Endothelium in Aortic Aneurysm Disease: New Insights

Author(s): Eleftherios Spartalis*, Michael Spartalis, Antonios Athanasiou, Stavroula A. Paschou, Nikolaos Patelis, Vassilis Voudris, Dimitrios C. Iliopoulos

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 7 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Inflammation is recognized as a fundamental element in the development and growth of aortic aneurysms. Aortic aneurysm is correlated with aortic wall deformities and injury, as a result of inflammation, matrix metalloproteinases activation, oxidative stress, and apoptosis of vascular smooth muscle cells. The endothelial wall has a critical part in the inflammation of the aorta and endothelial heterogeneity has proven to be significant for modeling aneurysm formation. Endothelial shear stress and blood flow affect the aortic wall through hindrance of cytokines and adhesion molecules excreted by endothelial cells, causing reduction of the inflammation process in the media and adventitia. This pathophysiological process results in the disruption of elastic fibers, degradation of collagen fibers, and destruction of vascular smooth muscle cells. Consequently, the aortic wall is impaired due to reduced thickness, decreased mechanical function, and cannot tolerate the impact of blood flow leading to aortic expansion. Surgery is still considered the mainstay therapy for large aortic aneurysms. The prevention of aortic dilation, though, is based on the hinderance of endothelial dysregulation with drugs, the reduction of reactive oxygen and nitrogen species, and also the reduction of pro-inflammatory molecules and metalloproteinases. Further investigations are required to enlighten the emerging role of endothelial cells in aortic disease.

Keywords: endothelium, endothelial dysfunction, aorta, cardiovascular disease, aneurysm, pathophysiological process

[1]
Piechota-Polanczyk, A.; Jozkowicz, A.; Nowak, W.; Eilenberg, W.; Neumayer, C.; Malinski, T.; Huk, I.; Brostjan, C. The abdominal aortic aneurysm and intraluminal thrombus: current concepts of development and treatment. Front. Cardiovasc. Med., 2015, 2, 19.
[http://dx.doi.org/10.3389/fcvm.2015.00019] [PMID: 26664891 ]
[2]
Bäck, M.; Gasser, T.C.; Michel, J.B.; Caligiuri, G. Biomechanical factors in the biology of aortic wall and aortic valve diseases. Cardiovasc. Res., 2013, 99(2), 232-241.
[http://dx.doi.org/10.1093/cvr/cvt040] [PMID: 23459103 ]
[3]
Gomez, D.; Al Haj Zen, A.; Borges, L.F.; Philippe, M.; Gutierrez, P.S.; Jondeau, G.; Michel, J.B.; Vranckx, R. Syndromic and non-syndromic aneurysms of the human ascending aorta share activation of the Smad2 pathway. J. Pathol., 2009, 218(1), 131-142.
[http://dx.doi.org/10.1002/path.2516] [PMID: 19224541 ]
[4]
Touat, Z.; Lepage, L.; Ollivier, V.; Nataf, P.; Hvass, U.; Labreuche, J.; Jandrot-Perrus, M.; Michel, J.B.; Jondeau, G. Dilation-dependent activation of platelets and prothrombin in human thoracic ascending aortic aneurysm. Arterioscler. Thromb. Vasc. Biol., 2008, 28(5), 940-946.
[http://dx.doi.org/10.1161/ATVBAHA.107.158576] [PMID: 18292393 ]
[5]
Tsilimigras, D.I.; Sigala, F.; Karaolanis, G.; Ntanasis-Stathopoulos, I.; Spartalis, E.; Spartalis, M.; Patelis, N.; Papalampros, A.; Long, C.; Moris, D. Cytokines as biomarkers of inflammatory response after open versus endovascular repair of abdominal aortic aneurysms: a systematic review. Acta Pharmacol. Sin., 2018, 39(7), 1164-1175. >.
