Актиновый цитоскелет эндотелиоцитов — структурные особенности организации на страже барьерной функции

Сноски

* Адресат для корреспонденции.

Финансирование

Работа поддержана РФФИ (грант 18-29-09082) и программой развития Московского университета (MSU Development Program PNR 5.13).

Конфликт интересов

Авторы заявляют об отсутствии конфликта интересов.

Список литературы

1. Ware, L.B., and Matthay, M.A. (2000) The acute respiratory distress syndrome, New Engl. J. Med., 342, 1344–1349, doi: 10.1056/NEJM200005043421806.

2. Garcia, J.G., Davis, H.W., and Patterson, C.E. (1995) Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation, J. Cell. Physiol., 163, 510–522, doi: 10.1002/jcp.1041630311.

3. Garcia, J.G., Verin, A.D., and Schaphorst, K.L. (1996) Regulation of thrombin-mediated endothelial cell contraction and permeability, Semin. Thromb. Hemostasis, 22, 309–315, doi: 10.1055/s-2007-999025.

4. Lum, H., and Malik, A.B. (1996) Mechanisms of increased endothelial permeability, Can. J. Physiol. Pharmacol., 74, 787–800.

5. Dudek, S., and Garcia, J. (2001) Cytoskeletal regulation of pulmonary vascular permeability, J. Appl. Physiol., 91, 1487–1500, doi: 10.1152/jappl.2001.91.4.1487.

6. Groeneveld, A.B.J. (2002) Vascular pharmacology of acute lung injury and acute respiratory distress syndrome, Vascular Pharmacol., 39, 247–256, doi: 10.1016/S1537-1891(03)00013-2.

7. Amann, K.J., and Pollard, T.D. (2000) Cellular regulation of actin network assembly, Curr. Biol., 10, 728–730, doi: 10.1016/S0960-9822(00)00751-X.

8. Shasby, D.M, Shasby, S.S., Sullivan, J.M., and Peach, M.J. (1982) Role of endothelial cell cytoskeleton in control of endothelial permeability, Circ. Res., 51, 657–661.

9. Phillips, P.G., Lum, H., Malik, A.B., and Tsan, M.F. (1989) Phallacidin prevents thrombin-induced increases in endothelial permeability to albumin, Am. J. Physiol., 257, 562–567, doi: 10.1152/ajpcell.1989.257.3.C562.

10. Dejan, E., Bazzoni, G., and Lampugnani, M.G. (1999) Vascular endothelial (VE)-cadherin: only an intercellular glue, Exp. Cell. Res., 252, 13–19, doi: 10.1006/excr.1999.4601.

11. Bazzoni, G., and Dejana, E. (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis, Physiol. Rev., 84, 869–901, doi: 10.1152/physrev.00035.2003.

12. Moreno, V., Gonzalo, P., Gomez-Escudero, J., Pollan, A., Acin-Perez, R., Breckenridge, M., Yanez-Mo, M., Barreiro, O., Orsenigo, F., Kadomatsu, K., Chen, C.S., Enriquez, J.A., Dejana, E., Sanchez-Madrid, F., and Arroyo, A.G. (2014) An emmprin-γ-catenin-Nm23 complex drives ATP production and actomyosin contractility at endothelial junctions, J. Cell Sci., 127, 3768–3781, doi: 10.1242/jcs.149518.

13. Giampietro, C., Disanza, A., Bravi, L., Barrios-Rodiles, M., Corada, M., Frittoli, E., Savorani, C., Lampugnani, M.G., Boggetti, B., Niessen, C., Wrana, J.L., Scita, G., and Dejana, E. (2015) The actin-binding protein EPS8 binds VE-cadherin and modulates YAP localization and signaling, J. Cell Biol., 211, 1177–1192, doi: 10.1083/jcb.201501089.

