Novel role of stathmin in microtubule-dependent control of endothelial permeability

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3862-3874

  Tian, Xinyong ^a   Tian, Yufeng ^a   Sarich, Nicolene ^a   Wu, Tinghuai ^a   Birukova, Anna A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Cytoskeleton; Dynamics; GEF H1; Lung; Rho GTPase

Indexed keywords

F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO KINASE; SMALL INTERFERING RNA; STATHMIN; THROMBIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; BLOOD VESSEL PERMEABILITY; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DEPHOSPHORYLATION; DOWN REGULATION; ENDOTHELIUM CELL; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO CULTURE; IN VIVO STUDY; LUNG ALVEOLUS CELL; LUNG INJURY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE PERMEABILITY; ENDOTHELIUM; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; LUNG; MALE; MICE; MICE, INBRED C57BL; MICROTUBULES; PHOSPHORYLATION; RESPIRATION, ARTIFICIAL; RNA, SMALL INTERFERING; STATHMIN; THROMBIN;

EID: 84865744109     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-207746     Document Type: Article

References (35)

1. Dudek, S. M., and Garcia, J. G. (2001) Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91, 1487-1500
2. Mehta, D., and Malik, A. B. (2006) Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86, 279-367
3. Waterman-Storer, C. M., and Salmon, E. (1999) Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr. Opin. Cell Biol. 11, 61-67
4. Gundersen, G. G., and Cook, T. A. (1999) Microtubules and signal transduction. Curr. Opin. Cell Biol. 11, 81-94
5. Birukova, A. A., Birukov, K. G., Smurova, K., Adyshev, D. M., Kaibuchi, K., Alieva, I., Garcia, J. G., and Verin, A. D. (2004) Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB J. 18, 1879-1890
6. Petrache, I., Birukova, A., Ramirez, S. I., Garcia, J. G., and Verin, A. D. (2003) The role of the microtubules in tumor necrosis factor-alpha-induced endothelial cell permeability. Am. J. Respir. Cell Mol. Biol. 28, 574-581
7. Birukova, A. A., Birukov, K. G., Adyshev, D., Usatyuk, P., Natarajan, V., Garcia, J. G., and Verin, A. D. (2005) Involvement of microtubules and Rho pathway in TGF-beta1-induced lung vascular barrier dysfunction. J. Cell. Physiol. 204, 934-947
8. 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
9. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249
10. Birukova, A. A., Adyshev, D., Gorshkov, B., Bokoch, G. M., Birukov, K. G., and Verin, A. A. (2006) GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am. J. Physiol. Lung. Cell. Mol. Physiol. 290, L540-L548
11. Chang, Y. C., Nalbant, P., Birkenfeld, J., Chang, Z. F., and Bokoch, G. M. (2008) GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol. Biol. Cell 19, 2147-2153
12. Kakiashvili, E., Speight, P., Waheed, F., Seth, R., Lodyga, M., Tanimura, S., Kohno, M., Rotstein, O. D., Kapus, A., and Szaszi, K. (2009) GEF-H1 mediates tumor necrosis factor-alpha-induced Rho activation and myosin phosphorylation: role in the regulation of tubular paracellular permeability. J. Biol. Chem. 284, 11454-11466
13. Manna, T., Thrower, D. A., Honnappa, S., Steinmetz, M. O., and Wilson, L. (2009) Regulation of microtubule dynamic instability in vitro by differentially phosphorylated stathmin. J. Biol. Chem. 284, 15640-15649
14. Birukova, A. A., Fu, P., Xing, J., Yakubov, B., Cokic, I., and Birukov, K. G. (2010) Mechanotransduction by GEF-H1 as a novel mechanism of ventilator-induced vascular endothelial permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L837-L848
15. Birukova, A. A., Xing, J., Fu, P., Yakubov, B., Dubrovskyi, O., Fortune, J. A., Klibanov, A. M., and Birukov, K. G. (2010) Atrial natriuretic peptide attenuates LPS-induced lung vascular leak: role of PAK1. Am. J. Physiol. Lung Cell. Mol. Physiol. 299, L652-L663
16. Singleton, P. A., Chatchavalvanich, S., Fu, P., Xing, J., Birukova, A. A., Fortune, J. A., Klibanov, A. M., Garcia, J. G., and Birukov, K. G. (2009) Akt-mediated transactivation of the S1P1 receptor in caveolin-enriched microdomains regulates endothelial barrier enhancement by oxidized phospholipids. Circ. Res. 104, 978-986