[http://dx.doi.org/10.1038/aps.2017.212] [PMID: 29770795 ]
[6]
Lederle, F.A.; Nelson, D.B.; Joseph, A.M. Smokers’ relative risk for aortic aneurysm compared with other smoking-related diseases: a systematic review. J. Vasc. Surg., 2003, 38(2), 329-334.
[http://dx.doi.org/10.1016/S0741-5214(03)00136-8] [PMID: 12891116 ]
[7]
Shantikumar, S.; Ajjan, R.; Porter, K.E.; Scott, D.J.A. Diabetes and the abdominal aortic aneurysm. Eur. J. Vasc. Endovasc. Surg., 2010, 39(2), 200-207.
[http://dx.doi.org/10.1016/j.ejvs.2009.10.014] [PMID: 19948418 ]
[8]
Choke, E.; Cockerill, G.; Wilson, W.R.; Sayed, S.; Dawson, J.; Loftus, I.; Thompson, M.M. A review of biological factors implicated in abdominal aortic aneurysm rupture. Eur. J. Vasc. Endovasc. Surg., 2005, 30(3), 227-244.
[http://dx.doi.org/10.1016/j.ejvs.2005.03.009] [PMID: 15893484 ]
[9]
Siasos, G.; Mourouzis, K.; Oikonomou, E.; Tsalamandris, S.; Tsigkou, V.; Vlasis, K.; Vavuranakis, M.; Zografos, T.; Dimitropoulos, S.; Papaioannou, T.G.; Kalampogias, A.; Stefanadis, C.; Papavassiliou, A.G.; Tousoulis, D. The role of endothelial dysfunction in aortic aneurysms. Curr. Pharm. Des., 2015, 21(28), 4016-4034.
[http://dx.doi.org/10.2174/1381612821666150826094156] [PMID: 26306838 ]
[10]
Sena, C.M.; Pereira, A.M.; Seiça, R. Endothelial dysfunction - a major mediator of diabetic vascular disease. Biochim. Biophys. Acta, 2013, 1832(12), 2216-2231.
[http://dx.doi.org/10.1016/j.bbadis.2013.08.006] [PMID: 23994612 ]
[11]
Moris, D.; Spartalis, M.; Tzatzaki, E.; Spartalis, E.; Karachaliou, G.S.; Triantafyllis, A.S.; Karaolanis, G.I.; Tsilimigras, D.I.; Theocharis, S. The role of reactive oxygen species in myocardial redox signaling and regulation. Ann. Transl. Med., 2017, 5(16), 324.
[http://dx.doi.org/10.21037/atm.2017.06.17] [PMID: 28861421 ]
[12]
Malashicheva, A.; Kostina, D.; Kostina, A.; Irtyuga, O.; Voronkina, I.; Smagina, L.; Ignatieva, E.; Gavriliuk, N.; Uspensky, V.; Moiseeva, O.; Vaage, J.; Kostareva, A. Phenotypic and functional changes of endothelial and smooth muscle cells in thoracic aortic aneurysms. Int. J. Vasc. Med., 2016, 20163107879
[http://dx.doi.org/10.1155/2016/3107879]
[13]
Corcoran, M.L.; Stetler-Stevenson, W.G.; Brown, P.D.; Wahl, L.M. Interleukin 4 inhibition of prostaglandin E2 synthesis blocks interstitial collagenase and 92-kDa type IV collagenase/gelatinase production by human monocytes. J. Biol. Chem., 1992, 267(1), 515-519.
[PMID: 1309751]
[14]
Varga, J.; Diaz-Perez, A.; Rosenbloom, J.; Jimenez, S.A. PGE2 causes a coordinate decrease in the steady state levels of fibronectin and types I and III procollagen mRNAs in normal human dermal fibroblasts. Biochem. Biophys. Res. Commun., 1987, 147(3), 1282-1288.
