A novel role for RhoA GTPase in the regulation of airway smooth muscle contraction

Canadian Journal of Physiology and Pharmacology

Volumn 93, Issue 2, 2014, Pages 129-136

  Zhang, Wenwu ^a   Huang, Youliang ^a   Wu, Yidi ^a   Gunst, Susan J ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin polymerization; Adhesion junction; Cdc42; Myosin light chain phosphorylation; Paxillin; Vinculin

Indexed keywords

FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR KINASE INTERACTING TARGET; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; P21 ACTIVATED KINASE; P21 ACTIVATED KINASE INTERACTING EXCHANGE FACTOR COMPLEX; PAXILLIN; PROTEIN; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VINCULIN; ACTIN; GUANOSINE TRIPHOSPHATASE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME INACTIVATION; LUNG; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; HUMAN; METABOLISM; MUSCLE CONTRACTION; SMOOTH MUSCLE;

ACTINS; GTP PHOSPHOHYDROLASES; HUMANS; LUNG; MUSCLE CONTRACTION; MUSCLE, SMOOTH; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84922159978     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/cjpp-2014-0388     Document Type: Article

References (49)

1. An, S.S., Laudadio, R.E., Lai, J., Rogers, R.A., and Fredberg, J.J. 2002. Stiffness changes in cultured airway smooth muscle cells. Am. J. Physiol. Cell Physiol. 283(3): C792-C801. doi:10.1152/ajpcell.00425.2001. PMID:12176736.
2. Bellis, S.L., Miller, J.T., and Turner, C.E. 1995. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270(29): 17437-17441. doi:10.1074/jbc.270.29.17437. PMID:7615549.
3. Burridge, K., and Wennerberg, K. 2004. Rho and Rac take center stage. Cell, 116(2): 167-179. doi:10.1016/S0092-8674(04)00003-0. PMID:14744429.
4. Carlier, M.F., Ducruix, A., and Pantaloni, D. 1999. Signalling to actin: the Cdc42- N-WASP-Arp2/3 connection. Chem. Biol. 6(9): R235-R240. doi:10.1016/S1074- 5521(99)80107-0. PMID:10467124.
5. Chrzanowska-Wodnicka, M., and Burridge, K. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133(6): 1403-1415. doi:10.1083/jcb.133.6.1403. PMID:8682874.
6. Dowell, M.L., Lakser, O.J., Gerthoffer, W.T., Fredberg, J.J., Stelmack, G.L., Halayko, A.J., et al. 2005. Latrunculin B increases force fluctuation-induced relengthening of ACh-contracted, isotonically shortened canine tracheal smooth muscle. J. Appl. Physiol. 98(2): 489-497. doi:10.1152/japplphysiol.01378. 2003. PMID:15465883.
7. Gunst, S.J., and Zhang, W. 2008. Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am. J. Physiol. Cell Physiol. 295(3): C576-C587. doi:10.1152/ajpcell.00253.2008. PMID:18596210.
8. Gunst, S.J., Tang, D.D., and Opazo, S.A. 2003. Cytoskeletal remodeling of the airway smooth muscle cell: a mechanism for adaptation to mechanical forces in the lung. Respir. Physiol. Neurobiol. 137(2-3): 151-168. doi:10.1016/S1569- 9048(03)00144-7. PMID:14516723.
9. Halayko, A.J., and Stelmack, G.L. 2005. The association of caveolae, actin, and the dystrophin-glycoprotein complex: a role in smooth muscle phenotype and function? Can. J. Physiol. Pharmacol. 83(10): 877-891. doi:10.1139/y05-107. PMID:16333360.
10. Herrera, A.M., Martinez, E.C., and Seow, C.Y. 2004. Electron microscopic study of actin polymerization in airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 286(6): L1161-L1168. doi:10.1152/ajplung.00298.2003. PMID:14751850.
11. Higgs, H.N., and Pollard, T.D. 2000. Activation by Cdc42 and PIP(2) of Wiskott- Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J. Cell Biol. 150(6): 1311-1320. doi:10.1083/jcb.150.6.1311. PMID: 10995437.
12. Higgs, H.N., and Pollard, T.D. 2001. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70: 649-676. doi:10.1146/annurev.biochem.70.1.649. PMID: 11395419.
13. Hirshman, C.A., and Emala, C.W. 1999. Actin reorganization in airway smooth muscle cells involves Gq and Gi-2 activation of Rho. Am. J. Physiol. 277(3): L653-L661. PMID:10484474.
14. Huang, Y., Zhang, W., and Gunst, S.J. 2011. Activation of vinculin induced by cholinergic stimulation regulates contraction of tracheal smooth muscle tissue. J. Biol. Chem. 286(5): 3630-3644. doi:10.1074/jbc.M110.139923. PMID: 21071443.
