Integrin β3 inhibition is a therapeutic strategy for supravalvular aortic stenosis

Journal of Experimental Medicine

Volumn 213, Issue 3, 2016, Pages 451-463

  Misra, Ashish ^a   Sheikh, Abdul Q ^a   Kumar, Abhishek ^a   Luo, Jiesi ^a   Zhang, Jiasheng ^a   Hinton, Robert B ^b   Smoot, Leslie ^c   Kaplan, Paige ^d   Urban, Zsolt ^e   Qyang, Yibing ^a   Tellides, George ^a   Greif, Daniel M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA3 INTEGRIN; CILENGITIDE; ELASTIN; FOCAL ADHESION KINASE; MYOSIN HEAVY CHAIN;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA MEDIA; AORTA SUPRAVALVULAR STENOSIS; AORTA WALL; ARTICLE; CELL DEDIFFERENTIATION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTINUOUS INFUSION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME PHOSPHORYLATION; EXPLANT; FEMALE; FETUS; GENE DOSAGE; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MALE; MOUSE; NEWBORN; NONHUMAN; OSMOTIC PUMP; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ANIMAL; AORTA; AORTIC STENOSIS, SUPRAVALVULAR; C57BL MOUSE; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; MUTATION; PATHOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA; AORTIC STENOSIS, SUPRAVALVULAR; CELL DEDIFFERENTIATION; CELL PROLIFERATION; DOWN-REGULATION; ELASTIN; GENE DOSAGE; HUMANS; INTEGRIN BETA3; MICE, INBRED C57BL; MOLECULAR TARGETED THERAPY; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; SIGNAL TRANSDUCTION;

EID: 84961219000     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150688     Document Type: Article

References (47)

1. Arciniegas, E., M.G. Frid, I.S. Douglas, and K.R. Stenmark. 2007. Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L1-L8. http://dx.doi.org/10.1152/ajplung.00378.2006
2. Arjonen, A., R. Kaukonen, and J. Ivaska. 2011. Filopodia and adhesion in cancer cell motility. Cell Adhes. Migr. 5:421-430. http://dx.doi.org/10.4161/cam.5.5.17723
3. Chen, P.Y., L. Qin, C. Barnes, K. Charisse, T. Yi, X. Zhang, R. Ali, P.P. Medina, J. Yu, F.J. Slack, et al. 2012. FGF regulates TGF-β signaling and endothelialto-mesenchymal transition via control of let-7 miRNA expression. Cell Reports. 2:1684-1696. http://dx.doi.org/10.1016/j.celrep.2012.10.021
4. Choi, E.T., M.F. Khan, J.E. Leidenfrost, E.T. Collins, K.P. Boc, B.R. Villa, D.V. Novack, W.C. Parks, and D.R. Abendschein. 2004. β3-integrin mediates smooth muscle cell accumulation in neointima after carotid ligation in mice. Circulation. 109:1564-1569. http://dx.doi.org/10.1161/01.CIR.0000121733.68724.FF
5. Curran, M.E., D.L. Atkinson, A.K. Ewart, C.A. Morris, M.F. Leppert, and M.T. Keating. 1993. The elastin gene is disrupted by a translocation associated with supravalvular aortic stenosis. Cell. 73:159-168. http://dx.doi.org/10.1016/0092-8674(93)90168-P
6. Dechantsreiter, M.A., E. Planker, B. Mathä, E. Lohof, G. Hölzemann, A. Jonczyk, S.L. Goodman, and H. Kessler. 1999. N-Methylated cyclic RGD peptides as highly active and selective αVβ3 integrin antagonists. J. Med. Chem. 42:3033-3040. http://dx.doi.org/10.1021/jm970832g
7. DeRuiter, M.C., R.E. Poelmann, J.C. VanMunsteren, V. Mironov, R.R. Markwald, and A.C. Gittenberger-de Groot. 1997. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ. Res. 80:444-451. http://dx.doi.org/10.1161/01.RES.80.4.444
