Substrate stiffness regulates solubility of cellular vimentin

Molecular Biology of the Cell

Volumn 25, Issue 1, 2014, Pages 87-94

  Murray, Maria E ^a,b   Mendez, Melissa G ^b   Janmey, Paul A ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEBBISTATIN; CYTOCHALASIN D; NOCODAZOLE; VIMENTIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CONTACT; CELL DISRUPTION; CELL FUNCTION; CELL GROWTH; CELL MEMBRANE; CELL MIGRATION; CELL SPREADING; CELL STRAIN 3T3; CELL STRUCTURE; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VIVO STUDY; INTERMEDIATE FILAMENT; MESENCHYMAL STEM CELL; NERVE CELL INHIBITION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; SIGNAL TRANSDUCTION; SOLUBILITY; SUBSTRATE STIFFNESS;

CELL ADHESION; CELLS, CULTURED; CULTURE MEDIA; CYTOSKELETON; DETERGENTS; ELASTIC MODULUS; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; RHO-ASSOCIATED KINASES; SOLUBILITY; VIMENTIN;

EID: 84891771576     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-06-0326     Document Type: Article

References (49)

1. Ando S, Nakao K, Gohara R, Takasaki Y, Suehiro K, Oishi Y (2004).Morphological analysis of glutaraldehyde-fixed vimentin intermediate filaments and assembly-intermediates by atomic force microscopy. Biochim Biophys Acta 1702, 53-65.
2. Bhadriraju K, Yang M, Ruiz SA, Pirone DM, Tan J, Chen CS, Alom Ruiz S (2007). Activation of ROCK by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp Cell Res 313, 3616-3623.
3. Blikstad I, Lazarides E (1983). Vimentin filaments are assembled from a soluble precursor in avian erythroid cells. J Cell Biol 96, 1803-1808.
4. Bocquet A, Berges R, Frank R, Robert P, Peterson AC, Eyer J (2009). Neurofilaments bind tubulin and modulate its polymerization. J Neurosci 29, 11043-11054.
5. Byfield FJ, Reen RK, Shentu T-P, Levitan I, Gooch KJ (2009). Endothelial actin and cell stiffness is modulated by substrate stiffness in 2D and 3D. J Biomech 42, 1114-1119.
6. Califano JP, Reinhart-King CA (2010). Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng 3, 68-75.
7. Chang L, Goldman RD (2004). Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol 5, 601-613.
8. Chang F, Lemmon C (2007). FAK potentiates Rac1 activation and localization to matrix adhesion sites: a role for βPIX. Mol Biol Cell 18, 253-264.
9. Dupont S et al. (2011). Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183.
10. Edwards DC, Sanders LC, Bokoch GM, Gill GN (1999). Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1, 253-259.
11. Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D (2004a). Substrate compliance versus ligand density in cell on gel responses. Biophys J 86, 617-628.
12. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE (2004b). Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166, 877-887.
13. Engler AJ, Sen S, Sweeney HL, Discher DE (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
14. Eriksson JE, He T, Trejo-Skalli AV, Härmälä-Braskén A-S, Hellman J, Chou Y-H, Goldman RD (2004). Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117, 919-932.
15. Even-Ram S, Doyle AD, Conti MA, Matsumoto K, Adelstein RS, Yamada KM (2007). Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat Cell Biol 9, 299-309.
16. Gilbert M, Fulton AB (1985). The specificity and stability of the Triton-extracted cytoskeletal framework of gerbil fibroma cells. J Cell Sci 73, 335-345.
17. Goto H, Kosako H, Tanabe K, Yanagida M, Sakurai M, Amano M, Kaibuchi K, Inagaki M (1998). Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J Biol Chem 273, 11728-11736.
18. Goto H, Tanabe K, Manser E, Lim L, Yasui Y, Inagaki M (2002). Phosphorylation and reorganization of vimentin by p21-activated kinase (PAK). Genes Cells 7, 91-97.
19. Gyoeva F, Gelfand V (1991). Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353, 445-448.
20. Helfand BT et al. (2011). Vimentin organization modulates the formation of lamellipodia. Mol Biol Cell 22, 1274-1289.
21. Helfand BT, Mikami A, Vallee RB, Goldman RD (2002). A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J Cell Biol 157, 795-806.
22. Herrmann H, Kreplak L, Aebi U (2004). Isolation, characterization, and in vitro assembly of intermediate filaments. Methods Cell Biol 78, 3-24.