15. Huang, Y., Day, R.N., and Gunst, S.J. 2014. Vinculin phosphorylation at Tyr1065 regulates vinculin conformation and tension development in airway smooth muscle tissues. J. Biol. Chem. 289(6): 3677-3688. doi:10.1074/jbc.M113.508077. PMID:24338477.
16. Iizuka, K., Yoshii, A., Samizo, K., Tsukagoshi, H., Ishizuka, T., Dobashi, K., et al. 1999. A major role for the rho-associated coiled coil forming protein kinase in G-protein-mediated Ca2+ sensitization through inhibition of myosin phosphatase in rabbit trachea. Br. J. Pharmacol. 128(4): 925-933. doi:10.1038/sj.bjp. 0702864. PMID:10556927.
17. Ito, M., Nakano, T., Erdodi, F., and Hartshorne, D.J. 2004. Myosin phosphatase: structure, regulation and function. Mol. Cell. Biochem. 259(1-2): 197-209. doi:10.1023/B:MCBI.0000021373.14288.00. PMID:15124925.
18. Lesh, R.E., Emala, C.W., Lee, H.T., Zhu, D., Panettieri, R.A., and Hirshman, C.A. 2001. Inhibition of geranylgeranylation blocks agonist-induced actin reorganization in human airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol 281(4): L824-L831. PMID:11557586.
19. Li, R., Debreceni, B., Jia, B., Gao, Y., Tigyi, G., and Zheng, Y. 1999. Localization of the PAK1-, WASP-, and IQGAP1-specifying regions of Cdc42. J. Biol. Chem. 274(42): 29648-29654. doi:10.1074/jbc.274.42.29648. PMID:10514434.
20. Lynch,E.A., Stall, J., Schmidt, G., Chavrier, P., and Souza-Schorey, C. 2006. Proteasome-mediated degradation of Rac1-GTP during epithelial cell scattering. Mol. Biol. Cell,17(5): 2236-2242. doi:10.1091/mbc.E05-08-0779. PMID:16481404.
21. Mehta, D., and Gunst, S.J. 1999. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J. Physiol. 519(3): 829-840. doi:10.1111/j.1469-7793.1999.0829n.x. PMID:10457094.
22. Mullins, R.D. 2000. How WASP-family proteins and the Arp2/3 complex convert intracellular signals into cytoskeletal structures. Curr. Opin. Cell Biol. 12(1): 91-96. doi:10.1016/S0955-0674(99)00061-7. PMID:10679362.
23. Opazo Saez, A., Zhang, W., Wu, Y., Turner, C.E., Tang, D.D., and Gunst, S.J. 2004. Tension development during contractile stimulation of smooth muscle requires recruitment of paxillin and vinculin to the membrane. Am. J. Physiol. Cell Physiol. 286(2): C433-C447. doi:10.1152/ajpcell.00030.2003. PMID:14576084.
24. Pasapera, A.M., Schneider, I.C., Rericha, E., Schlaepfer, D.D., and Waterman, C.M. 2010. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188(6): 877-890. doi:10.1083/jcb.200906012. PMID:20308429.
25. Petit,V., Boyer, B., Lentz, D., Turner, C.E., Thiery, J.P., and Valles, A.M. 2000. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT- II cells. J. Cell Biol. 148(5): 957-970. doi:10.1083/jcb.148.5.957. PMID:10704446.
26. Puetz, S., Lubomirov, L.T., and Pfitzer, G. 2009. Regulation of smooth muscle contraction by small GTPases. Physiology (Bethesda), 24: 342-356. doi:10.1152/ physiol.00023.2009. PMID:19996365.
27. Rohatgi,R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T., et al. 1999. The interaction between N-WASP and the Arp2/3 complex links Cdc42- dependent signals to actin assembly. Cell,97(2): 221-231. doi:10.1016/S0092- 8674(00)80732-1. PMID:10219243.
28. Rohatgi, R., Ho, H.Y., and Kirschner, M.W. 2000. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150(6): 1299-1310. doi:10.1083/jcb.150.6.1299. PMID:10995436.
29. Rosenberger, G., Jantke, I., Gal, A., and Kutsche, K. 2003. Interaction of alphaPIX (ARHGEF6) with beta-parvin (PARVB) suggests an involvement of alphaPIX in integrin-mediated signaling. Hum. Mol. Genet. 12(2): 155-167. doi:10.1093/ hmg/ddg019. PMID:12499396.
30. Schaller, M.D., and Parsons, J.T. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15(5): 2635-2645. PMID:7537852.
31. Sinha, S., and Yang, W. 2008. Cellular signaling for activation of Rho GTPase Cdc42. Cell. Signal. 20(11): 1927-1934. doi:10.1016/j.cellsig.2008.05.002. PMID: 18558478.
32. Somlyo, A.P., and Somlyo, A.V. 2003. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83(4): 1325-1358. doi:10.1152/physrev.00023.2003. PMID: 14506307.