14. Sluysmans, S., Vasileva, E., Spadaro, D., Shah, J., Rouaud, F., and Citi, S. (2017) The role of apical cell–cell junctions and associated cytoskeleton in mechanotransduction, Biol. Cell, 109, 139–161, doi: 10.1111/boc.201600075.

15. Prasain, N., and Stevens, T. (2009) The actin cytoskeleton in endothelial cell phenotypes, Microvasc. Res., 77, 53–63, doi: 10.1016/j.mvr.2008.09.012.

16. Zheng, W., Nurmi, H., Appak, S., Sabine, A., Bovay, E., Korhonen, E.A., Orsenigo, F., Lohela, M., D’Amico, G., Holopainen, T., Leow, C.C., Dejana, E., Petrova, T.V, Augustin, H.G., and Alitalo, K. (2014) Angiopoietin 2 regulates the transformation and integrity of lymphatic endothelial cell junctions, Genes Dev., 28, 592–603, doi: 10.1101/gad.237677.114.

17. Birdsey, G.M., Shah, A.V., Dufton, N., Reynolds, L.E., Osuna Almagro, L., Yang, Y., Aspalter, I.M., Khan, S.T., Mason, J.C., Dejana, E., Gottgens, B., Hodivala-Dilke, K., Gerhardt, H., Adams, R.H., and Randi, A.M. (2015) The endothelial transcription factor ERG promotes vascular stability and growth through Wnt/β-catenin signaling, Dev. Cell, 32, 82–96, doi: 10.1016/j.devcel.2014.11.016.

18. Trani, M., and Dejana, E. (2015) New insights in the control of vascular permeability: vascular endothelial-cadherin and other players, Curr. Opin. Hematol., 22, 267–272.

19. Ziegler, N., Awwad, K., Fisslthaler, B., Reis, M., Devraj, K., Corada, M., Minardi, S.P., Dejana, E., Plate, K.H., Fleming, I., and Liebner, S. (2016) β-Catenin is required for endothelial Cyp1b1 regulation influencing metabolic barrier function, J. Neurosci., 36, 8921–8935, doi: 10.1523/jneurosci.0148-16.2016.

20. Cerutti, C., and Ridley, A.J. (2017) Endothelial cell–cell adhesion and signaling, Exp. Cell Res., 358, 31–38, doi: 10.1016/j.yexcr.2017.06.003.

21. Dejana, E., Orsenigo, F., and Lampugnani, M.G. (2008) The role of adherens junctions and VE-cadherin in the control of vascular permeability, J. Cell Sci., 121, 2115–2122, doi: 10.1242/jcs.017897.

22. Vandekerckhove, J., and Weber, K. (1978) At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide, J. Mol. Biol., 126, 783–802, doi: 10.1016/0022-2836(78)90020-7.

23. Ampe, C., and VanTroys, M. (2017) Mammalian actins: isoform-specific functions and diseases, Handb. Exp. Pharmacol., 235, 1–37, doi: 10.1007/164_2016_43.

24. Dugina, V., Zwaenepoel, I., Gabbiani, G., Clement, S., and Chaponnier, C. (2009) Beta and gamma-cytoplasmic actins display distinct distribution and functional diversity, J. Cell Sci., 122, 2980–2988, doi: 10.1242/jcs.041970.

25. Baranwal, S., Naydenov, N.G., Harris, G., Dugina, V., Morgan, K.G., Chaponnier, C., and Ivanov, A.I. (2012) Nonredundant roles of cytoplasmic β- and γ-actin isoforms in regulation of epithelial apical junctions, Mol. Biol. Cell, 23, 3542–3553, doi: 10.1091/mbc.E12-02-0162.

26. Lechuga, S., Baranwal, S., Li, C., Naydenov, N.G., Kuemmerle, J.F., Dugina, V., Chaponnier, C., and Ivanov, A.I. (2014) Loss of γ-cytoplasmic actin triggers myofibroblast transition of human epithelial cells, Mol. Biol. Cell, 25, 3133–3146, doi: 10.1091/mbc.E14-03-0815.