8. Feil, S., F. Hofmann, and R. Feil. 2004. SM22α modulates vascular smooth muscle cell phenotype during atherogenesis. Circ. Res. 94:863-865. http://dx.doi.org/10.1161/01.RES.0000126417.38728.F6
9. Ge, X., Y. Ren, O. Bartulos, M.Y. Lee, Z. Yue, K.Y. Kim, W. Li, P.J. Amos, E.C. Bozkulak, A. Iyer, et al. 2012. Modeling supravalvular aortic stenosis syndrome with human induced pluripotent stem cells. Circulation. 126:1695-1704. http://dx.doi.org/10.1161/CIRCULATIONAHA.112.116996
10. Greif, D.M., M. Kumar, J.K. Lighthouse, J. Hum, A. An, L. Ding, K. Red-Horse, F.H. Espinoza, L. Olson, S. Offermanns, and M.A. Krasnow. 2012. Radial construction of an arterial wall. Dev. Cell. 23:482-493. http://dx.doi.org/10.1016/j.devcel.2012.07.009
11. Herring, B.P., A.M. Hoggatt, C. Burlak, and S. Offermanns. 2014. Previously differentiated medial vascular smooth muscle cells contribute to neointima formation following vascular injury. Vasc. Cell. 6:21. http://dx.doi.org/10.1186/2045-824X-6-21
12. Hodivala-Dilke, K.M., K.P. McHugh, D.A. Tsakiris, H. Rayburn, D. Crowley, M. Ullman-Culleré, F.P. Ross, B.S. Coller, S. Teitelbaum, and R.O. Hynes. 1999. β3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J. Clin. Invest. 103:229-238. http://dx.doi.org/10.1172/JCI5487
13. Hoshiga, M., C.E. Alpers, L.L. Smith, C.M. Giachelli, and S.M. Schwartz. 1995. αVβ3 integrin expression in normal and atherosclerotic artery. Circ. Res. 77:1129-1135. http://dx.doi.org/10.1161/01.RES.77.6.1129
14. Karnik, S.K., B.S. Brooke, A. Bayes-Genis, L. Sorensen, J.D. Wythe, R.S. Schwartz, M.T. Keating, and D.Y. Li. 2003. A critical role for elastin signaling in vascular morphogenesis and disease. Development. 130:411-423. http://dx.doi.org/10.1242/dev.00223
15. Lawler, J., R. Weinstein, and R.O. Hynes. 1988. Cell attachment to thrombospondin: the role of ARG-GLY-ASP, calcium, and integrin receptors. J. Cell Biol. 107:2351-2361. http://dx.doi.org/10.1083/jcb.107.6.2351
16. Li, D.Y., B. Brooke, E.C. Davis, R.P. Mecham, L.K. Sorensen, B.B. Boak, E. Eichwald, and M.T. Keating. 1998a. Elastin is an essential determinant of arterial morphogenesis. Nature. 393:276-280. http://dx.doi.org/10.1038/30522
17. Li, D.Y., G. Faury, D.G. Taylor, E.C. Davis, W.A. Boyle, R.P. Mecham, P. Stenzel, B. Boak, and M.T. Keating. 1998b. Novel arterial pathology in mice and humans hemizygous for elastin. J. Clin. Invest. 102:1783-1787. http://dx.doi.org/10.1172/JCI4487
18. Li, W., Q. Li, L. Qin, R. Ali, Y. Qyang, M. Tassabehji, B.R. Pober, W.C. Sessa, F.J. Giordano, and G. Tellides. 2013. Rapamycin inhibits smooth muscle cell proliferation and obstructive arteriopathy attributable to elastin deficiency. Arterioscler. Thromb. Vasc. Biol. 33:1028-1035. http://dx.doi.org/10.1161/ATVBAHA.112.300407
19. Maile, L.A., W.H. Busby, T.C. Nichols, D.A. Bellinger, E.P. Merricks, M. Rowland, U. Veluvolu, and D.R. Clemmons. 2010. A monoclonal antibody against αVβ3 integrin inhibits development of atherosclerotic lesions in diabetic pigs. Sci. Transl. Med. 2:18ra11. http://dx.doi.org/10.1126/scitranslmed.3000476
20. Miano, J.M., P. Cserjesi, K.L. Ligon, M. Periasamy, and E.N. Olson. 1994. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ. Res. 75:803-812. http://dx.doi.org/10.1161/01.RES.75.5.803
