Preexisting smooth muscle cells contribute to neointimal cell repopulation at an incidence varying widely among individual lesions

Surgery (United States)

Volumn 159, Issue 2, 2016, Pages 602-612

  Yang, Pu ^a   Hong, Michael S ^a   Fu, Chunhua ^a   Schmit, Bradley M ^a   Su, Yunchao ^b   Berceli, Scott A ^a,c   Jiang, Zhihua ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; COLLAGEN TYPE 1;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENDOTHELIAL MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; INCIDENCE; MALE; MOUSE; NEOINTIMA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; TUNICA MEDIA; ANIMAL; C57BL MOUSE; CELL MOTION; COMMON CAROTID ARTERY; FEMORAL ARTERY; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; CAROTID ARTERY, COMMON; CELL DIFFERENTIATION; CELL MOVEMENT; ENDOTHELIAL CELLS; FEMORAL ARTERY; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA;

EID: 84955169198     PISSN: 00396060     EISSN: 15327361     Source Type: Journal    
DOI: 10.1016/j.surg.2015.08.015     Document Type: Article

References (38)

1. H. Imai, K.J. Lee, S.K. Lee, K.T. Lee, R.M. O'Neal, and W.A. Thomas Ultrastructural features of aortic cells in mitosis in control and cholesterol-fed swine Lab Invest 23 1970 401 415
2. K.T. Lee, W.A. Thomas, R.A. Florentin, J.M. Reiner, and W.M. Lee Evidence for a polyclonal origin and proliferative heterogeneity of atherosclerotic lesions induced by dietary cholesterol in young swine Ann N Y Acad Sci 275 1976 336 347
3. A.W. Clowes, M.M. Clowes, and M.A. Reidy Kinetics of cellular proliferation after arterial injury. III. Endothelial and smooth muscle growth in chronically denuded vessels Lab Invest 54 1986 295 303
4. K. Tanaka, M. Sata, Y. Hirata, and R. Nagai Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries Circ Res 93 2003 783 790
5. Y. Hu, M. Mayr, B. Metzler, M. Erdel, F. Davison, and Q. Xu Both donor and recipient origins of smooth muscle cells in vein graft atherosclerotic lesions Circ Res 91 2002 e13 e20
6. Y. Shi, J.E. O'Brien Jr., J.D. Mannion, R.C. Morrison, W. Chung, A. Fard, and et al. Remodeling of autologous saphenous vein grafts. The role of perivascular myofibroblasts Circulation 95 1997 2684 2693
7. Z. Tang, A. Wang, F. Yuan, Z. Yan, B. Liu, J.S. Chu, and et al. Differentiation of multipotent vascular stem cells contributes to vascular diseases Nat Commun 3 2012 875
8. Y. Hu, Z. Zhang, E. Torsney, A.R. Afzal, F. Davison, B. Metzler, and et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice J Clin Invest 113 2004 1258 1265
9. A.T. Nguyen, D. Gomez, R.D. Bell, J.H. Campbell, A.W. Clowes, G. Gabbiani, and et al. Smooth muscle cell plasticity: fact or fiction? Circ Res 112 2013 17 22
10. Z. Tang, A. Wang, D. Wang, and S. Li Smooth muscle cells: to be or not to be? Response to Nguyen et Al Circ Res 112 2013 23 26
11. R.A. Nemenoff, H. Horita, A.C. Ostriker, S.B. Furgeson, P.A. Simpson, V. VanPutten, and et al. SDF-1alpha induction in mature smooth muscle cells by inactivation of PTEN is a critical mediator of exacerbated injury-induced neointima formation Arterioscler Thromb Vasc Biol 31 2011 1300 1308
12. B.P. Herring, A.M. Hoggatt, C. Burlak, and S. Offermanns Previously differentiated medial vascular smooth muscle cells contribute to neointima formation following vascular injury Vasc Cell 6 2014 21
13. W. Li, Q. Li, Y. Jiao, L. Qin, R. Ali, J. Zhou, and et al. Tgfbr2 disruption in postnatal smooth muscle impairs aortic wall homeostasis J Clin Invest 124 2014 755 767
14. P.Y. Chen, L. Qin, C. Barnes, K. Charisse, T. Yi, X. Zhang, and et al. FGF Regulates TGF-beta Signaling and Endothelial-to-Mesenchymal Transition via Control of let-7 miRNA Expression Cell Rep 2 2012 1684 1696
15. B.C. Cooley, J. Nevado, J. Mellad, D. Yang, H.C. St, A. Negro, and et al. TGF-beta signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling Sci Transl Med 6 2014 227ra34
16. C.P. Regan, P.J. Adam, C.S. Madsen, and G.K. Owens Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury J Clin Invest 106 2000 1139 1147
17. J.R. Gothert, S.E. Gustin, J.A. van Eekelen, U. Schmidt, M.A. Hall, S.M. Jane, and et al. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium Blood 104 2004 1769 1777
