Endothelial-to-mesenchymal transition contributes to fibro-proliferative vascular disease and is modulated by fluid shear stress

Cardiovascular Research

Volumn 108, Issue 3, 2015, Pages 377-386

  Moonen, Jan Renier A J ^a   Lee, Ee Soo ^a   Schmidt, Marc ^b   Maleszewska, Monika ^a   Koerts, Jasper A ^a   Brouwer, Linda A ^a   Van Kooten, Theo G ^a   Van Luyn, Marja J A ^a   Zeebregts, Clark J ^a   Krenning, Guido ^a   Harmsen, Martin C ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Endothelial to mesenchymal transition; ERK5; Fibrosis; Neointimal hyperplasia; Shear stress

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; CD31 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5; TRANSGELIN; VASCULAR ENDOTHELIAL CADHERIN; MAP2K5 PROTEIN, RAT; MAPK7 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; CELL TRANSFORMATION; CONTROLLED STUDY; ENDOTHELIAL MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYME CELL; MOUSE; NEOINTIMA; NEOINTIMA HYPERPLASIA; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; SIGNAL TRANSDUCTION; STABLE EXPRESSION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; AORTA DISEASE; BLOOD FLOW; C57BL MOUSE; CAROTID ARTERY; CAROTID ARTERY DISEASE; CELL PROLIFERATION; DISEASE MODEL; EPITHELIAL MESENCHYMAL TRANSITION; FIBROSIS; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PIG; RNA INTERFERENCE; THORACIC AORTA; TIME FACTOR; VASCULAR REMODELING;

ANIMALS; AORTA, THORACIC; AORTIC DISEASES; CAROTID ARTERIES; CAROTID ARTERY DISEASES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MAP KINASE KINASE 5; MECHANOTRANSDUCTION, CELLULAR; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEOINTIMA; PLAQUE, ATHEROSCLEROTIC; REGIONAL BLOOD FLOW; RNA INTERFERENCE; STRESS, MECHANICAL; SWINE; TIME FACTORS; TRANSFECTION; VASCULAR REMODELING;

EID: 84950315882     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv175     Document Type: Article

References (50)