[http://dx.doi.org/10.1016/S0006-291X(87)80209-7] [PMID: 3478047]
[15]
Salcedo, R.; Zhang, X.; Young, H.A.; Michael, N.; Wasserman, K.; Ma, W.H.; Martins-Green, M.; Murphy, W.J.; Oppenheim, J.J. Angiogenic effects of prostaglandin E2 are mediated by up-regulation of CXCR4 on human microvascular endothelial cells. Blood, 2003, 102(6), 1966-1977.
[http://dx.doi.org/10.1182/blood-2002-11-3400] [PMID: 12791666 ]
[16]
Wang, D.; Wang, H.; Brown, J.; Daikoku, T.; Ning, W.; Shi, Q.; Richmond, A.; Strieter, R.; Dey, S.K.; DuBois, R.N. CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer. J. Exp. Med, 2006, 203(4), 941-951. >.
[http://dx.doi.org/10.1084/jem.20052124] [PMID: 16567391 ]
[17]
Nakayama, T.; Mutsuga, N.; Yao, L.; Tosato, G. Prostaglandin E2 promotes degranulation-independent release of MCP-1 from mast cells. J. Leukoc. Biol., 2006, 79(1), 95-104.
[http://dx.doi.org/10.1189/jlb.0405226] [PMID: 16275896 ]
[18]
Qian, R.Z.; Yue, F.; Zhang, G.P.; Hou, L.K.; Wang, X.H.; Jin, H.M. Roles of cyclooxygenase-2 in microvascular endothelial cell proliferation induced by basic fibroblast growth factor. Chin. Med. J. (Engl.), 2008, 121(24), 2599-2603.
[http://dx.doi.org/10.1097/00029330-200812020-00023] [PMID: 19187602 ]
[19]
Gitlin, J.M.; Trivedi, D.B.; Langenbach, R.; Loftin, C.D. Genetic deficiency of cyclooxygenase-2 attenuates abdominal aortic aneurysm formation in mice. Cardiovasc. Res., 2007, 73(1), 227-236.
[http://dx.doi.org/10.1016/j.cardiores.2006.10.015] [PMID: 17137566 ]
[20]
Walton, L.J.; Franklin, I.J.; Bayston, T.; Brown, L.C.; Greenhalgh, R.M.; Taylor, G.W.; Powell, J.T. Inhibition of prostaglandin E2 synthesis in abdominal aortic aneurysms: implications for smooth muscle cell viability, inflammatory processes, and the expansion of abdominal aortic aneurysms. Circulation, 1999, 100(1), 48-54.
[http://dx.doi.org/10.1161/01.CIR.100.1.48] [PMID: 10393680 ]
[21]
Bayston, T.; Ramessur, S.; Reise, J.; Jones, K.G.; Powell, J.T. Prostaglandin E2 receptors in abdominal aortic aneurysm and human aortic smooth muscle cells. J. Vasc. Surg., 2003, 38(2), 354-359.
[http://dx.doi.org/10.1016/S0741-5214(03)00339-2] [PMID: 12891120 ]
[22]
King, V.L.; Trivedi, D.B.; Gitlin, J.M.; Loftin, C.D. Selective cyclooxygenase-2 inhibition with celecoxib decreases angiotensin II-induced abdominal aortic aneurysm formation in mice. Arterioscler. Thromb. Vasc. Biol., 2006, 26(5), 1137-1143.
[http://dx.doi.org/10.1161/01.ATV.0000216119.79008.ac] [PMID: 16514081 ]
[23]
Wang, M.; Lee, E.; Song, W.; Ricciotti, E.; Rader, D.J.; Lawson, J.A.; Puré, E.; FitzGerald, G.A. Microsomal prostaglandin E synthase-1 deletion suppresses oxidative stress and angiotensin II-induced abdominal aortic aneurysm formation. Circulation, 2008, 117(10), 1302-1309.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.731398] [PMID: 18285567 ]
[24]
Moris, D.; Spartalis, M.; Spartalis, E.; Karachaliou, G.S.; Karaolanis, G.I.; Tsourouflis, G.; Tsilimigras, D.I.; Tzatzaki, E.; Theocharis, S. The role of reactive oxygen species in the pathophysiology of cardiovascular diseases and the clinical significance of myocardial redox. Ann. Transl. Med., 2017, 5(16), 326.