18. Z. Jiang, M. Tao, K.A. Omalley, D. Wang, C.K. Ozaki, and S.A. Berceli Established neointimal hyperplasia in vein grafts expands via TGF-beta-mediated progressive fibrosis Am J Physiol Heart Circ Physiol 297 2009 200 207
19. C. Fu, P. Yu, M. Tao, T. Gupta, L.L. Moldawer, S.A. Berceli, and et al. Monocyte chemoattractant protein-1/CCR2 axis promotes vein graft neointimal hyperplasia through its signaling in graft-extrinsic cell populations Arterioscler Thromb Vasc Biol 32 2012 2418 2426
20. T. Jokela, and S. Vainio Conditional tamoxifen Cre induced mutagenesis in the embryonic kidney in organ culture Genesis 45 2007 757 761
21. E.M. Zeisberg, O. Tarnavski, M. Zeisberg, A.L. Dorfman, J.R. McMullen, E. Gustafsson, and et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis Nat Med 13 2007 952 961
22. S. Piera-Velazquez, Z. Li, and S.A. Jimenez Role of endothelial-mesenchymal transition (EndoMT) in the pathogenesis of fibrotic disorders Am J Pathol 179 2011 1074 1080
23. L. Maddaluno, N. Rudini, R. Cuttano, L. Bravi, C. Giampietro, M. Corada, and et al. EndMT contributes to the onset and progression of cerebral cavernous malformations Nature 498 2013 492 496
24. C.P. Regan, I. Manabe, and G.K. Owens Development of a smooth muscle-targeted cre recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation Circ Res 87 2000 363 369
25. V. Naik, E.M. Leaf, J.H. Hu, H.Y. Yang, N.B. Nguyen, C.M. Giachelli, and et al. Sources of cells that contribute to atherosclerotic intimal calcification: an in vivo genetic fate mapping study Cardiovasc Res 94 2012 545 554
26. Z. Shen, C. Li, R.A. Frieler, A.S. Gerasimova, S.J. Lee, J. Wu, and et al. Smooth muscle protein 22 alpha-Cre is expressed in myeloid cells in mice Biochem Biophys Res Commun 422 2012 639 642
27. A. Wirth, Z. Benyo, M. Lukasova, B. Leutgeb, N. Wettschureck, S. Gorbey, and et al. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension Nat Med 14 2008 64 68
28. G.K. Owens, M.S. Kumar, and B.R. Wamhoff Molecular regulation of vascular smooth muscle cell differentiation in development and disease Physiol Rev 84 2004 767 801
29. A.S. Cuttler, R.J. LeClair, J.P. Stohn, Q. Wang, C.M. Sorenson, L. Liaw, and et al. Characterization of Pdgfrb-Cre transgenic mice reveals reduction of ROSA26 reporter activity in remodeling arteries Genesis 49 2011 673 680
30. M. Sata, D. Fukuda, K. Tanaka, Y. Kaneda, H. Yashiro, and I. Shirakawa The role of circulating precursors in vascular repair and lesion formation J Cell Mol Med 9 2005 557 568
31. J.F. Bentzon, C.S. Sondergaard, M. Kassem, and E. Falk Smooth muscle cells healing atherosclerotic plaque disruptions are of local, not blood, origin in apolipoprotein E knockout mice Circulation 116 2007 2053 2061
32. J.M. Daniel, W. Bielenberg, P. Stieger, S. Weinert, H. Tillmanns, and D.G. Sedding Time-course analysis on the differentiation of bone marrow-derived progenitor cells into smooth muscle cells during neointima formation Arterioscler Thromb Vasc Biol 30 2010 1890 1896
33. H. Iwata, I. Manabe, K. Fujiu, T. Yamamoto, N. Takeda, K. Eguchi, and et al. Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages Circulation 122 2010 2048 2057
34. A.H. Kumar, P. Metharom, J. Schmeckpeper, S. Weiss, K. Martin, and N.M. Caplice Bone marrow-derived CX3CR1 progenitors contribute to neointimal smooth muscle cells via fractalkine CX3CR1 interaction FASEB J 24 2010 81 92
35. P. Metharom, A.H. Kumar, S. Weiss, and N.M. Caplice A specific subset of mouse bone marrow cells has smooth muscle cell differentiation capacity-brief report Arterioscler Thromb Vasc Biol 30 2010 533 535
36. M. Giel-Moloney, D.S. Krause, G. Chen, R.A. Van Etten, and A.B. Leiter Ubiquitous and uniform in vivo fluorescence in ROSA26-EGFP BAC transgenic mice Genesis 45 2007 83 89
37. E. Arciniegas, M.G. Frid, I.S. Douglas, and K.R. Stenmark Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension Am J Physiol Lung Cell Mol Physiol 293 2007 L1 L8
38. W.C. Aird Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms Circ Res 100 2007 158 173