27. Latham, S.L., Chaponnier, C., Dugina, V., Couraud, P.-O., Grau, G.E.R., and Combes, V. (2013) Cooperation between β- and γ-cytoplasmic actins in the mechanical regulation of endothelial microparticle formation, FASEB J., 27, 672–683, doi: 10.1096/fj.12-216531.

28. Bunnell, T.M., Burbach, B.J., Shimizu, Y., and Ervasti, J.M. (2011) β-Actin specifically controls cell growth, migration, and the G-actin pool, Mol. Biol. Cell, 22, 4047–4058, doi: 10.1091/mbc.E11-06-0582.

29. Bunnell, T.M., and Ervasti, J.M. (2010) Delayed embryonic development and impaired cell growth and survival in Actg1 null mice, Cytoskeleton, 67, 564–572, doi: 10.1002/cm.20467.

30. Shum, M.S.Y., Pasquier, E., Po’uha, S.T., O’Neill, G.M., Chaponnier, C., Gunning, P.W., and Kavallaris, M. (2011) γ-Actin regulates cell migration and modulates the ROCK signaling pathway, FASEB J., 25, 4423–4433, doi: 10.1096/fj.11-185447.

31. Dugina, V., Khromova, N., Rybko, V., Blizniukov, O., Shagieva, G., Chaponnier, C., Kopnin, B., and Kopnin, P. (2015) Tumor promotion by γ and suppression by β non-muscle actin isoforms, Oncotarget, 6, 14556–14571, doi: 10.18632/oncotarget.3989.

32. Shakhov, A.S., Verin, A.D., and Alieva, I.B. (2014) Reorganization of endothelial cells cytoskeleton during formation of functional monolayer in vitro, Cell Tissue Biol., 8, 138–151, doi: 10.1134/S1990519X14020096.

33. Shakhov, A.S., Dugina, V.B., and Alieva, I.B. (2015) Reorganization of actin and microtubule systems in human vein endothelial cells during intercellular contact formation, Cell. Tissue Biol., 9, 299–309, doi: 10.1134/S1990519X15040112.

34. Shagieva, G.S., Domnina, L.V, Chipysheva, T.A., Ermilova, V.D., Chaponnier, C., and Dugina, V.B. (2012) Actin isoforms and reorganization of adhesion junctions in epithelial-to-mesenchymal transition of cervical carcinoma cells, Biochemistry (Moscow), 77, 1266–1276, doi: 10.1134/S0006297912110053.

35. Piccin, A., Murphy, W.G., and Smith, O.P. (2007) Circulating microparticles: pathophysiology and clinical implications, Blood Rev., 21, 157–171, doi: 10.1016/j.blre.2006.09.001.

36. George, F.D. (2008) Microparticles in vascular diseases, Thromb. Res., 122, 55–59, doi: 10.1016/S0049-3848(08)70020-3.

37. Pasquier, E., Tuset, M.-P., Sinnappan, S., Carnell, M., Macmillan, A., and Kavallaris, M. (2015) γ-Actin plays a key role in endothelial cell motility and neovessel maintenance, Vasc. Cell, 7, 1–16, doi: 10.1186/s13221-014-0027-2.

38. Zhang, L.J., Tao, B.B., Wang, M.J., Jin, H.M., and Zhu, Y.C. (2012) PI3K p110a isoform-dependent Rho GTPase Rac1 activation mediates H2S-promoted endothelial cell migration via actin cytoskeleton reorganization, PLoS One, 7, doi: 10.1371/journal.pone.0044590.

39. Rodriguez, O.C., Schaefer, A.W., Mandato, C.A., Forscher, P., Bement, W.M., and Waterman-Storer, C.M. (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis, Nat. Cell Biol., 5, 599–609, doi: 10.1038/ncb0703-599.