[http://dx.doi.org/10.21037/atm.2017.06.27] [PMID: 28861423 ]
[25]
Soler, M.; Camacho, M.; Escudero, J.R.; Iñiguez, M.A.; Vila, L. Human vascular smooth muscle cells but not endothelial cells express prostaglandin E synthase. Circ. Res., 2000, 87(6), 504-507.
[http://dx.doi.org/10.1161/01.RES.87.6.504] [PMID: 10988243 ]
[26]
Camacho, M.; Gerbolés, E.; Escudero, J.R.; Antón, R.; García-Moll, X.; Vila, L. Microsomal prostaglandin E synthase-1, which is not coupled to a particular cyclooxygenase isoenzyme, is essential for prostaglandin E(2) biosynthesis in vascular smooth muscle cells. J. Thromb. Haemost., 2007, 5(7), 1411-1419.
[http://dx.doi.org/10.1111/j.1538-7836.2007.02555.x] [PMID: 17403097 ]
[27]
Solà-Villà, D.; Camacho, M.; Solà, R.; Soler, M.; Diaz, J.M.; Vila, L. IL-1β induces VEGF, independently of PGE2 induction, mainly through the PI3-K/mTOR pathway in renal mesangial cells. Kidney Int., 2006, 70(11), 1935-1941.
[http://dx.doi.org/10.1038/sj.ki.5001948] [PMID: 17035941 ]
[28]
Blackburn, E.H. Structure and function of telomeres. Nature, 1991, 350(6319), 569-573.
[http://dx.doi.org/10.1038/350569a0] [PMID: 1708110 ]
[29]
Chan, S.R.; Blackburn, E.H. Telomeres and telomerase. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2004, 359(1441), 109-121.
[http://dx.doi.org/10.1098/rstb.2003.1370] [PMID: 15065663 ]
[30]
op den Buijs, J.; van den Bosch, P.P.; Musters, M.W.; van Riel, N.A. Mathematical modeling confirms the length-dependency of telomere shortening. Mech. Ageing Dev., 2004, 125(6), 437-444.
[http://dx.doi.org/10.1016/j.mad.2004.03.007] [PMID: 15178133 ]
[31]
Dimitroulis, D.; Katsargyris, A.; Klonaris, C.; Avgerinos, E.D.; Fragou-Plemenou, M.; Kouraklis, G.; Liapis, C.D. Telomerase expression on aortic wall endothelial cells is attenuated in abdominal aortic aneurysms compared to healthy nonaneurysmal aortas. J. Vasc. Surg., 2011, 54(6), 1778-1783.
[http://dx.doi.org/10.1016/j.jvs.2011.06.079] [PMID: 21917401 ]
[32]
Cafueri, G.; Parodi, F.; Pistorio, A.; Bertolotto, M.; Ventura, F.; Gambini, C.; Bianco, P.; Dallegri, F.; Pistoia, V.; Pezzolo, A.; Palombo, D. Endothelial and smooth muscle cells from abdominal aortic aneurysm have increased oxidative stress and telomere attrition. PLoS One, 2012, 7(4)e35312
[http://dx.doi.org/10.1371/journal.pone.0035312] [PMID: 22514726 ]
[33]
Wilson, W.R.; Herbert, K.E.; Mistry, Y.; Stevens, S.E.; Patel, H.R.; Hastings, R.A.; Thompson, M.M.; Williams, B. Blood leucocyte telomere DNA content predicts vascular telomere DNA content in humans with and without vascular disease. Eur. Heart J., 2008, 29(21), 2689-2694.