21. Morimoto, M., Z. Liu, H.T. Cheng, N. Winters, D. Bader, and R. Kopan. 2010. Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J. Cell Sci. 123:213-224. http://dx.doi.org/10.1242/jcs.058669
22. Muzumdar, M.D., B. Tasic, K. Miyamichi, L. Li, and L. Luo. 2007. A global double-fluorescent Cre reporter mouse. Genesis. 45:593-605. http://dx.doi.org/10.1002/dvg.20335
23. Owens, G.K., M.S. Kumar, and B.R. Wamhoff. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84:767-801. http://dx.doi.org/10.1152/physrev.00041.2003
24. Pampori, N., T. Hato, D.G. Stupack, S. Aidoudi, D.A. Cheresh, G.R. Nemerow, and S.J. Shattil. 1999. Mechanisms and consequences of affinity modulation of integrin αVβ3 detected with a novel patch-engineered monovalent ligand. J. Biol. Chem. 274:21609-21616. http://dx.doi.org/10.1074/jbc.274.31.21609
25. Pober, B.R., M. Johnson, and Z. Urban. 2008. Mechanisms and treatment of cardiovascular disease in Williams-Beuren syndrome. J. Clin. Invest. 118:1606-1615. http://dx.doi.org/10.1172/JCI35309
26. Qiao, L., T. Nishimura, L. Shi, D. Sessions, A. Thrasher, J.R. Trudell, G.J. Berry, R.G. Pearl, and P.N. Kao. 2014. Endothelial fate mapping in mice with pulmonary hypertension. Circulation. 129:692-703. http://dx.doi.org/10.1161/CIRCULATIONAHA.113.003734
27. Raines, E.W., and R. Ross. 1993. Smooth muscle cells and the pathogenesis of the lesions of atherosclerosis. Br. Heart J. 69(1 Suppl):S30-S37. http://dx.doi.org/10.1136/hrt.69.1_Suppl.S30
28. Ranchoux, B., F. Antigny, C. Rucker-Martin, A. Hautefort, C. Péchoux, H.J. Bogaard, P. Dorfmüller, S. Remy, F. Lecerf, S. Planté, et al. 2015. Endothelial-to-mesenchymal transition in pulmonary hypertension. Circulation. 131:1006-1018. http://dx.doi.org/10.1161/CIRCULATIONAHA.114.008750
29. Rinkevich, Y., P. Lindau, H. Ueno, M.T. Longaker, and I.L. Weissman. 2011. Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature. 476:409-413. http://dx.doi.org/10.1038/nature10346
30. Sandberg, L.B., N.T. Soskel, and J.G. Leslie. 1981. Elastin structure, biosynthesis, and relation to disease states. N. Engl. J. Med. 304:566-579. http://dx.doi.org/10.1056/NEJM198103053041004
31. Scheppke, L., E.A. Murphy, A. Zarpellon, J.J. Hofmann, A. Merkulova, D.J. Shields, S.M. Weis, T.V. Byzova, Z.M. Ruggeri, M.L. Iruela-Arispe, and D.A. Cheresh. 2012. Notch promotes vascular maturation by inducing integrin-mediated smooth muscle cell adhesion to the endothelial basement membrane. Blood. 119:2149-2158. http://dx.doi.org/10.1182/blood-2011-04-348706
32. Schneider, J.G., Y. Zhu, T. Coleman, and C.F. Semenkovich. 2007. Macrophage β3 integrin suppresses hyperlipidemia-induced inflammation by modulating TNFα expression. Arterioscler. Thromb. Vasc. Biol. 27:2699-2706. http://dx.doi.org/10.1161/ATVBAHA.107.153650
33. Seidelmann, S.B., J.K. Lighthouse, and D.M. Greif. 2014. Development and pathologies of the arterial wall. Cell. Mol. Life Sci. 71:1977-1999. http://dx.doi.org/10.1007/s00018-013-1478-y
34. Shankman, L.S., D. Gomez, O.A. Cherepanova, M. Salmon, G.F. Alencar, R.M. Haskins, P. Swiatlowska, A.A. Newman, E.S. Greene, A.C. Straub, et al. 2015. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat. Med. 21:628-637. http://dx.doi.org/10.1038/nm.3866
35. Sheikh, A.Q., J.K. Lighthouse, and D.M. Greif. 2014. Recapitulation of developing artery muscularization in pulmonary hypertension. Cell Reports. 6:809-817. http://dx.doi.org/10.1016/j.celrep.2014.01.042