40. Bershadsky, A.D., Ballestrem, C., Carramusa, L., Zilberman, Y., Gilquin, B., Khochbin, S., Alexandrova, A.Y., Verkhovsky, A.B., Shemesh, T., and Kozlov, M.M. (2006) Assembly and mechanosensory function of focal adhesions: experiments and models, Eur. J. Cell. Biol., 85, 165–173, doi: 10.1016/j.ejcb.2005.11.001.

41. Applewhite, D.A., Grode, K.D., Keller, D., Zadeh, A.D., Slep, K.C., and Rogers, S.L. (2010) The spectraplakin short stop is an actin – microtubule cross-linker that contributes to organization of the microtubule network, Mol. Biol. Cell, 21, 1714–1724, doi: 10.1091/mbc.e10-01-0011.

42. Preciado Lopez, M., Huber, F., Grigoriev, I., Steinmetz, M.O., Akhmanova, A., Dogterom, M., and Koenderink, G.H. (2014) In vitro reconstitution of dynamic micro-tubules interacting with actin filament networks, Methods Enzymol., 540, 301–320, doi: 10.1016/B978-0-12-397924-7.00017-0.

43. Birukova, A., Birukov, K., Smurova, K., Kaibuchi, K., Alieva, I., Garcia, J.G., and Verin, A. (2004) Novel role of microtubules in thrombin-induced endothelial barrier dysfunction, FASEB J., 18, 1879–1890, doi: 10.1096/fj.04-2328com.

44. Birukova, A.A, Smurova, K.M., Birukov, K.G., Kaibuchi, K., Garcia, J.G., and Verin, A.D. (2004) Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction, Microvasc. Res., 67, 64–77, doi: 10.1016/j.mvr.2003.09.007.

45. Smurova, K.M., Verin, A.D., and Alieva, I.B. (2011) Inhibition of RHO-kinase depends on factors that modify endothelial permeability, Cell Tissue Biol., 5, 221–227.

46. Alieva, I.B., Zemskov, E.A., Smurova, K.M., Kaverina, I.N., and Verin, A.D. (2013) The leading role of microtubules in endothelial barrier dysfunction: disassembly of peripheral microtubules leaves behind the cytoskeletal reorganization, J. Cell. Biochem., 114, 2258–2272, doi: 10.1002/jcb.24575.

47. Krendel, M., Zenke, F.T., and Bokoch, G.M. (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton, Nat. Cell Biol., 4, 294–301, doi: 10.1038/ncb773.

48. Sehrawat, S., Cullere, X., Patel, S., Italiano, J., and Mayadas, T.N. (2008) Role of Epac1, an exchange factor for Rap GTPases, in endothelial microtubule dynamics and barrier function, Mol. Biol. Cell, 19, 1261–1270, doi: 10.1091/mbc.E06.

49. Pertz, O. (2010) Spatio-temporal Rho GTPase signaling – where are we now? J. Cell Sci., 123, 1841–1850, doi: 10.1242/jcs.064345.

50. Akhshi, T.K., Wernike, D., and Piekny, A. (2014) Microtubules and actin cross-talk in cell migration and division, Cytoskeleton (Hoboken), 71, 1–23, doi: 10.1002/cm.21150.

51. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K., and Narumiya, S. (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase, Science, 285, 895–898.

52. Gorovoy, M., Niu, J., Bernard, O., Profirovic, J., Minshall, R., Neamu, R., and Voyno-Yasenetskaya, T. (2005) LIM kinase 1 coordinates microtubule stability and actin polymerization in human endothelial cells, J. Biol. Chem., 280, 26533–26542, doi: 10.1074/jbc.M502921200.

53. Смурова К.М., Бирюкова А.А, Верин А.Д., Алиева И.Б. (2008) Доз-зависимый эффект нокодазола на цитоскелет эндотелиальных клеток, Биологические мембраны, 25, 181–190.