[http://dx.doi.org/10.1093/eurheartj/ehn386] [PMID: 18762552 ]
[34]
Atturu, G.; Brouilette, S.; Samani, N.J.; London, N.J.; Sayers, R.D.; Bown, M.J. Short leukocyte telomere length is associated with abdominal aortic aneurysm (AAA). Eur. J. Vasc. Endovasc. Surg., 2010, 39(5), 559-564.
[http://dx.doi.org/10.1016/j.ejvs.2010.01.013] [PMID: 20172749 ]
[35]
Reuter, S.; Gupta, S.C.; Chaturvedi, M.M.; Aggarwal, B.B. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med, 2010, 49(11), 1603-1616. 0.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.09.006] [PMID: 20840865 ]
[36]
Golledge, J.; Muller, R.; Clancy, P.; McCann, M.; Norman, P.E. Evaluation of the diagnostic and prognostic value of plasma D-dimer for abdominal aortic aneurysm. Eur. Heart J., 2011, 32(3), 354-364.
[http://dx.doi.org/10.1093/eurheartj/ehq171] [PMID: 20530504 ]
[37]
Kanai, A.J.; Strauss, H.C.; Truskey, G.A.; Crews, A.L.; Grunfeld, S.; Malinski, T. Shear stress induces ATP-independent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor. Circ. Res., 1995, 77(2), 284-293.
[http://dx.doi.org/10.1161/01.RES.77.2.284] [PMID: 7614715 ]
[38]
Kawashima, S. The two faces of endothelial nitric oxide synthase in the pathophysiology of atherosclerosis. Endothelium, 2004, 11(2), 99-107.
[http://dx.doi.org/10.1080/10623320490482637] [PMID: 15370069 ]
[39]
Khan, B.V.; Harrison, D.G.; Olbrych, M.T.; Alexander, R.W.; Medford, R.M. Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc. Natl. Acad. Sci. USA, 1996, 93(17), 9114-9119.
[http://dx.doi.org/10.1073/pnas.93.17.9114] [PMID: 8799163 ]
[40]
van den Oever, I.A.; Raterman, H.G.; Nurmohamed, M.T.; Simsek, S. Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus. Mediators Inflamm., 2010, 2010792393
[http://dx.doi.org/10.1155/2010/792393]
[41]
Johanning, J.M.; Armstrong, P.J.; Franklin, D.P.; Han, D.C.; Carey, D.J.; Elmore, J.R. Nitric oxide in experimental aneurysm formation: early events and consequences of nitric oxide inhibition. Ann. Vasc. Surg., 2002, 16(1), 65-72.
[http://dx.doi.org/10.1007/s10016-001-0139-z] [PMID: 11904807 ]
[42]
Gao, L.; Siu, K.L.; Chalupsky, K.; Nguyen, A.; Chen, P.; Weintraub, N.L.; Galis, Z.; Cai, H. Role of uncoupled endothelial nitric oxide synthase in abdominal aortic aneurysm formation: treatment with folic acid. Hypertension, 2012, 59(1), 158-166.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.181644] [PMID: 22083158 ]
[43]
Lizarbe, T.R.; Tarín, C.; Gómez, M.; Lavin, B.; Aracil, E.; Orte, L.M.; Zaragoza, C. Nitric oxide induces the progression of abdominal aortic aneurysms through the matrix metalloproteinase inducer EMMPRIN. Am. J. Pathol., 2009, 175(4), 1421-1430.
[http://dx.doi.org/10.2353/ajpath.2009.080845] [PMID: 19779140 ]
[44]
Mai, J.; Nanayakkara, G.; Lopez-Pastrana, J.; Li, X.; Li, Y.F.; Wang, X.; Song, A.; Virtue, A.; Shao, Y.; Shan, H.; Liu, F.; Autieri, M.V.; Kunapuli, S.P.; Iwakura, Y.; Jiang, X.; Wang, H.; Yang, X.F. Interleukin-17A promotes aortic endothelial cell activation via transcriptionally and post-translationally activating p38 mitogen-activated protein kinase (MAPK) pathway. J. Biol. Chem., 2016, 291(10), 4939-4954.
