Cardiovasc Pharmacol. 1993; 21:423–429.CrossrefMedlineGoogle Scholar6. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide.Circulation. 2008; 117:2351–2360. doi: 10.1161/CIRCULATIONAHA.107.753467.LinkGoogle Scholar7. Mani S, Li H, Untereiner A, Wu L, Yang G, Austin RC, Dickhout JG, Lhoták Š, Meng QH, Wang R. Decreased endogenous production of hydrogen sulfide accelerates atherosclerosis.Circulation. 2013; 127:2523–2534. doi: 10.1161/CIRCULATIONAHA.113.002208.LinkGoogle Scholar8. Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, Rothenberg FG, Neltner B, Romig-Martin SA, Dickson EW, Rudich S, Weintraub NL. Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding.Circ Res. 2009; 104:541–549. doi: 10.1161/CIRCRESAHA.108.182998.LinkGoogle Scholar9. Zhang DX, Borbouse L, Gebremedhin D, Mendoza SA, Zinkevich NS, Li R, Gutterman DD. H2O2-induced dilation in human coronary arterioles: role of protein kinase G dimerization and large-conductance Ca2+-activated K+ channel activation.Circ Res. 2012; 110:471–480. doi: 10.1161/CIRCRESAHA.111.258871.LinkGoogle Scholar10. Ketsawatsomkron P, Lorca RA, Keen HL, Weatherford ET, Liu X, Pelham CJ, Grobe JL, Faraci FM, England SK, Sigmund CD. PPARγ regulates resistance vessel tone through a mechanism involving RGS5-mediated control of protein kinase C and BKCa channel activity.Circ Res. 2012; 111:1446–1458. doi: 10.1161/CIRCRESAHA.112.271577.LinkGoogle Scholar11. Dabertrand F, Nelson MT, Brayden JE. Acidosis dilates brain parenchymal arterioles by conversion of calcium waves to sparks to activate BK channels.Circ Res. 2012; 110:285–294. doi: 10.1161/CIRCRESAHA.111.258145.LinkGoogle Scholar12. Crecelius AR, Richards JC, Luckasen GJ, Larson DG, Dinenno FA. Reactive hyperemia occurs via activation of inwardly rectifying potassium channels and Na+/K+-ATPase in humans.Circ Res. 2013; 113:1023–1032. doi: 10.1161/CIRCRESAHA.113.301675.LinkGoogle Scholar13. Hellsten Y, Nyberg M, Jensen LG, Mortensen SP. Vasodilator interactions in skeletal muscle blood flow regulation.J Physiol. 2012; 590:6297–6305. doi: 10.1113/jphysiol.2012.240762.CrossrefMedlineGoogle Scholar14. Beretta M, Wölkart G, Schernthaner M, Griesberger M, Neubauer R, Schmidt K, Sacherer M, Heinzel FR, Kohlwein SD, Mayer B. Vascular bioactivation of nitroglycerin is catalyzed by cytosolic aldehyde dehydrogenase-2.Circ Res. 2012; 110:385–393. doi: 10.1161/CIRCRESAHA.111.245837.LinkGoogle Scholar15. Singhal SS, Piper JT, Srivastava SK, Chaubey M, Bandorowicz-Pikula J, Awasthi S, Awasthi YC. Rabbit aorta glutathione S-transferases and their role in bioactivation of trinitroglycerin.Toxicol Appl Pharmacol. 1996; 140:378–386. doi: 10.1006/taap.1996.0234.CrossrefMedlineGoogle Scholar16. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M, Ullrich V, Mülsch A, Schulz E, Keaney JF, Stamler JS, Münzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance.J Clin Invest. 2004; 113:482–489. doi: 10.1172/JCI19267.CrossrefMedlineGoogle Scholar17. Sage PR, de la Lande IS, Stafford I, Bennett CL, Phillipov G, Stubberfield J, Horowitz JD. Nitroglycerin tolerance in human vessels: evidence for impaired nitroglycerin bioconversion.Circulation. 