17. Thomas, M., Ge, Q., Lu, J. J., Chen, J., and Klibanov, A. M. (2005) Cross-linked small polyethylenimines: while still non-toxic, deliver DNA efficiently to mammalian cells in vitro and in vivo. Pharm. Res. 22, 373-380
18. Thomas, M., Lu, J. J., Ge, Q., Zhang, C., Chen, J., and Klibanov, A. M. (2005) Full deacylation of polyethylenimine dramatically boosts its gene delivery efficiency and specificity to mouse lung. Proc. Natl. Acad. Sci. U. S. A. 102, 5679-5684
19. Xing, J., and Birukova, A. A. (2010) ANP attenuates inflammatory signaling and Rho pathway of lung endothelial permeability induced by LPS and TNFalpha. Microvasc. Res. 79, 26-62
20. 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
21. Essler, M., Amano, M., Kruse, H. J., Kaibuchi, K., Weber, P. C., and Aepfelbacher, M. (1998) Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J. Biol. Chem. 273, 21867-21874
22. Amano, M., Kaneko, T., Maeda, A., Nakayama, M., Ito, M., Yamauchi, T., Goto, H., Fukata, Y., Oshiro, N., Shinohara, A., Iwamatsu, A., and Kaibuchi, K. (2003) Identification of Tau and MAP2 as novel substrates of Rho-kinase and myosin phosphatase. J. Neurochem. 87, 780-790
23. Komarova, Y., De Groot, C. O., Grigoriev, I., Gouveia, S. M., Munteanu, E. L., Schober, J. M., Honnappa, S., Buey, R. M., Hoogenraad, C. C., Dogterom, M., Borisy, G. G., Steinmetz, M. O., and Akhmanova, A. (2009) Mammalian end binding proteins control persistent microtubule growth. J. Cell Biol. 184, 691-706
24. Birukova, A. A., Burdette, D., Moldobaeva, N., Xing, J., Fu, P., and Birukov, K. G. (2010) Rac GTPase is a hub for protein kinase A and Epac signaling in endothelial barrier protection by cAMP. Microvasc. Res. 79, 128-138
25. Birukova, A. A., Fu, P., Xing, J., Cokic, I., and Birukov, K. G. (2010) Lung endothelial barrier protection by iloprost in the 2-hit models of ventilator-induced lung injury (VILI) involves inhibition of Rho signaling. Transl. Res. 155, 44-54
26. Gradin, H. M., Larsson, N., Marklund, U., and Gullberg, M. (1998) Regulation of microtubule dynamics by extracellular signals: cAMP-dependent protein kinase switches off the activity of oncoprotein 18 in intact cells. J. Cell Biol. 140, 131-141
27. Baldassarre, G., Belletti, B., Nicoloso, M. S., Schiappacassi, M., Vecchione, A., Spessotto, P., Morrione, A., Canzonieri, V., and Colombatti, A. (2005) p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7, 51-63
28. Giampietro, C., Luzzati, F., Gambarotta, G., Giacobini, P., Boda, E., Fasolo, A., and Perroteau, I. (2005) Stathmin expression modulates migratory properties of GN-11 neurons in vitro. Endocrinology 146, 1825-1834
29. Jin, K., Mao, X. O., Cottrell, B., Schilling, B., Xie, L., Row, R. H., Sun, Y., Peel, A., Childs, J., Gendeh, G., Gibson, B. W., and Greenberg, D. A. (2004) Proteomic and immunochemical characterization of a role for stathmin in adult neurogenesis. FASEB J. 18, 287-299
30. 2+/calmodulin-dependent phosphatase 2B in thrombin-induced endothelial cell contractile responses. Am. J. Physiol. Lung Cell. Mol. Physiol.275, L788-L799
31. Curmi, P. A., Maucuer, A., Asselin, S., Lecourtois, M., Chaffotte, A., Schmitter, J. M., and Sobel, A. (1994) Molecular characterization of human stathmin expressed in Escherichia coli: site-directed mutagenesis of two phosphorylatable serines (Ser-25 and Ser-63). Biochem. J. 300, 331-338
32. Chen, P. W., Lin, S. J., Tsai, S. C., Lin, J. H., Chen, M. R., Wang, J. T., Lee, C. P., and Tsai, C. H. (2010) Regulation of microtubule dynamics through phosphorylation on stathmin by Epstein-Barr virus kinase BGLF4. J. Biol. Chem. 285, 10053-10063
33. Wittmann, T., Bokoch, G. M., and Waterman-Storer, C. M. (2004) Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J. Biol. Chem. 279, 6196-6203
34. Mei, F. C., Qiao, J., Tsygankova, O. M., Meinkoth, J. L., Quilliam, L. A., and Cheng, X. (2002) Differential signaling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation. J. Biol. Chem. 277, 11497-11504
35. Birukova, A. A., Zagranichnaya, T., Alekseeva, E., Fu, P., Chen, W., Jacobson, J. R., and Birukov, K. G. (2007) Prostaglandins PGE2 and PGI2 promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp. Cell Res. 313, 2504-2520