[http://dx.doi.org/10.1074/jbc.M115.690081] [PMID: 26733204 ]
[45]
Greene, J.A.; Portillo, J.A.; Lopez Corcino, Y.; Subauste, C.S. Lopez, Corcino, Y.; Subauste, C.S. CD40-TRAF signaling upregulates CX3CL1 and TNF-α in human aortic endothelial cells but not in retinal endothelial cells. PLoS One, 2015, 10(12)e0144133
[http://dx.doi.org/10.1371/journal.pone.0144133] [PMID: 26710229 ]
[46]
Adamopoulos, C.; Piperi, C.; Gargalionis, A.N.; Dalagiorgou, G.; Spilioti, E.; Korkolopoulou, P.; Diamanti-Kandarakis, E.; Papavassiliou, A.G. Advanced glycation end products upregulate lysyl oxidase and endothelin-1 in human aortic endothelial cells via parallel activation of ERK1/2-NF-κB and JNK-AP-1 signaling pathways. Cell. Mol. Life Sci., 2016, 73(8), 1685-1698.
[http://dx.doi.org/10.1007/s00018-015-2091-z] [PMID: 26646068 ]
[47]
Ravi, S.; Chaikof, E.L. Biomaterials for vascular tissue engineering. Regen. Med., 2010, 5(1), 107-120.
[http://dx.doi.org/10.2217/rme.09.77] [PMID: 20017698 ]
[48]
Otsuka, F.; Finn, A.V.; Yazdani, S.K.; Nakano, M.; Kolodgie, F.D.; Virmani, R. The importance of the endothelium in atherothrombosis and coronary stenting. Nat. Rev. Cardiol., 2012, 9(8), 439-453.
[http://dx.doi.org/10.1038/nrcardio.2012.64] [PMID: 22614618 ]
[49]
Melchiorri, A.J.; Hibino, N.; Fisher, J.P. Strategies and techniques to enhance the in situ endothelialization of small-diameter biodegradable polymeric vascular grafts. Tissue Eng. Part B Rev., 2013, 19(4), 292-307.
[http://dx.doi.org/10.1089/ten.teb.2012.0577] [PMID: 23252992 ]
[50]
Hur, J.; Yoon, C.H.; Kim, H.S.; Choi, J.H.; Kang, H.J.; Hwang, K.K.; Oh, B.H.; Lee, M.M.; Park, Y.B. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler. Thromb. Vasc. Biol., 2004, 24(2), 288-293.
[http://dx.doi.org/10.1161/01.ATV.0000114236.77009.06] [PMID: 14699017 ]
[51]
Avci-Adali, M.; Ziemer, G.; Wendel, H.P. Induction of EPC homing on biofunctionalized vascular grafts for rapid in vivo self-endothelialization--a review of current strategies. Biotechnol. Adv., 2010, 28(1), 119-129.
[http://dx.doi.org/10.1016/j.biotechadv.2009.10.005] [PMID: 19879347 ]
[52]
Schopka, S.; Schmid, T.; Schmid, C.; Lehle, K. Current strategies in cardiovascular biomaterial functionalization. Materials (Basel), 2010, 3(1), 638-655.
[http://dx.doi.org/10.3390/ma3010638]
[53]
Seifalian, A.M.; Tiwari, A.; Rashid, S.T.; Salacinski, H.; Hamilton, G. Impregnation of the the polymeric graft with adhesives molecules, typically oligopeptides or glycoprotein improves retention. Artif. Organs, 2002, 26(2), 209-210.
[http://dx.doi.org/10.1046/j.1525-1594.2002.00878.x] [PMID: 11879251 ]
[54]
Meinhart, J.G.; Deutsch, M.; Fischlein, T.; Howanietz, N.; Fröschl, A.; Zilla, P. Clinical autologous in vitro endothelialization of 153 infrainguinal ePTFE grafts. Ann. Thorac. Surg., 2001, 71(Suppl. 5), S327-S331.