2000; 102:2810–2815.LinkGoogle Scholar18. Krueger MA, Huke SS, Glenny RW. Visualizing regional myocardial blood flow in the mouse.Circ Res. 2013; 112:e88–e97. doi: 10.1161/CIRCRESAHA.113.301162.LinkGoogle Scholar19. Bartelle BB, Berríos-Otero CA, Rodriguez JJ, Friedland AE, Aristizábal O, Turnbull DH. Novel genetic approach for in vivo vascular imaging in mice.Circ Res. 2012; 110:938–947. doi: 10.1161/CIRCRESAHA.111.254375.LinkGoogle Scholar20. Thunemann M, Wen L, Hillenbrand M, Vachaviolos A, Feil S, Ott T, Han X, Fukumura D, Jain RK, Russwurm M, de Wit C, Feil R. Transgenic mice for cGMP imaging.Circ Res. 2013; 113:365–371. doi: 10.1161/CIRCRESAHA.113.301063.LinkGoogle Scholar21. Majmudar MD, Nahrendorf M. Cardiovascular molecular imaging: the road ahead.J Nucl Med. 2012; 53:673–676. doi: 10.2967/jnumed.111.099838.CrossrefMedlineGoogle Scholar22. Broisat A, Hernot S, Toczek J, De Vos J, Riou LM, Martin S, Ahmadi M, Thielens N, Wernery U, Caveliers V, Muyldermans S, Lahoutte T, Fagret D, Ghezzi C, Devoogdt N. Nanobodies targeting mouse/human VCAM1 for the nuclear imaging of atherosclerotic lesions.Circ Res. 2012; 110:927–937. doi: 10.1161/CIRCRESAHA.112.265140.LinkGoogle Scholar23. Majmudar MD, Yoo J, Keliher EJ, Truelove JJ, Iwamoto Y, Sena B, Dutta P, Borodovsky A, Fitzgerald K, Di Carli MF, Libby P, Anderson DG, Swirski FK, Weissleder R, Nahrendorf M. Polymeric nanoparticle PET/MR imaging allows macrophage detection in atherosclerotic plaques.Circ Res. 2013; 112:755–761. doi: 10.1161/CIRCRESAHA.111.300576.LinkGoogle Scholar24. Colin S, Chinetti-Gbaguidi G, Staels B. Macrophage phenotypes in atherosclerosis.Immunol Rev. 2014; 262:153–166. doi: 10.1111/imr.12218.CrossrefMedlineGoogle Scholar25. Döring Y, Drechsler M, Wantha S, Kemmerich K, Lievens D, Vijayan S, Gallo RL, Weber C, Soehnlein O. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice.Circ Res. 2012; 110:1052–1056. doi: 10.1161/CIRCRESAHA.112.265868.LinkGoogle Scholar26. Hamers AA, Vos M, Rassam F, Marinković G, Marincovic G, Kurakula K, van Gorp PJ, de Winther MP, Gijbels MJ, de Waard V, de Vries CJ. Bone marrow-specific deficiency of nuclear receptor Nur77 enhances atherosclerosis.Circ Res. 2012; 110:428–438. doi: 10.1161/CIRCRESAHA.111.260760.LinkGoogle Scholar27. Westerterp M, Murphy AJ, Wang M, Pagler TA, Vengrenyuk Y, Kappus MS, Gorman DJ, Nagareddy PR, Zhu X, Abramowicz S, Parks JS, Welch C, Fisher EA, Wang N, Yvan-Charvet L, Tall AR. Deficiency of atp-binding cassette transporters a1 and g1 in macrophages increases inflammation and accelerates atherosclerosis in mice.Circ Res. 2013; 112:1456–1465.LinkGoogle Scholar28. Blomkalns AL, Chatterjee T, Weintraub NL. Turning ACS outside in: linking perivascular adipose tissue to acute coronary syndromes.Am J Physiol Heart Circ Physiol. 2010; 298:H734–H735. doi: 10.1152/ajpheart.00058.2010.CrossrefMedlineGoogle Scholar29. Li P, Zhu N, Yi B, Wang N, Chen M, You X, Zhao X, Solomides CC, Qin Y, Sun J. MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation.Circ Res. 2013; 113:1117–1127. doi: 10.1161/CIRCRESAHA.113.301306.LinkGoogle Scholar30. Johnstone SR, Kroncke BM, Straub AC, Best AK, Dunn CA, Mitchell LA, Peskova Y, Nakamoto RK, Koval M, Lo CW, Lampe PD, Columbus L, Isakson BE. MAPK phosphorylation of connexin 43 promotes binding of cyclin E and smooth muscle cell proliferation.Circ Res. 2012; 111:201–211. doi: 10.1161/CIRCRESAHA.112.272302.LinkGoogle Scholar31. van der Veer EP, de Bruin RG, Kraaijeveld AO, et al. Quaking, an RNA-binding protein, is a critical regulator of vascular smooth muscle cell phenotype.Circ Res. 2013; 113:1065–1075. doi: 10.1161/CIRCRESAHA.113.301302.LinkGoogle Scholar32. Sun Y, Byon CH, Yuan K, Chen J, Mao X, Heath JM, Javed A, Zhang K, Anderson PG, Chen Y. Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification.Circ Res. 2012; 111:543–552. doi: 10.1161/CIRCRESAHA.112.267237.LinkGoogle Scholar33. Liu Y, Drozdov I, Shroff R, Beltran LE, Shanahan CM. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells.Circ Res. 2013; 112:e99–109. doi: 10.1161/CIRCRESAHA.111.300543.LinkGoogle Scholar34. Marshall LM, Carlson EJ, O'Malley J, Snyder CK, Charbonneau NL, Hayflick SJ, Coselli JS, Lemaire SA, Sakai LY. Thoracic aortic aneurysm frequency and dissection are associated with fibrillin-1 fragment concentrations in circulation.Circ Res. 2013; 113:1159–1168. doi: 10.1161/CIRCRESAHA.113.301498.LinkGoogle Scholar35. Matt P, Habashi J, Carrel T, Cameron DE, Van Eyk JE, Dietz HC. Recent advances in understanding Marfan syndrome: should we now treat surgical patients with losartan?J Thorac Cardiovasc Surg. 2008; 135:389–394. doi: 10.1016/j.jtcvs.2007.08.047.CrossrefMedlineGoogle Scholar36. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, Tsao PS, Iosef C, Berry GJ, Mohr FW, Spin JM, Alvira CM, Robbins RC, Fischbein MP. miR-29b participates in early aneurysm development in Marfan syndrome.Circ Res. 2012; 110:312–324. doi: 10.1161/CIRCRESAHA.111.253740.LinkGoogle Scholar37. Zhang X, Thatcher SE, Rateri DL, Bruemmer D, Charnigo R, Daugherty A, Cassis LA. Transient exposure of neonatal female mice to testosterone abrogates the sexual dimorphism of abdominal aortic aneurysms.Circ Res. 2012; 110:e73–e85. doi: 10.1161/CIRCRESAHA.111.253880.LinkGoogle Scholar38. Makrygiannis G, Courtois A, Drion P, Defraigne JO, Kuivaniemi H, Sakalihasan N. Sex differences in abdominal aortic aneurysm: The role of sex hormones.Ann Vasc Surg. 2014; 287:1946–1958.CrossrefGoogle Scholar39. Galasso G, De Rosa R, Ciccarelli M, Sorriento D, Del Giudice C, Strisciuglio T, De Biase C, Luciano R, Piccolo R, Pierri A, Di Gioia G, Prevete N, Trimarco B, Piscione F, Iaccarino G. β2-Adrenergic receptor stimulation improves endothelial progenitor cell-mediated ischemic neoangiogenesis.Circ Res. 2013; 112:1026–1034. doi: 10.1161/CIRCRESAHA.111.300152.LinkGoogle Scholar40. Moraes F, Paye J, Mac Gabhann F, Zhuang ZW, Zhang J, Lanahan AA, Simons M. Endothelial cell-dependent regulation of arteriogenesis.Circ Res. 2013; 113:1076–1086. doi: 10.1161/CIRCRESAHA.113.301340.LinkGoogle Scholar41. Sweet DT, Chen Z, Givens CS, Owens AP, Rojas M, Tzima E. Endothelial Shc regulates arteriogenesis through dual control of arterial specification and inflammation via the notch and nuclear factor-κ-light-chain-enhancer of activated B-cell pathways.Circ Res. 2013; 113:32–39. doi: 10.1161/CIRCRESAHA.113.301407.LinkGoogle Scholar42. Yin L, Ohanyan V, Pung YF, Delucia A, Bailey E, Enrick M, Stevanov K, Kolz CL, Guarini G, Chilian WM. Induction of vascular progenitor cells from endothelial cells stimulates coronary collateral growth.Circ Res. 2012; 110:241–252. doi: 10.1161/CIRCRESAHA.111.250126.LinkGoogle Scholar43. Hassel D, Cheng P, White MP, Ivey KN, Kroll J, Augustin