54. Смурова К.М., Верин А.Д., Алиева И.Б. (2011) Эффект ингибирования Rho-киназы при барьерной дисфункции зависит от природы факторов, изменяющих проницаемость эндотелия, Цитология, 53, 359–366.

55. Small, J.V., and Kaverina, I. (2003) Microtubules meet substrate adhesions to arrange cell polarity, Curr. Opin. Cell Biol., 15, 40–47, doi: 10.1016/S0955-0674(02)00008-X.

56. Po’uha, S.T., and Kavallaris, M. (2015) Gamma-actin is involved in regulating centrosome function and mitotic progression in cancer cells, Cell Cycle, 14, 3908–3919, doi: 10.1080/15384101.2015.1120920.

57. Alberico, E.O., Zhu, Z.C., Wu, Y.-F.O., Gardner, M.K., Kovar, D.R., and Goodson, H.V. (2016) Interactions between the microtubule binding protein EB1 and F-actin, J. Mol. Biol., 428, 1304–1314, doi: 10.1016/j.jmb.2016.01.032.

58. Lansbergen, G., and Akhmanova, A. (2006) Microtubule plus end: a hub of cellular activities, Traffic (Copenhagen, Denmark), 7, 499–507, doi: 10.1111/j.1600-0854.2006.00400.x.

59. Akhmanova, A., and Steinmetz, M.O. (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips, Nat. Rev. Mol. Cell Biol., 9, 309–322, doi: 10.1038/nrm2369.

60. Fukata, M., Watanabe, T., Noritake, J., Nakagawa, M., Yamaga, M., Kuroda, S., Matsuura, Y., Iwamatsu, A., Perez, F., and Kaibuchi, K. (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170, Cell, 109, 873–885, doi: 10.1016/S0092-8674(02)00800-0.

61. Watanabe, T., Wang, S., Noritake, J., Sato, K, Fukata, M., Takefuji, M., Nakagawa, M., Izumi, N., Akiyama, T., and Kaibuchi, K. (2004) Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration, Dev. Cell, 7, 871–883, doi: 10.1016/j.devcel.2004.10.017.

62. Goryunov, D., and Liem, R.K.H. (2016) Microtubule-actin cross-linking factor 1: domains, interaction partners, and tissue-specific functions, Methods Enzymol., 569, 331–353, doi: 10.1016/bs.mie.2015.05.022.

63. Ning, W., Yu, Y., Xu, H., Liu, X., Wang, D., Wang, J., Wang Y., and Meng, W. (2016) The CAMSAP3-ACF7 complex couples noncentrosomal microtubules with actin filaments to coordinate their dynamics, Dev. Cell, 39, 61–74, doi: 10.1016/j.devcel.2016.09.003.

64. Dugina, V., Alieva, I., Khromova, N., Kireev, I., Gunning, P.W., and Kopnin, P. (2016) Interaction of microtubules with the actin cytoskeleton via cross-talk of EB1-containing +TIPs and γ-actin in epithelial cells, Oncotarget, 7, 72699–72715, doi: 10.18632/oncotarget.12236.

65. Henty-Ridilla, J.L., Rankova, A., Eskin, J.A., Kenny, K., and Goode, B.L. (2016) Accelerated actin filament polymerization from microtubule plus ends, Science, 352, 1004–1009, doi: 10.1126/science.aaf1709.

66. Heil, A., Nazmi, A.R, Koltzscher, M., Poeter, M., Austermann, J., Assard, N., Baudier, J., Kaibuchi, K., and Gerke, V. (2011) S100P is a novel interaction partner and regulator of IQGAP1, J. Biol. Chem., 286, 7227–7238, doi: 10.1074/jbc.M110.135095.

67. Nammalwar, R.C., Heil, A., and Gerke, V. (2015) Ezrin interacts with the scaffold protein IQGAP1 and affects its cortical localization, Biochim. Biophys. Acta, 1853, 2086–2094, doi: 10.1016/j.bbamcr.2014.12.026.