33. Suzuki, T., Mimuro, H., Miki, H., Takenawa, T., Sasaki, T., Nakanishi, H., et al. 2000. Rho family GTPase Cdc42 is essential for the actin-based motility of Shigella in mammalian cells. J. Exp. Med. 191(11): 1905-1920. doi:10.1084/jem. 191.11.1905. PMID:10839806.
34. Tang, D.D., and Gunst, S.J. 2001. Depletion of focal adhesion kinase by antisense depresses contractile activation of smooth muscle. Am. J. Physiol. Cell Physiol. 280(4): C874-C883. PMID:11245605.
35. Tang, D.D., and Gunst, S.J. 2004. The small GTPase Cdc42 regulates actin polymerization and tension development during contractile stimulation of smooth muscle. J. Biol. Chem. 279(50): 51722-51728. doi:10.1074/jbc.M408351200. PMID:15456777.
36. Tang, D.D., Turner, C.E., and Gunst, S.J. 2003. Expression of non-phosphorylatable paxillin mutants in canine tracheal smooth muscle inhibits tension development. J. Physiol. 553(1): 21-35. doi:10.1113/jphysiol.2003. 045047. PMID:12949231.
37. Tang, D.D., Zhang, W., and Gunst, S.J. 2005. The adapter protein CrkII regulates neuronal Wiskott-Aldrich syndrome protein, actin polymerization, and tension development during contractile stimulation of smooth muscle. J. Biol. Chem. 280(24): 23380-23389. doi:10.1074/jbc.M413390200. PMID:15834156.
38. Togashi, H., Emala, C.W., Hall, I.P., and Hirshman, C.A. 1998. Carbachol-induced actin reorganization involves Gi activation of Rho in human airway smooth muscle cells. Am. J. Physiol. 274(5): L803-L809. PMID:9612296.
39. Vicente-Manzanares, M., Ma, X., Adelstein, R.S., and Horwitz, A.R. 2009. Nonmuscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10(11): 778-790. doi:10.1038/nrm2786. PMID:19851336.
40. Walsh, M.P., and Cole, W.C. 2013. The role of actin filament dynamics in the myogenic response of cerebral resistance arteries. J. Cereb. Blood Flow Metab. 33(1): 1-12. doi:10.1038/jcbfm.2012.144. PMID:23072746.
41. Wang, Z., Pavalko, F.M., and Gunst, S.J. 1996. Tyrosine phosphorylation of the dense plaque protein paxillin is regulated during smooth muscle contraction. Am. J. Physiol. 271(5): C1594-C1602. PMID:8944643.
42. Yamin, R., and Morgan, K.G. 2012. Deciphering actin cytoskeletal function in the contractile vascular smooth muscle cell. J. Physiol. 590(17): 4145-4154. doi: 10.1113/jphysiol.2012.232306. PMID:22687615.
43. Zhang, W.W., and Gunst, S.J. 2006. Dynamic association between alpha-actinin and beta-integrin regulates contraction of canine tracheal smooth muscle. J. Physiol. (Lond.), 572(3): 659-676. doi:10.1113/jphysiol.2006.106518. PMID: 16513669.
44. Zhang,W., and Gunst, S.J. 2008a. Interactions of airway smooth muscle cells with their tissue matrix: implications for contraction. Proc. Am. Thorac. Soc. 5(1): 32-39. doi:10.1513/pats.200704-048VS. PMID:18094082.
45. Zhang,W. and Gunst, S.J. 2008b. Dynamics of cytoskeletal and contractile protein organization: an emerging paradigm for airway smooth muscle contraction. In Airway smooth muscle biology and pharmacology. Edited by K.F. Chung. Wiley Press.
46. Zhang, W., Wu, Y., Du, L., Tang, D.D., and Gunst, S.J. 2005. Activation of the Arp2/3 complex by N-WASp is required for actin polymerization and contraction in smooth muscle. Am. J. Physiol. Cell Physiol. 288(5): C1145-C1160. doi:10.1152/ajpcell.00387.2004. PMID:15625304.
47. Zhang, W., Wu, Y., Wu, C., and Gunst, S.J. 2007. Integrin-linked kinase (ILK) regulates N-WASp-mediated actin polymerization and tension development in tracheal smooth muscle. J. Biol. Chem. 282(47): 34568-34580. doi:10.1074/ jbc.M704966200. PMID:17897939.
48. Zhang, W., Du, L., and Gunst, S.J. 2010. The effects of the small GTPase RhoA on the muscarinic contraction of airway smooth muscle result from its role in regulating actin polymerization. Am. J. Physiol. Cell Physiol. 299(2): C298- C306. doi:10.1152/ajpcell.00118.2010. PMID:20445174.
49. Zhang, W., Huang, Y., and Gunst, S.J. 2012. The small GTPase RhoA regulates the contraction of smooth muscle tissues by catalyzing the assembly of cytoskeletal signaling complexes at membrane adhesion sites. J. Biol. Chem. 287(41): 33996-34008. doi:10.1074/jbc.M112.369603. PMID:22893699.