1. Ross R, Glomset JA. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 1973;180:1332-1339.
2. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, Stone PH. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J Am Coll Cardiol 2007;49: 2379-2393.
3. Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 1983;53:502-514.
4. Cunningham KS, Gotlieb AI. The role of shear stress in the pathogenesis of atherosclerosis. Lab Invest 2005;85:9-23.
5. Nackman GB, Fillinger MF, Shafritz R,Wei T, Graham AM. Flow modulates endothelial regulation of smooth muscle cell proliferation: a new model. Surgery 1998;124: 353-360.
6. Krenning G, Moonen JR, Van Luyn MJ, Harmsen MC. Vascular smooth muscle cells for use in vascular tissue engineering obtained by endothelial-to-mesenchymal transdifferentiation (EnMT) on collagen matrices. Biomaterials 2008;29:3703-3711.
7. Maleszewska M, Moonen JR, Huijkman N, Van De Sluis B, Krenning G, Harmsen MC. IL-1beta and TGFbeta2 synergistically induce endothelial to mesenchymal transition in an NFkappaB-dependent manner. Immunobiology 2013;218:443-454.
8. Moonen JR, Krenning G, Brinker MG, Koerts JA, Van Luyn MJ, Harmsen MC. Endothelial progenitor cells give rise to pro-angiogenic smooth muscle-like progeny. Cardiovasc Res 2010;86:506-515.
9. Van Meeteren LA, ten Dijke P. Regulation of endothelial cell plasticity by TGF-beta. Cell Tissue Res 2012;347:177-186.
10. Markwald RR, Fitzharris TP, Manasek FJ. Structural development of endocardial cushions. Am J Anat 1977;148:85-119.
11. Zhu P, Huang L, Ge X, Yan F, Wu R, Ao Q. Transdifferentiation of pulmonary arteriolar endothelial cells into smooth muscle-like cells regulated by myocardin involved in hypoxia-induced pulmonary vascular remodelling. Int J Exp Pathol 2006;87:463-474.
12. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, Chandraker A, Yuan X, Pu WT, Roberts AB, Neilson EG, Sayegh MH, Izumo S, Kalluri R. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007;13:952-961.
13. Zeisberg EM, Potenta SE, Sugimoto H, Zeisberg M, Kalluri R. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 2008;19: 2282-2287.
14. Beranek JT, Cavarocchi NC. Undifferentiated vascular endothelial cells in coronary allograft atherosclerosis. Int J Cardiol 1990;28:127-128.
15. Beranek JT. Vascular endothelium-derived cells containing smooth muscle actin are present in restenosis. Lab Invest 1995;72:771.
16. Carrillo LM, Arciniegas E, Rojas H, Ramirez R. Immunolocalization of endocan during the endothelial-mesenchymal transition process. Eur J Histochem 2011;55:e13.
17. Comerford A, David T. Computer model of nucleotide transport in a realistic porcine aortic trifurcation. Ann Biomed Eng 2008;36:1175-1187.
18. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LC, Wofovitz E. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 2003;81:177-199.
19. Markwald RR, Fitzharris TP, Smith WN. Sturctural analysis of endocardial cytodifferentiation. Dev Biol 1975;42:160-180.
20. Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol 1998;18:677-685.
21. Parmar KM, Larman HB, Dai G, Zhang Y, Wang ET, Moorthy SN, Kratz JR, Lin Z, Jain MK, Gimbrone MA Jr, Garcia-Cardena G. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor. J Clin Invest 2006;116:49-58.
22. Yan C, Takahashi M, Okuda M, Lee JD, Berk BC. Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells. Dependence on tyrosine kinases and intracellular calcium. J Biol Chem 1999;274:143-150.
23. Ohnesorge N, Viemann D, Schmidt N, Czymai T, Spiering D, Schmolke M, Ludwig S, Roth J, Goebeler M, Schmidt M. Erk5 activation elicits a vasoprotective endothelial phenotype via induction of Kruppel-like factor 4 (KLF4). J Biol Chem 2010;285: 26199-26210.
24. McCullagh KA, Balian G. Collagen characterisation and cell transformation in human atherosclerosis. Nature 1975;258:73-75.
25. Johnson RC, Leopold JA, Loscalzo J. Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res 2006;99:1044-1059.
26. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 2010;16:1400-1406.
27. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res 2007; 67:10123-10128.
28. Cooley BC, Nevado J, Mellad J, Yang D, St HC, Negro A, Fang F, Chen G, San H, Walts AD, Schwartzbeck RL, Taylor B, Lanzer JD,Wragg A, Elagha A, Beltran LE, Berry C, Feil R, Virmani R, Ladich E, Kovacic JC, Boehm M. TGF-beta signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling. Sci Transl Med 2014;6:227ra34.
29. Yao Y, Jumabay M, Ly A, Radparvar M, Cubberly MR, Boström KI. A role for the endothelium in vascular calcification. Circ Res 2013;113:495-504.
30. Clowes AW, Collazzo RE, Karnovsky MJ. A morphologic and permeability study of luminal smooth muscle cells after arterial injury in the rat. Lab Invest 1978;39:141-150.
31. Clowes AW, Clowes MM, Reidy MA. Kinetics of cellular proliferation after arterial injury. III. Endothelial and smooth muscle growth in chronically denuded vessels. Lab Invest 1986;54:295-303.
32. Qiao L, Nishimura T, Shi L, Sessions D, Thrasher A, Trudell JR, Berry GJ, Pearl RG, Kao PN. Endothelial fate mapping in mice with pulmonary hypertension. Circulation 2014;129:692-703.
33. Sheikh AQ, Lighthouse JK, Greif DM. Recapitulation of developing artery muscularization in pulmonary hypertension. Cell Rep 2014;6:809-817.
34. Dickinson MG, Bartelds B, Borgdorff MA, Berger RM. The role of disturbed blood flow in the development of pulmonary arterial hypertension: lessons from preclinical animal models. Am J Physiol Lung Cell Mol Physiol 2013;305:L1-L14.
35. Dekker RJ, Van Soest S, Fontijn RD, Salamanca S, De Groot PG, VanBavel E, Pannekoek H, Horrevoets AJ. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Kruppel-like factor (KLF2). Blood 2002; 100:1689-1698.
36. Lee JS, Yu Q, Shin JT, Sebzda E, Bertozzi C, Chen M, Mericko P, Stadtfeld M, Zhou D, Cheng L, Graf T, MacRae CA, Lepore JJ, Lo CW, Kahn ML. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev Cell 2006;11:845-857.
37. Villarreal G Jr, Zhang Y, Larman HB, Gracia-Sancho J, Koo A, Garcia-Cardena G. Defining the regulation of KLF4 expression and its downstream transcriptional targets in vascular endothelial cells. Biochem Biophys Res Commun 2010;391:984-989.
38. Wang Z, Wang DZ, Pipes GC, Olson EN. Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci USA 2003;100:7129-7134.
39. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, Owens GK. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem 2005;280:9719-9727.
40. Adam PJ, Regan CP, Hautmann MB, Owens GK. Positive-and negative-acting Kruppellike transcription factors bind a transforming growth factor beta control element required for expression of the smooth muscle cell differentiation marker SM22alpha in vivo. J Biol Chem 2000;275:37798-37806.
41. Hu B, Wu Z, Liu T, Ullenbruch MR, Jin H, Phan SH. Gut-enriched Kruppel-like factor interaction with Smad3 inhibits myofibroblast differentiation. Am J Respir Cell Mol Biol 2007;36:78-84.
42. Yori JL, Seachrist DD, Johnson E, Lozada KL, Abdul-Karim FW, Chodosh LA, Schiemann WP, Keri RA. Kruppel-like factor 4 inhibits tumorigenic progression and metastasis in a mouse model of breast cancer. Neoplasia 2011;13:601-610.
43. Yori JL, Johnson E, Zhou G, Jain MK, Keri RA. Kruppel-like factor 4 inhibits epithelial-to-mesenchymal transition through regulation of E-cadherin gene expression. J Biol Chem 2010;285:16854-16863.
44. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83.
45. Cowan CE, Kohler EE, Dugan TA, Mirza MK, Malik AB,Wary KK. Kruppel-like factor-4 transcriptionally regulates VE-cadherin expression and endothelial barrier function. Circ Res 2010;107:959-966.
46. Komaravolu RK, Adam C, Moonen JR, Harmsen MC, Goebeler M, Schmidt M. Erk5 inhibits endothelial migration via KLF2-dependent downregulation of PAK1. Cardiovasc Res 2015;105:86-95.
47. Kalluri R. EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest 2009;119:1417-1419.
48. Ubil E, Duan J, Pillai IC, Rosa-Garrido M, Wu Y, Bargiacchi F, Lu Y, Stanbouly S, Huang J, Rojas M, Vondriska TM, Stefani E, Deb A. Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature 2014;514:585-590.
49. Lin K, Hsu PP, Chen BP, Yuan S, Usami S, Shyy JY, Li YS, Chien S. Molecular mechanism of endothelial growth arrest by laminar shear stress. Proc Natl Acad Sci USA 2000;97: 9385-9389.
50. Yoon HS, Chen X, Yang VW. Kruppel-like factor 4 mediates p53-dependent G1/S cell cycle arrest in response to DNA damage. J Biol Chem 2003;278:2101-2105.