[http://dx.doi.org/10.1016/S0003-4975(01)02555-3] [PMID: 11388216 ]
[55]
Thomas, A.C.; Campbell, G.R.; Campbell, J.H. Advances in vascular tissue engineering. Cardiovasc. Pathol., 2003, 12(5), 271-276.
[http://dx.doi.org/10.1016/S1054-8807(03)00086-3] [PMID: 14507577 ]
[56]
McGuigan, A.P.; Sefton, M.V. The influence of biomaterials on endothelial cell thrombogenicity. Biomaterials, 2007, 28(16), 2547-2571.
[http://dx.doi.org/10.1016/j.biomaterials.2007.01.039] [PMID: 17316788 ]
[57]
Graham, L.M.; Burkel, W.E.; Ford, J.W.; Vinter, D.W.; Kahn, R.H.; Stanley, J.C. Immediate seeding of enzymatically derived endothelium in Dacron vascular grafts. Early experimental studies with autologous canine cells. Arch. Surg, 1980, 115(11), 1289-1294. 9.
[http://dx.doi.org/10.1001/archsurg.1980.01380110033005] [PMID: 6449186 ]
[58]
Melero-Martin, J.M.; Khan, Z.A.; Picard, A.; Wu, X.; Paruchuri, S.; Bischoff, J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood, 2007, 109(11), 4761-4768.
[http://dx.doi.org/10.1182/blood-2006-12-062471] [PMID: 17327403 ]
[59]
Urbich, C.; Dimmeler, S. Endothelial progenitor cells: characterization and role in vascular biology. Circ. Res., 2004, 95(4), 343-353.
[http://dx.doi.org/10.1161/01.RES.0000137877.89448.78] [PMID: 15321944 ]
[60]
Jevon, M.; Dorling, A.; Hornick, P.I. Progenitor cells and vascular disease. Cell Prolif., 2008, 41(Suppl. 1), 146-164.
[http://dx.doi.org/10.1111/j.1365-2184.2008.00488.x] [PMID: 18181954 ]
[61]
Krenning, G.; Moonen, J.R.; van Luyn, M.J.; Harmsen, M.C. Generating new blood flow: integrating developmental biology and tissue engineering. Trends Cardiovasc. Med., 2008, 18(8), 312-323.
[http://dx.doi.org/10.1016/j.tcm.2009.01.004] [PMID: 19345319 ]
[62]
Hsu, S.H.; Sun, S.H.; Chen, D.C. Improved retention of endothelial cells seeded on polyurethane small-diameter vascular grafts modified by a recombinant RGD-containing protein. Artif. Organs, 2003, 27(12), 1068-1078.
[http://dx.doi.org/10.1111/j.1525-1594.2003.07141.x] [PMID: 14678420 ]
[63]
Asahara, T.; Murohara, T.; Sullivan, A.; Silver, M.; van der Zee, R.; Li, T.; Witzenbichler, B.; Schatteman, G.; Isner, J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science, 1997, 275(5302), 964-967.
[http://dx.doi.org/10.1126/science.275.5302.964] [PMID: 9020076 ]
[64]
Alobaid, N.; Salacinski, H.J.; Sales, K.M.; Ramesh, B.; Kannan, R.Y.; Hamilton, G.; Seifalian, A.M. Nanocomposite containing bioactive peptides promote endothelialisation by circulating progenitor cells: an in vitro evaluation. Eur. J. Vasc. Endovasc. Surg., 2006, 32(1), 76-83.
[http://dx.doi.org/10.1016/j.ejvs.2005.11.034] [PMID: 16466940 ]
[65]
de Mel, A.; Jell, G.; Stevens, M.M.; Seifalian, A.M. Biofunctionalization of biomaterials for accelerated in situ endothelialization: a review. Biomacromolecules, 2008, 9(11), 2969-2979.
