N-cadherin induction by ECM stiffness and FAK overrides the spreading requirement for proliferation of vascular smooth muscle cells

Cell Reports

Volumn 10, Issue 9, 2015, Pages 1477-1486

  Mui, Keeley L ^a,b   Bae, Yong Ho ^a,b   Gao, Lin ^c   Liu, Shu Lin ^a,b   Xu, Tina ^a,b   Radice, Glenn L ^d   Chen, Christopher S ^c,e   Assoian, Richard K ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; FOCAL ADHESION KINASE; NERVE CELL ADHESION MOLECULE; RAC PROTEIN; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL ADHESION; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX STIFFNESS; GENE DELETION; GENE EXPRESSION REGULATION; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; N CADHERIN GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

EID: 84924584490     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.023     Document Type: Article

References (59)

1. Assoian R.K., Klein E.A. Growth control by intracellular tension and extracellular stiffness. Trends Cell Biol. 2008, 7:24-27.
2. Bae Y.H., Mui K.L., Hsu B.Y., Liu S.-L., Cretu A., Razinia Z., Xu T., Puré E., Assoian R.K. A FAK-Cas-Rac-lamellipodin signaling module transduces extracellular matrix stiffness into mechanosensitive cell cycling. Sci. Signal. 2014, 7:ra57.
3. Baumeister U., Funke R., Ebnet K., Vorschmitt H., Koch S., Vestweber D. Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J. 2005, 24:1686-1695.
4. Braga V.M., Betson M., Li X., Lamarche-Vane N. Activation of the small GTPase Rac is sufficient to disrupt cadherin-dependent cell-cell adhesion in normal human keratinocytes. Mol. Biol. Cell 2000, 11:3703-3721.
5. Cary L.A., Han D.C., Polte T.R., Hanks S.K., Guan J.L. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J.Cell Biol. 1998, 140:211-221.
6. Chalasani K., Brewster R.M. N-cadherin-mediated cell adhesion restricts cell proliferation in the dorsal neural tube. Mol. Biol. Cell 2011, 22:1505-1515.
7. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276:1425-1428.
8. Chopra A., Tabdanov E., Patel H., Janmey P.A., Kresh J.Y. Cardiac myocyte remodeling mediated by N-cadherin-dependent mechanosensing. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H1252-H1266.
9. Chrzanowska-Wodnicka M., Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J.Cell Biol. 1996, 133:1403-1415.
10. Conway D.E., Breckenridge M.T., Hinde E., Gratton E., Chen C.S., Schwartz M.A. Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1. Curr. Biol. 2013, 23:1024-1030.
11. Desprat N., Supatto W., Pouille P.-A., Beaurepaire E., Farge E. Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev. Cell 2008, 15:470-477.
12. Dupont S., Morsut L., Aragona M., Enzo E., Giulitti S., Cordenonsi M., Zanconato F., Le Digabel J., Forcato M., Bicciato S., et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
13. Fonseca P.M., Shin N.-Y., Brábek J., Ryzhova L., Wu J., Hanks S.K. Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell. Signal. 2004, 16:621-629.
14. Fournier A.K., Campbell L.E., Castagnino P., Liu W.F., Chung B.M., Weaver V.M., Chen C.S., Assoian R.K. Rac-dependent cyclin D1 gene expression regulated by cadherin- and integrin-mediated adhesion. J.Cell Sci. 2008, 121:226-233.
15. Gao L., McBeath R., Chen C.S. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 2010, 28:564-572.
16. Geiger B., Bershadsky A., Pankov R., Yamada K.M. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
17. Grazia Lampugnani M., Zanetti A., Corada M., Takahashi T., Balconi G., Breviario F., Orsenigo F., Cattelino A., Kemler R., Daniel T.O., Dejana E. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J.Cell Biol. 2003, 161:793-804.
18. Haÿ E., Nouraud A., Marie P.J. N-cadherin negatively regulates osteoblast proliferation and survival by antagonizing Wnt, ERK and PI3K/Akt signalling. PLoS ONE 2009, 4:e8284.
19. Janmey P.A., Wells R.G., Assoian R.K., McCulloch C.A. From tissue mechanics to transcription factors. Differentiation 2013, 86:112-120.
20. Jones M., Sabatini P.J., Lee F.S., Bendeck M.P., Langille B.L. N-cadherin upregulation and function in response of smooth muscle cells to arterial injury. Arterioscler. Thromb. Vasc. Biol. 2002, 22:1972-1977.
21. Kim N.-G., Koh E., Chen X., Gumbiner B.M. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl. Acad. Sci. USA 2011, 108:11930-11935.
22. Klein E.A., Yin L., Kothapalli D., Castagnino P., Byfield F.J., Xu T., Levental I., Hawthorne E., Janmey P.A., Assoian R.K. Cell-cycle control by physiological matrix elasticity and invivo tissue stiffening. Curr. Biol. 2009, 19:1511-1518.
23. Kothapalli D., Zhao L., Hawthorne E.A., Cheng Y., Lee E., Puré E., Assoian R.K. Hyaluronan and CD44 antagonize mitogen-dependent cyclin D1 expression in mesenchymal cells. J.Cell Biol. 2007, 176:535-544.
24. le Duc Q., Shi Q., Blonk I., Sonnenberg A., Wang N., Leckband D., de Rooij J. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J.Cell Biol. 2010, 189:1107-1115.
25. McClatchey A.I., Yap A.S. Contact inhibition (of proliferation) redux. Curr. Opin. Cell Biol. 2012, 24:685-694.
26. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 2006, 18:516-523.
27. Nelson C.M., Chen C.S. Cell-cell signaling by direct contact increases cell proliferation via a PI3K-dependent signal. FEBS Lett. 2002, 514:238-242.
28. Nelson C.M., Pirone D.M., Tan J.L., Chen C.S. Vascular endothelial-cadherin regulates cytoskeletal tension, cell spreading, and focal adhesions by stimulating RhoA. Mol. Biol. Cell 2004, 15:2943-2953.
29. Nelson C.M., Liu W.F., Chen C.S. Manipulation of cell-cell adhesion using bowtie-shaped microwells. Methods Mol. Biol. 2007, 370:1-10.
30. Oda H., Tsukita S., Takeichi M. Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev. Biol. 1998, 203:435-450.
31. Owens G.K., Kumar M.S., Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 2004, 84:767-801.
32. Parsons J.T., Horwitz A.R., Schwartz M.A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 2010, 11:633-643.
33. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
34. Pelham R.J., Wang Yl. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 1997, 94:13661-13665.
35. Radice G.L., Rayburn H., Matsunami H., Knudsen K.A., Takeichi M., Hynes R.O. Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 1997, 181:64-78.
36. Reddy P., Liu L., Ren C., Lindgren P., Boman K., Shen Y., Lundin E., Ottander U., Rytinki M., Liu K. Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol. Endocrinol. 2005, 19:2564-2578.
37. Resink T.J., Philippova M., Joshi M.B., Kyriakakis E., Erne P. Cadherins and cardiovascular disease. Swiss Med. Wkly. 2009, 139:122-134.
38. Robinson B.S., Moberg K.H. Cell-cell junctions: α-catenin and E-cadherin help fence in Yap1. Curr. Biol. 2011, 21:R890-R892.
39. Ruest P.J., Shin N.Y., Polte T.R., Zhang X., Hanks S.K. Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 2001, 21:7641-7652.
40. Sabatini P.J.B., Zhang M., Silverman-Gavrila R., Bendeck M.P., Langille B.L. Homotypic and endothelial cell adhesions via N-cadherin determine polarity and regulate migration of vascular smooth muscle cells. Circ. Res. 2008, 103:405-412.
41. Sakane F., Miyamoto Y. N-cadherin regulates the proliferation and differentiation of ventral midbrain dopaminergic progenitors. Dev. Neurobiol. 2013, 73:518-529.
42. Sata M., Maejima Y., Adachi F., Fukino K., Saiura A., Sugiura S., Aoyagi T., Imai Y., Kurihara H., Kimura K., et al. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J.Mol. Cell. Cardiol. 2000, 32:2097-2104.
43. Schaller M.D., Hildebrand J.D., Shannon J.D., Fox J.W., Vines R.R., Parsons J.T. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 1994, 14:1680-1688.
44. Schlaepfer D.D., Hunter T. Evidence for invivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 1996, 16:5623-5633.
45. Schwartz M.A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2010, 2:a005066.
46. Silvis M.R., Kreger B.T., Lien W.-H., Klezovitch O., Rudakova G.M., Camargo F.D., Lantz D.M., Seykora J.T., Vasioukhin V. α-Catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci. Signal. 2011, 4:ra33.
47. Solon J., Levental I., Sengupta K., Georges P.C., Janmey P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 2007, 93:4453-4461.
48. Stockinger A., Eger A., Wolf J., Beug H., Foisner R. E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J.Cell Biol. 2001, 154:1185-1196.
49. Takaishi K., Sasaki T., Kotani H., Nishioka H., Takai Y. Regulation of cell-cell adhesion by rac and rho small G proteins in MDCK cells. J.Cell Biol. 1997, 139:1047-1059.
50. Tang Y., Rowe R.G., Botvinick E.L., Kurup A., Putnam A.J., Seiki M., Weaver V.M., Keller E.T., Goldstein S., Dai J., et al. MT1-MMP-dependent control of skeletal stem cell commitment via a β1-integrin/YAP/TAZ signaling axis. Dev. Cell 2013, 25:402-416.
51. Tinkle C.L., Lechler T., Pasolli H.A., Fuchs E. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc. Natl. Acad. Sci. USA 2004, 101:552-557.
52. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell Biol. 2000, 2:E231-E236.
53. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., Cao G., DeLisser H., Schwartz M.A. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437:426-431.
54. Uglow E.B., Slater S., Sala-Newby G.B., Aguilera-Garcia C.M., Angelini G.D., Newby A.C., George S.J. Dismantling of cadherin-mediated cell-cell contacts modulates smooth muscle cell proliferation. Circ. Res. 2003, 92:1314-1321.
55. Watanabe T., Sato K., Kaibuchi K. Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. Cold Spring Harb. Perspect. Biol. 2009, 1:a003020.
56. Wildenberg G.A., Dohn M.R., Carnahan R.H., Davis M.A., Lobdell N.A., Settleman J., Reynolds A.B. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006, 127:1027-1039.
57. Woods A., Wang G., Dupuis H., Shao Z., Beier F. Rac1 signaling stimulates N-cadherin expression, mesenchymal condensation, and chondrogenesis. J.Biol. Chem. 2007, 282:23500-23508.
58. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
59. Zhu A.J., Watt F.M. Expression of a dominant negative cadherin mutant inhibits proliferation and stimulates terminal differentiation of human epidermal keratinocytes. J.Cell Sci. 1996, 109:3013-3023.