68. Lasserre, R., Charrin, S., Cuche, C., Danckaert, A., Thoulouze, M.I., de Chaumont, F., Duong, T., Perrault, N., Varin-Blank, N., Olivo-Marin, J.C., Etienne-Manneville, S., Arpin, M., Di Bartolo, V., and Alcover, A. (2010) Ezrin tunes T-cell activation by controlling and microtubule positioning at the immunological synapse, EMBO J., 29, 2301–2314, doi: 10.1038/emboj.2010.127.

69. Cook, T.A., Nagasaki, T., and Gundersen, G.G. (1998) Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lyso-phosphatidic acid, J. Cell Biol., 141, 175–185.

70. Daub, H., Gevaert, K., Vandekerckhove, J., Sobel, A., and Hall, A. (2001) Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16, J. Biol. Chem., 276, 1677–1680, doi: 10.1074/jbc.C000635200.

71. Ishizaki, T., Morishima, Y., Okamoto, M., Furuyashiki, T., Kato, T., and Narumiya, S. (2001) Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1, Nat. Cell Biol., 3, 8–14, doi: 10.1038/35050598.

72. Palazzo, A., Cook, T.A., Alberts, A.S., and Gundersen, G.G. (2001) mDia mediates Rho-regulated formation and orientation of stable microtubules, Nat. Cell Biol., 3, 723–730, doi: 10.1038/35087035.

73. Jaffe, A.B., and Hall, A. (2005) Rho GTPases: biochemistry and biology, Annu. Rev. Cell Dev. Biol., 21, 247–269, doi: 10.1146/annurev.cellbio.21.020604.150721.

74. Tian, X., Tian, Y., Moldobaeva, N., Sarich, N., and Birukova, A.A. (2014) Microtubule dynamics control HGF-induced lung endothelial barrier enhancement, PLoS One, 9, e105912, doi: 10.1371/journal.pone.0105912.

75. Tian, X., Tian, Y., Gawlak, G., Meng, F., Kawasaki, Y., Akiyama, T., and Birukova, A.A. (2015) Asef controls vascular endothelial permeability and barrier recovery in the lung, Mol. Biol. Cell, 26, 636–650, doi: 10.1091/mbc.E14-02-0725.

76. Tian, Y., Tian, X., Gawlak, G., O’Donnell, J.J., Sacks, D.B., and Birukova, A.A. (2014) IQGAP1 regulates endothelial barrier function via EB1-cortactin cross talk, Mol. Cell. Biol., 34, 3546–3558, doi: 10.1128/MCB.00248-14.

77. Tian, Y., Gawlak, G., Shah, A.S., Higginbotham, K., Tian, X., Kawasaki, Y., Akiyama, T., Sacks, D.B., and Birukova, A.A. (2015) Hepatocyte growth factor-induced Asef-IQGAP1 complex controls cytoskeletal remodeling and endothelial barrier, J. Biol. Chem., 290, 4097–4109, doi: 10.1074/jbc.M114.620377.

78. Villalonga, P., and Ridley, A.J. (2006) Rho GTPases and cell cycle control, Growth Factors, 24, 159–164, doi: 10.1080/08977190600560651.

79. Смурова К.М., Бирюкова А.А, Верин А.Д., Алиева И.Б. (2008) Система микротрубочек при барьерной дисфункции эндотелия: деполимеризация на краю клетки и реорганизация во внутренней цитоплазме, Цитология, 50, 49–55.

80. Pronk, M.C.A., van Bezu, J.S.M., van Nieuw Amerongen, G.P., van Hinsbergh, V.W.M., and Hordijk, P.L. (2017) RhoA, RhoB and RhoC differentially regulate endothelial barrier function, Small GTPases, 1–19, doi: 10.1080/21541248.2017.1339767.

