Am J Physiol Cell Physiol 291(3): C483-C489

Role of vimentin in smooth muscle force development

Center for Cardiovascular Sciences, Albany Medical College, 47 New Scotland Avenue, MC-8, Albany, NY 12208

Correspondence: Dale D. Tang, Center for Cardiovascular Sciences, Albany Medical College, 47 New Scotland Avenue, MC-8, Albany, NY 12208, Tel: (518)-262-6416; Fax: (518)-262-8101, E-mail: ude.cma.liam@dgnat

Abstract

Vimentin intermediate filaments undergo spatial reorganization in cultured smooth muscle cells in response to contractile activation; however, the role of vimentin in physiologic properties of smooth muscle has not been well elucidated. In this report, tracheal smooth muscle strips were loaded with antisense oligonucleotides against vimentin, and these muscle strips were then cultured for 2 days to allow for protein degradation. The treatment with vimentin antisense but not sense oligonucleotides suppressed vimentin protein expression; neither antisense nor sense oligonucleotides affected protein levels of desmin and actin. Force development in response to stimulation with acetylcholine (ACh) or KCl depolarization was lower in vimentin-deficient tissues than in muscle tissues treated with sense oligonucleotides or in muscle strips not treated with oligonucleotides. Passive tension was also depressed in vimentin-depleted muscle tissues. Vimentin downregulation did not attenuate increases in myosin light chain phosphorylation in response to contractile stimulation or basal myosin light chain phosphorylation. In smooth muscle strips that had been treated with vimentin sense or without oligonucleotides, the desmosomal protein plakoglobin was primarily localized in cell periphery. The membrane-associated localization of plakoglobin was reduced in vimentin-depleted muscle tissues. These studies suggest that vimentin filaments play an important role in mediating active force development and passive tension, which is not regulated by myosin light chain phosphorylation. Vimentin downregulation impairs the structural organization of desmosomes, which may be associated with the decrease in force development.

Keywords: Intermediate filaments, cytoskeleton, contraction, smooth muscle, vimentin, desmin