HG, Katus HA, Stainier DY, Srivastava D. MicroRNA-10 regulates the angiogenic behavior of zebrafish and human endothelial cells by promoting vascular endothelial growth factor signaling.Circ Res. 2012; 111:1421–1433. doi: 10.1161/CIRCRESAHA.112.279711.LinkGoogle Scholar44. Shi L, Fisslthaler B, Zippel N, Frömel T, Hu J, Elgheznawy A, Heide H, Popp R, Fleming I. MicroRNA-223 antagonizes angiogenesis by targeting β1 integrin and preventing growth factor signaling in endothelial cells.Circ Res. 2013; 113:1320–1330. doi: 10.1161/CIRCRESAHA.113.301824.LinkGoogle Scholar45. Zhu S, Deng S, Ma Q, Zhang T, Jia C, Zhuo D, Yang F, Wei J, Wang L, Dykxhoorn DM, Hare JM, Goldschmidt-Clermont PJ, Dong C. MicroRNA-10A* and MicroRNA-21 modulate endothelial progenitor cell senescence via suppressing high-mobility group A2.Circ Res. 2013; 112:152–164. doi: 10.1161/CIRCRESAHA.112.280016.LinkGoogle Scholar46. Renault MA, Chapouly C, Yao Q, Larrieu-Lahargue F, Vandierdonck S, Reynaud A, Petit M, Jaspard-Vinassa B, Belloc I, Traiffort E, Ruat M, Duplàa C, Couffinhal T, Desgranges C, Gadeau AP. Desert hedgehog promotes ischemia-induced angiogenesis by ensuring peripheral nerve survival.Circ Res. 2013; 112:762–770. doi: 10.1161/CIRCRESAHA.113.300871.LinkGoogle Scholar47. Renault MA, Vandierdonck S, Chapouly C, Yu Y, Qin G, Metras A, Couffinhal T, Losordo DW, Yao Q, Reynaud A, Jaspard-Vinassa B, Belloc I, Desgranges C, Gadeau AP. Gli3 regulation of myogenesis is necessary for ischemia-induced angiogenesis.Circ Res. 2013; 113:1148–1158. doi: 10.1161/CIRCRESAHA.113.301546.LinkGoogle Scholar48. Li Q, Park K, Li C, Rask-Madsen C, Mima A, Qi W, Mizutani K, Huang P, King GL. Induction of vascular insulin resistance and endothelin-1 expression and acceleration of atherosclerosis by the overexpression of protein kinase C-β isoform in the endothelium.Circ Res. 2013; 113:418–427. doi: 10.1161/CIRCRESAHA.113.301074.LinkGoogle Scholar49. Estrada IA, Donthamsetty R, Debski P, Zhou MH, Zhang SL, Yuan JX, Han W, Makino A. STIM1 restores coronary endothelial function in type 1 diabetic mice.Circ Res. 2012; 111:1166–1175. doi: 10.1161/CIRCRESAHA.112.275743.LinkGoogle Scholar50. Spinetti G, Cordella D, Fortunato O, Sangalli E, Losa S, Gotti A, Carnelli F, Rosa F, Riboldi S, Sessa F, Avolio E, Beltrami AP, Emanueli C, Madeddu P. Global remodeling of the vascular stem cell niche in bone marrow of diabetic patients: implication of the microRNA-155/FOXO3a signaling pathway.Circ Res. 2013; 112:510–522. doi: 10.1161/CIRCRESAHA.112.300598.LinkGoogle Scholar51. Sansbury BE, Cummins TD, Tang Y, Hellmann J, Holden CR, Harbeson MA, Chen Y, Patel RP, Spite MR, Bhatnagar A, Hill BG. Overexpression of endothelial nitric oxide synthase prevents diet-induced obesity and regulates adipocyte phenotype.Circ Res. 2012; 111:1176–1189.LinkGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Conklin D and Bhatnagar A (2018) Aldehydes and Cardiovascular Disease Comprehensive Toxicology, 10.1016/B978-0-12-801238-3.02038-9, (514-537), . December 5, 2014Vol 115, Issue 12 Advertisement Article InformationMetrics © 2014 American Heart Association, Inc.https://doi.org/10.1161/CIRCRESAHA.114.305639PMID: 25477491 Originally publishedDecember 5, 2014 PDF download Advertisement
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