81. Bruneel, A., Labas, V., Mailloux, A., Sharma, S., Vinh, J., Vaubourdolle, M., and Baudin, B. (2003) Proteomic study of human umbilical vein endothelial cells in culture, Proteomics, 3, 714–723, doi: 10.1002/pmic.200300409.

82. Liu, T., Guevara, O.E., Warburton, R.R., Hill, N.S., Gaestel, M., and Kayyali, U.S. (2010) Regulation of vimentin intermediate filaments in endothelial cells by hypoxia, Am. J. Physiol. Cell Physiol., 299, 363–373, doi: 10.1152/ajpcell.00057.2010.

83. Mokry, J., Cizkova, D., Filip, S., Ehrmann, J., Osterreicher, J., Kolar, Z., and English, D. (2004) Nestin expression by newly formed human blood vessels, Stem Cells Dev., 13, 658–664, doi: 10.1089/scd.2004.13.658.

84. Mokry, J., Ehrmann, J., Karbanova, J., Cizkova, D., Soukup, T., Suchanek, J., Filip, S., and Kolar, Z. (2008) Expression of intermediate filament nestin in blood vessels of neural and non-neural tissues, Acta Medica (Hradec Kralove), 51, 173–179.

85. Cizkova, D., Soukup, T., and Mokry, J. (2009) Nestin expression reflects formation, revascularization and reinnervation of new myofibers in regenerating rat hind limb skeletal muscles, Cells Tissues Organs, 189, 338–347, doi: 10.1159/000142161.

86. Rusu, M.C., Jianu, A.M., Pop, F., Hostiuc, S., Leonardi, R., and Curca, G.C. (2012) Immunolocalization of 200 kDa neurofilaments in human cardiac endothelial cells, Acta Histochem., 114, 842–845, doi: 10.1016/j.acthis.2012.03.001.

87. Schnittler, H.J., Schmandra, T., and Drenckhahn, D. (1998) Correlation of endothelial vimentin content with hemodynamic parameters, Histochem. Cell Biol., 110, 161–167, doi: 10.1007/s004180050277.

88. Cary, R.B., Klymkowsky, M.W., Evans, R.M., Domingo, A., Dent, J.A., and Backhus, L.E. (1994) Vimentin’s tail interacts with actin-containing structures in vivo, J. Cell Sci., 107, 1609–1622.

89. Esue, O., Carson, A.A., Tseng, Y., and Wirtz, D. (2006) A direct interaction between actin and vimentin filaments mediated by the tail domain of vimentin, J. Biol. Chem., 281, 30393–30399, doi: 10.1074/jbc.M605452200.

90. Robert, A., Herrmann, H., Davidson, M.W., and Gelfand, V.I. (2014) Microtubule-dependent transport of vimentin filament precursors is regulated by actin and by the concerted action of Rho- and p21-activated kinases, FASEB J., 28, 2879–2890, doi: 10.1096/fj.14-250019.

91. Jiu, Y., Peranen, J., Schaible, N., Cheng, F., Eriksson, J.E., Krishnan, R., and Lappalainen, P. (2017) Vimentin intermediate filaments control actin stress fiber assembly through GEF-H1 and RhoA, J. Cell Sci., 130, 892–902, doi: 10.1242/jcs.196881.

92. Ren, Y., Li, R., Zheng, Y., and Busch, H. (1998) Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases, J. Biol. Chem., 273, 34954–34960, doi: 10.1074/jbc.273.52.34954.

93. Sandi, M.-J., Marshall, C.B., Balan, M., Coyaud, E., Zhou, M., Monson, D.M., Ishiyama, N., Chandrakumar, A.A., La Rose, J., Couzens, A.L., Gingras, A.C., Raught, B., Xu, W., Ikura, M., Morrison, D.K., and Rottapel, R. (2017) MARK3-mediated phosphorylation of ARHGEF2 couples microtubules to the actin cytoskeleton to establish cell polarity, Sci. Sign., 10, 3286, doi: 10.1126/scisignal.aan3286.