Abstract

References

1. Ashton FT, Somlyo AV, Somlyo APThe contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy. J Mol Biol. 1975;98:17–29.[PubMed][Google Scholar]
2. Barany M, Barron JT, Gu L, Barany KExchange of the actin-bound nucleotide in intact arterial smooth muscle. J Biol Chem. 2001;276:48398–48403.[PubMed][Google Scholar]
3. Bornslaeger EA, Godsel LM, Corcoran CM, Park JK, Hatzfeld M, Kowalczyk AP, Green KJPlakophilin 1 interferes with plakoglobin binding to desmoplakin, yet together with plakoglobin promotes clustering of desmosomal plaque complexes at cell-cell borders. J Cell Sci. 2001;114:727–738.[PubMed][Google Scholar]
4. Chan W, Kozma R, Yasui Y, Inagaki M, Leung T, Manser E, Lim LVimentin intermediate filament reorganization by Cdc42: involvement of PAK and p70 S6 kinase. Eur J Cell Biol. 2002;81:692–701.[PubMed][Google Scholar]
5. Chang L, Goldman RDIntermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol. 2004;5:601–613.[PubMed][Google Scholar]
6. Chidgey MDesmosomes and disease: an update. Histol Histopathol. 2002;17:1179–1192.[PubMed][Google Scholar]
7. Correia I, Chu D, Chou YH, Goldman RD, Matsudaira P. Integrating the actin and vimentin cytoskeletons. adhesion-dependent formation of fimbrin-vimentin complexes in macrophages. J Cell Biol. 1999;146:831–842.
8. Garrod DR, Merritt AJ, Nie ZDesmosomal adhesion: structural basis, molecular mechanism and regulation. Mol Membr Biol. 2002;19:81–94.[PubMed][Google Scholar]
9. Gerthoffer WT, Gunst SJInvited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol. 2001;91:963–972.[PubMed][Google Scholar]
10. Green KJ, Geiger B, Jones JC, Talian JC, Goldman RDThe relationship between intermediate filaments and microfilaments before and during the formation of desmosomes and adherens-type junctions in mouse epidermal keratinocytes. J Cell Biol. 1987;104:1389–1402.[Google Scholar]
11. Green KJ, Goldman RDEvidence for an interaction between the cell surface and intermediate filaments in cultured fibroblasts. Cell Motil Cytoskeleton. 1986;6:389–405.[PubMed][Google Scholar]
12. Halayko AJ, Salari H, MA X, Stephens NLMarkers of airway smooth muscle cell phenotype. Am J Physiol. 1996;270:L1040–51.[PubMed][Google Scholar]
13. Herrmann H, Aebi UIntermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol. 2000;12:79–90.[PubMed][Google Scholar]
14. Johansson B, Eriksson A, Virtanen I, Thornell LEIntermediate filament proteins in adult human arteries. Anat Rec. 1997;247:439–448.[PubMed][Google Scholar]
15. Ko KS, McCulloch CAIntercellular mechanotransduction: cellular circuits that coordinate tissue responses to mechanical loading. Biochem Biophys Res Commun. 2001;285:1077–1083.[PubMed][Google Scholar]
16. Lepekhin EA, Eliasson C, Berthold CH, Berezin V, Bock E, Pekny MIntermediate filaments regulate astrocyte motility. J Neurochem. 2001;79:617–625.[PubMed][Google Scholar]
17. Marganski WA, Gangopadhyay SS, Je HD, Gallant C, Morgan KGTargeting of a novel Ca+2/calmodulin-dependent protein kinase II is essential for extracellular signal-regulated kinase-mediated signaling in differentiated smooth muscle cells. Circ Res. 2005;97:541–549.[PubMed][Google Scholar]
18. Matsushita T, Oyamada M, Kurata H, Masuda S, Takahashi A, Emmoto T, Shiraishi I, Wada Y, Oka T, Takamatsu TFormation of cell junctions between grafted and host cardiomyocytes at the border zone of rat myocardial infarction. Circulation. 1999;100:II262–II268.[PubMed][Google Scholar]
19. Meriane M, Mary S, Comunale F, Vignal E, Fort P, Gauthier-Rouviere CCdc42Hs and Rac1 GTPases induce the collapse of the vimentin intermediate filament network. J Biol Chem. 2000;275:33046–33052.[PubMed][Google Scholar]
20. Opazo SA, Zhang W, Wu Y, Turner CE, Tang DD, Gunst SJTension development during contractile stimulation of smooth muscle requires recruitment of paxillin and vinculin to the membrane. Am J Physiol Cell Physiol. 2004;286:C433–C447.[PubMed][Google Scholar]
21. Paul RJ, Bowman PS, Kolodney MSEffects of microtubule disruption on force, velocity, stiffness and [Ca(2+)](i) in porcine coronary arteries. Am J Physiol Heart Circ Physiol. 2000;279:H2493–H2501.[PubMed][Google Scholar]