36. Sheikh, A.Q., A. Misra, I.O. Rosas, R.H. Adams, and D.M. Greif. 2015. Smooth muscle cell progenitors are primed to muscularize in pulmonary hypertension. Sci. Transl. Med. 7:308ra159. http://dx.doi.org/10.1126/scitranslmed.aaa9712
37. Shifren, A., A.G. Durmowicz, R.H. Knutsen, E. Hirano, and R.P. Mecham. 2007. Elastin protein levels are a vital modifier affecting normal lung development and susceptibility to emphysema. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:L778-L787. http://dx.doi.org/10.1152/ajplung.00352.2006
38. Stouffer, G.A., Z. Hu, M. Sajid, H. Li, G. Jin, M.T. Nakada, S.R. Hanson, and M.S. Runge. 1998. β3 integrins are upregulated after vascular injury and modulate thrombospondin- and thrombin-induced proliferation of cultured smooth muscle cells. Circulation. 97:907-915. http://dx.doi.org/10.1161/01.CIR.97.9.907
39. Streuli, C.H. 2009. Integrins and cell-fate determination. J. Cell Sci. 122:171-177. http://dx.doi.org/10.1242/jcs.018945
40. Stupp, R., M.E. Hegi, T. Gorlia, S.C. Erridge, J. Perry, Y.K. Hong, K.D. Aldape, B. Lhermitte, T. Pietsch, D. Grujicic, et al. CEN TRIC Study Team. 2014. Cilengitide combined with standard treatment for patients with newly diagnosed glioblastoma with methylated MGMT promoter (CEN TRIC EOR TC 26071-22072 study): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 15:1100-1108. http://dx.doi.org/10.1016/S1470-2045(14)70379-1
41. Urbán, Z., S. Riazi, T.L. Seidl, J. Katahira, L.B. Smoot, D. Chitayat, C.D. Boyd, and A. Hinek. 2002. Connection between elastin haploinsufficiency and increased cell proliferation in patients with supravalvular aortic stenosis and Williams-Beuren syndrome. Am. J. Hum. Genet. 71:30-44. http://dx.doi.org/10.1086/341035
42. Wagenseil, J.E., C.H. Ciliberto, R.H. Knutsen, M.A. Levy, A. Kovacs, and R.P. Mecham. 2009. Reduced vessel elasticity alters cardiovascular structure and function in newborn mice. Circ. Res. 104:1217-1224. http://dx.doi.org/10.1161/CIRCRESAHA.108.192054
43. Wagenseil, J.E., C.H. Ciliberto, R.H. Knutsen, M.A. Levy, A. Kovacs, and R.P. Mecham. 2010. The importance of elastin to aortic development in mice. Am. J. Physiol. Heart Circ. Physiol. 299:H257-H264. http://dx.doi.org/10.1152/ajpheart.00194.2010
44. Wang, Y., M. Nakayama, M.E. Pitulescu, T.S. Schmidt, M.L. Bochenek, A. Sakakibara, S. Adams, A. Davy, U. Deutsch, U. Lüthi, et al. 2010. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 465:483-486. http://dx.doi.org/10.1038/nature09002
45. Wendling, O., J.M. Bornert, P. Chambon, and D. Metzger. 2009. Efficient temporally-controlled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis. 47:14-18. http://dx.doi.org/10.1002/dvg.20448
46. Weng, S., L. Zemany, K.N. Standley, D.V. Novack, M. La Regina, C. Bernal-Mizrachi, T. Coleman, and C.F. Semenkovich. 2003. β3 integrin deficiency promotes atherosclerosis and pulmonary inflammation in high-fat-fed, hyperlipidemic mice. Proc. Natl. Acad. Sci. USA. 100:6730-6735. http://dx.doi.org/10.1073/pnas.1137612100
47. Yamashita, J., H. Itoh, M. Hirashima, M. Ogawa, S. Nishikawa, T. Yurugi, M. Naito, K. Nakao, and S. Nishikawa. 2000. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 408:92-96. http://dx.doi.org/10.1038/35040568