[http://dx.doi.org/10.1021/bm800681k] [PMID: 18831592 ]
[66]
Alobaid, N.; Salacinski, H.J.; Sales, K.M.; Hamilton, G.; Seifalian, A.M. Single stage cell seeding of small diameter prosthetic cardiovascular grafts. Clin. Hemorheol. Microcirc., 2005, 33(3), 209-226.
[PMID: 16215287 ]
[67]
Wu, Y.F.; Zhang, J.; Gu, Y.Q.; Li, J.X.; Wang, L.C.; Wang, Z.G. Reendothelialization of tubular scaffolds by sedimentary and rotative forces: a first step toward tissue-engineered venous graft. Cardiovasc. Revasc. Med., 2008, 9(4), 238-247.
[http://dx.doi.org/10.1016/j.carrev.2008.01.005] [PMID: 18928949 ]
[68]
Teebken, O.E.; Puschmann, C.; Breitenbach, I.; Rohde, B.; Burgwitz, K.; Haverich, A. Preclinical development of tissue-engineered vein valves and venous substitutes using re-endothelialised human vein matrix. Eur. J. Vasc. Endovasc. Surg., 2009, 37(1), 92-102.
[http://dx.doi.org/10.1016/j.ejvs.2008.10.012] [PMID: 19008126 ]
[69]
Lehle, K.; Stock, M.; Schmid, T.; Schopka, S.; Straub, R.H.; Schmid, C. Cell-type specific evaluation of biocompatibility of commercially available polyurethanes. J. Biomed. Mater. Res. B Appl. Biomater., 2009, 90(1), 312-318.
[http://dx.doi.org/10.1002/jbm.b.31287] [PMID: 19072978 ]
[70]
Gulbins, H.; Pritisanac, A.; Petzold, R.; Goldemund, A.; Doser, M.; Dauner, M.; Meiser, B.; Reichart, B.; Daebritz, S. A low-flow adaptation phase improves shear-stress resistance of artificially seeded endothelial cells. Thorac. Cardiovasc. Surg, 2005, 53(2), 96-102. t>.
[http://dx.doi.org/10.1055/s-2004-830325] [PMID: 15786008 ]
[71]
Zilla, P.; Bezuidenhout, D.; Human, P. Prosthetic vascular grafts: wrong models, wrong questions and no healing. Biomaterials, 2007, 28(34), 5009-5027.
[http://dx.doi.org/10.1016/j.biomaterials.2007.07.017] [PMID: 17688939 ]
[72]
Rotmans, J.I.; Heyligers, J.M.; Stroes, E.S.; Pasterkamp, G. Endothelial progenitor cell-seeded grafts: rash and risky. Can. J. Cardiol., 2006, 22(11), 929-932.
[http://dx.doi.org/10.1016/S0828-282X(06)70311-7] [PMID: 16971977 ]
[73]
Knight, R.L.; Wilcox, H.E.; Korossis, S.A.; Fisher, J.; Ingham, E. The use of acellular matrices for the tissue engineering of cardiac valves. Proc. Inst. Mech. Eng. H, 2008, 222(1), 129-143.
[http://dx.doi.org/10.1243/09544119JEIM230] [PMID: 18335724 ]
[74]
Liu, T.; Liu, S.; Zhang, K.; Chen, J.; Huang, N. Endothelialization of implanted cardiovascular biomaterial surfaces: the development from in vitro to in vivo. J. Biomed. Mater. Res. A, 2014, 102(10), 3754-3772.
[http://dx.doi.org/10.1002/jbm.a.35025] [PMID: 24243819 ]
[75]
Zilla, P.P.; Greisler, H.P. Tissue engineering of vascular prosthetic grafts; RG Landes: Austin, TX, USA, 1999.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 27
ISSUE: 7
Year: 2020
Published on: 16 March, 2020
Page: [1081 - 1088]
Pages: 8
DOI: 10.2174/0929867326666190923151959
Price: $65

Article Metrics

PDF: 23
HTML: 6