22. Rembold CM, Murphy RAHistamine concentration and Ca2+ mobilization in arterial smooth muscle. Am J Physiol. 1989;257:C122–C128.[PubMed][Google Scholar]
23. Rokolya A, Singer HAInhibition of CaM kinase II activation and force maintenance by KN-93 in arterial smooth muscle. Am J Physiol Cell Physiol. 2000;278:C537–C545.[PubMed][Google Scholar]
24. Sin WC, Chen XQ, Leung T, Lim LRhoA-binding kinase alpha translocation is facilitated by the collapse of the vimentin intermediate filament network. Mol Cell Biol. 1998;18:6325–6339.[Google Scholar]
25. Small JVStructure-function relationships in smooth muscle: the missing links. Bioessays. 1995;17:785–792.[PubMed][Google Scholar]
26. Somlyo AP, Somlyo AVSignal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 522 Pt. 2000;2:177–185.[Google Scholar]
27. Tang DC, Stull JT, Kubota Y, Kamm KERegulation of the Ca2+ dependence of smooth muscle contraction. J Biol Chem. 1992;267:11839–11845.[PubMed][Google Scholar]
28. Tang DD, Bai Y, Gunst SJSilencing of p21-activated kinase attenuates vimentin phosphorylation on Ser-56 and reorientation of the vimentin network during stimulation of smooth muscle cells by 5-hydroxytryptamine. Biochem J. 2005;388:773–783.[Google Scholar]
29. Tang DD, Gunst SJDepletion of focal adhesion kinase by antisense depresses contractile activation of smooth muscle. Am J Physiol Cell Physiol. 2001;280:C874–C883.[PubMed][Google Scholar]
30. Tang DD, Gunst SJThe small GTPase Cdc42 regulates actin polymerization and tension development during contractile stimulation of smooth muscle. J Biol Chem. 2004;279:51722–51728.[PubMed][Google Scholar]
31. Tang DD, Tan JDownregulation of profilin with antisense oligodeoxynucleotides inhibits force development during stimulation of smooth muscle. Am J Physiol Heart Circ Physiol. 2003;285:H1528–H1536.[PubMed][Google Scholar]
32. Tang DD, Tan JRole of Crk-Associated Substrate in the Regulation of Vascular Smooth Muscle Contraction. Hypertension. 2003;42:858–863.[PubMed][Google Scholar]
33. Tang DD, Tao P, Bai YP21-activated protein kinase 1 (PAK1) is required for vimentin phosphorylation at ser-56 during stimulation of smooth muscle tissues. FASEB J. 2004;18:A1085.[PubMed][Google Scholar]
34. Tang DD, Turner CE, Gunst SJExpression of non-phosphorylatable paxillin mutants in canine tracheal smooth muscle inhibits tension development. J Physiol. 2003;553:21–35.[Google Scholar]
35. Tang DD, Turner CE, Gunst SJExpression of non-phosphorylatable paxillin mutants in canine tracheal smooth muscle inhibits tension development. J Physiol. 2003;553:21–35.[Google Scholar]
36. Tang DD, Wu MF, Opazo Saez AM, Gunst SJThe focal adhesion protein paxillin regulates contraction in canine tracheal smooth muscle. J Physiol. 2002;542:501–513.[Google Scholar]
37. Tang DD, Zhang W, Gunst SJThe Adapter Protein CrkII Regulates Neuronal Wiskott-Aldrich Syndrome Protein, Actin Polymerization, and Tension Development during Contractile Stimulation of Smooth Muscle. J Biol Chem. 2005;280:23380–23389.[PubMed][Google Scholar]
38. Valgeirsdottir S, Claesson-Welsh L, Bongcam-Rudloff E, Hellman U, Westermark B, Heldin CHPDGF induces reorganization of vimentin filaments. J Cell Sci. 1998;111 ( Pt 14):1973–1980.[PubMed][Google Scholar]
39. Wede OK, Lofgren M, Li Z, Paulin D, Arner AMechanical function of intermediate filaments in arteries of different size examined using desmin deficient mice. J Physiol. 2002;540:941–949.[Google Scholar]
40. Yin T, Getsios S, Caldelari R, Godsel LM, Kowalczyk AP, Muller EJ, Green KJMechanisms of plakoglobin-dependent adhesion: desmosome-specific functions in assembly and regulation by epidermal growth factor receptor. J Biol Chem. 2005;280:40355–40363.[PubMed][Google Scholar]
41. Zhang D, Jin N, Rhoades RA, Yancey KW, Swartz DRInfluence of microtubules on vascular smooth muscle contraction. J Muscle Res Cell Motil. 2000;21:293–300.[PubMed][Google Scholar]
42. Zhang W, Wu Y, Du L, Tang DD, Gunst SJActivation of the Arp2/3 complex by N-WASp is required for actin polymerization and contraction in smooth muscle. Am J Physiol Cell Physiol. 2005;288:C1145–C1160.[PubMed][Google Scholar]