94. Costigliola, N., Ding, L., Burckhardt, C.J., Han, S.J., Gutierrez, E., and Mota, A. (2017) Vimentin fibers orient traction stress, Proc. Natl. Acad. Sci. USA, 114, 5195–5200, doi: 10.1073/pnas.1614610114.

95. Gan, Z., Ding, L., Burckhardt, C.J., Lowery, J., Zaritsky, A., Sitterley, K., Mota, A., Costigliola, N., Starker, C.G., Voytas, D.F., Tytell, J., Goldman, R.D., and Danuser, G. (2016) Vimentin intermediate filaments template microtubule networks to enhance persistence in cell polarity and directed migration, Cell Systems, 3, 252–263, doi: 10.1016/j.cels.2016.08.007.

96. Castanon, M.J., Walko, G., Winter, L., and Wiche, G. (2013) Plectin-intermediate filament partnership in skin, skeletal muscle, and peripheral nerve, Histochem. Cell Biol., 140, 33–53, doi: 10.1007/s00418-013-1102-0.

97. Jiu, Y., Lehtimaki, J., Tojkander, S., Cheng, F., Jaalinoja, H., Liu, X., Varjosalo, M., Eriksson, J.E., and Lappalainen, P. (2015) Bidirectional interplay between vimentin intermediate filaments and contractile actin stress fibers, Cell Rep., 11, 1511–1518, doi: 10.1016/j.celrep.2015.05.008.

98. Zielinski, A., Linnartz, C., Pleschka, C., Dreissen, G., Springer, R., Merkel, R., and Hoffmann, B. (2018) Reorientation dynamics and structural interdependencies of actin, microtubules and intermediate filaments upon cyclic stretch application, Cytoskeleton, 75, 385–394, doi: 10.1002/cm.21470.

99. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton, Annu. Rev. Cell Biol., 4, 487–525, doi: 10.1146/annurev.cb.04.110188.002415.

100. Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K.M. (2001) Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk, Nat. Rev. Mol. Cell Biol., 2, 793–805, doi: 10.1038/35099066.

101. Mehta, D., and Malik, A.B. (2006) Signaling mechanisms regulating endothelial permeability, Physiol. Rev., 86, 279–367, doi: 10.1152/physrev.00012.2005.

102. Cerutti, C., and Ridley, A.J. (2017) Endothelial cell-cell adhesion and signaling, Exper. Cell Res., 358, 31–38, doi: 10.1016/j.yexcr.2017.06.003.

103. Van Buul, J.D., and Timmerman, I. (2016) Small Rho GTPase-mediated actin dynamics at endothelial adherens junctions, Small GTPases, 7, 21–31, doi: 10.1080/21541248.2015.1131802.

104. Timmerman, I., Heemskerk, N., Kroon, J., Schaefer, A., van Rijssel, J., Hoogenboezem, M., van Unen, J., Goedhart, J., Gadella, T.W. Jr, Yin, T., Wu, Y., Huveneers, S., and van Buul, J.D. (2015) A local VE-cadherin and Trio-based signaling complex stabilizes endothelial junctions through Rac1, J. Cell Sci., 128, 3041–3054, doi: 10.1242/jcs.168674.

105. Hoelzle, M.K., and Svitkina, T. (2012) The cytoskeletal mechanisms of cell–cell junction formation in endothelial cells, Mol. Biol. Cell, 23, 310–323, doi: 10.1091/mbc.E11-08-0719.

106. Paatero, I., Sauteur, L., Lee, Mi., Lagendijk, A.K., Heutschi, D., Wiesner, C., Guzman, C., Bieli, D., Hogan, B.M., Affolter, M., and Belting, H.-G. (2018) Junction-based lamellipodia drive endothelial cell rearrangements in vivo via a VE-cadherin-F-actin based oscillatory cell-cell interaction, Nat. Commun., 9, 3545, doi: 10.1038/s41467-018-05851-9.