23. Hinz B, Dugina V, Ballestream C, Wehrle-Haller B, Chaponnier C (2003). Alpha smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts. Mol Biol Cell 14, 2508-2519.
24. Hyder CL, Pallari H-M, Kochin V, Eriksson JE (2008). Providing cellular signposts-post-translational modifications of intermediate filaments. FEBS Lett 582, 2140-2148.
25. Janmey PA, Euteneuer U, Traub P, Schliwa M (1991). Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J Cell Biol 113, 155-160.
26. Kacher CM, Weiss IM, Stewart RJ, Schmidt CF, Hansma PK, Radmacher M, Fritz M (2000). Imaging microtubules and kinesin decorated microtubules using tapping mode atomic force microscopy in fluids. Eur Biophys J 28, 611-620.
27. Kim TJ, Seong J, Ouyang M, Sun J, Lu S, Hong JP, Wang N, Wang Y (2009). Substrate rigidity regulates Ca2+ oscillation via RhoA pathway in stem cells. J Cell Physiol 218, 285-293.
28. Klein EA, Yin L, Kothapalli D, Castagnino P, Byfield FJ, Xu T, Levental I, Hawthorne E, Janmey PA, Assoian RK (2009). Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr Biol 19, 1511-1518.
29. Kreplak L, Bär H, Leterrier JF, Herrmann H, Aebi U (2005). Exploring the mechanical behavior of single intermediate filaments. J Mol Biol 354, 569-577.
30. Levental I, Georges PC, Janmey PA (2007). Soft biological materials and their impact on cell function. Soft Matter 3, 299-306.
31. Li Q-F, Spinelli AM, Wang R, Anfinogenova Y, Singer HA, Tang DD (2006). Critical role of vimentin phosphorylation at Ser-56 by p21-activated kinase in vimentin cytoskeleton signaling. J Biol Chem 281, 34716-34724.
32. Liu B, Chrzanowska-Wodnicka M, Burridge K (1998). Microtubule depolymerization induces stress fibers, focal adhesions, and DNA synthesis via the GTP-binding protein Rho. Cell Adhes Commun 5, 249-255.
33. Mücke N, Kirmse R, Wedig T, Leterrier JF, Kreplak L (2005). Investigation of the morphology of intermediate filaments adsorbed to different solid supports. J Struct Biol 150, 268-276.
34. Osborn M, Weber K (1977). The detergent-resistant cytoskeleton of tissue culture cells includes the nucleus and the microfilament bundles. Exp Cell Res 106, 339-349.
35. Pelham RJ Jr, Wang Y (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94, 13661-13665.
36. Peyton SR, Putnam AJ (2005). Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 204, 198-209.
37. Polioudaki H, Kastrinaki M-C, Papadaki HA, Theodoropoulos PA (2009). Microtubule-interacting drugs induce moderate and reversible damage to human bone marrow mesenchymal stem cells. Cell Prolif 42, 434-447.
38. Qin Z, Kreplak L, Buehler MJ (2009). Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLoS One 4, e7294.
39. Raab M, Swift J, Dingal PPCD, Shah P, Shin J-W, Discher DE (2012). Crawling from soft to stiff matrix polarizes the cytoskeleton and phosphoregulates myosin-II heavy chain. J Cell Biol 199, 669-683.
40. Ridley AJ, Hall A (1992). The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
41. Rotsch C, Radmacher M (2000). Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys J 78, 520-535.
42. Soellner P, Quinlan RA, Franke WW (1985). Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells. Proc Natl Acad Sci USA 82, 7929-7933.
43. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA (2007). Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93, 4453-4461.
44. Strelkov SV, Herrmann H, Aebi U (2003). Molecular architecture of intermediate filaments. Bioessays 25, 243-251.
45. Tee S-Y, Fu J, Chen CS, Janmey PA (2011). Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100, L25-7.
46. Weisenhorn AL, Drake B, Prater CB, Gould Sa, Hansma PK, Ohnesorge F, Egger M, Heyn SP, Gaub HE (1990). Immobilized proteins in buffer imaged at molecular resolution by atomic force microscopy. Biophys J 58, 1251-1258.
47. Winer JP, Janmey PA, McCormick ME, Funaki M (2009a). Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A 15, 147-154.
48. Winer JP, Oake S, Janmey PA (2009b). Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS One 4, e6382.
49. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, Zahir N, Ming W, Weaver V, Janmey PA (2005). Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60, 24-34.