Morphology and viscoelasticity of actin networks formed with the mutually interacting crosslinkers: Palladin and alpha-actinin

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Grooman, Brian ^a   Fujiwara, Ikuko ^b   Otey, Carol ^c   Upadhyaya, Arpita ^a  

^a University of Maryland   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA ACTININ; BINDING PROTEIN; PALLADIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL MOTION; CELL STRUCTURE; CYTOSKELETON; FOCAL ADHESION; MORPHOLOGY; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; STRESS FIBER; VISCOELASTICITY;

ACTININ; ACTINS; BIOPOLYMERS; CYTOSKELETAL PROTEINS; ELASTICITY; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; VISCOSITY;

EID: 84865072891     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042773     Document Type: Article

References (45)

1. Stossel TP, (1993) On the crawling of animal cells. Science 260: 1086-1094.
2. Stossel TP, Chaponnier C, Ezzell RM, Hartwig JH, Janmey PA, et al. (1985) Nonmuscle actin-binding proteins. Annu Rev Cell Biol 1: 353-402.
3. Revenu C, Athman R, Robine S, Louvard D, (2004) The co-workers of actin filaments: from cell structures to signals. Nat Rev Mol Cell Biol 5: 635-646.
4. Janmey PA, McCulloch CA, (2007) Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9: 1-34.
5. Janmey PA, Winer JP, Murray ME, Wen Q, (2009) The hard life of soft cells. Cell Motil Cytoskele-ton 66: 597-605.
6. Fletcher DA, Mullins RD, (2010) Cell mechanics and the cytoskeleton. Nature 463: 485-492.
7. Parast MM, Otey CA, (2000) Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J Cell Biol 150: 643-656.
8. Dixon RD, Arneman DK, Rachlin AS, Sundaresan NR, Costello MJ, et al. (2008) Palladin is an actin cross-linking protein that uses immunoglobulin-like domains to bind filamentous actin. J Biol Chem 283: 6222-6231.
9. Endlich N, Schordan E, Cohen CD, Kretzler M, Lewko B, et al. (2009) Palladin is a dynamic actin-associated protein in podocytes. Kidney Int 75: 214-226.
10. Goicoechea SM, Arneman D, Otey CA, (2008) The role of palladin in actin organization and cell motility. Eur J Cell Biol 87: 517-525.
11. Goicoechea SM, Bednarski B, Garcia-Mata R, Prentice-Dunn H, Kim HJ, et al. (2009) Palladin contributes to invasive motility in human breast cancer cells. Oncogene 28: 587-598.
12. Goicoechea S, Arneman D, Disanza A, Garcia-Mata R, Scita G, et al. (2006) Palladin binds to Eps8 and enhances the formation of dorsal ruffles and podosomes in vascular smooth muscle cells. J Cell Sci 119: 3316-3324.
13. Jin L, Yoshida T, Ho R, Owens GK, Somlyo AV, (2009) The actin-associated protein Palladin is required for development of normal contractile properties of smooth muscle cells derived from embryoid bodies. J Biol Chem 284: 2121-2130.
14. Luo H, Liu X, Wang F, Huang Q, Shen S, et al. (2005) Disruption of palladin results in neural tube closure defects in mice. Mol Cell Neurosci 29: 507-515.
15. Ronty M, Taivainen A, Moza M, Otey CA, Carpen O, (2004) Molecular analysis of the interaction between palladin and alpha-actinin. FEBS Lett 566: 30-34.
16. Tseng Y, Kole TP, Lee JS, Fedorov E, Almo SC, et al. (2005) How actin crosslinking and bundling proteins cooperate to generate an enhanced cell mechanical response. Biochem Biophys Res Com-mun 334: 183-192.
17. Wachsstock DH, Schwartz WH, Pollard TD, (1993) Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels. Biophys J 65: 205-214.
18. Shin JH, Gardel ML, Mahadevan L, Matsudaira P, Weitz DA, (2004) Relating microstructure to rheology of a bundled and cross-linked f-actin network in vitro. Proc Natl Acad Sci U S A 101: 9636-9641.
19. Tempel M, Isenberg G, Sackmann E, (1996) Temperature-induced sol-gel transition and microgel formation in alpha-actinin cross-linked actin networks: A rheological study. Phys Rev E 54: 1802-1810.
20. Ward SM, Weins A, Pollak MR, Weitz DA, (2008) Dynamic viscoelasticity of actin cross-linked with wild-type and disease-causing mutant alpha-actinin-4. Biophys J 95: 4915-4923.
21. Kasza KE, Rowat AC, Liu J, Angelini TE, Brangwynne CP, et al. (2007) The cell as a material. Curr Opin Cell Biol 19: 101-107.
22. Gardel ML, Kasza KE, Brangwynne CP, Liu J, Weitz DA, (2008) Chapter 19: Mechanical response of cytoskeletal networks. Methods Cell Biol 89: 487-519.
23. Kas J, Strey H, Tang JX, Finger D, Ezzell R, et al. (1996) F-actin, a model polymer for semiexible chains in dilute, semidilute, and liquid crystalline solutions. Biophys J 70: 609-625.
24. Sato M, Schwarz WH, Pollard TD, (1987) Dependence of the mechanical properties of actin/alpha-actinin gels on deformation rate. Nature 325: 828-830.
25. Wagner B, Tharmann R, Haase I, Fischer M, Bausch AR, (2006) Cytoskeletal polymer networks: the molecular structure of cross-linkers determines macroscopic properties. Proc Natl Acad Sci USA 103: 13974-13978.
26. Tseng Y, Wirtz D, (2001) Mechanics and multiple-particle tracking microheterogeneity of alpha-actinin-cross-linked actin filament networks. Biophys J 81: 1643-1656.
27. Gardel ML, Shin JH, MacKintosh FC, Mahadevan L, Matsudaira P, et al. (2004) Elastic behaviour of cross-linked and bundled actin networks. Science 304: 1301-1305.
28. Gardel ML, Nakamura F, Hartwig J, Crocker JC, Stossel TP, et al. (2006) Stress-dependent elas-ticity of composite actin networks as a model for cell behavior. Phys Rev Lett 96: 088102.
29. Schmoller KM, Lieleg O, Bausch AR, (2009) Structural and viscoelastic properties of actin/filamin networks: cross-linked versus bundled networks. Biophys J 97: 83-89.
30. Schmoller KM, Lieleg O, Bausch AR, (2008) Cross-linking molecules modify composite actin networks independently. Phys Rev Lett 101: 118102.
31. Esue O, Tseng Y, Wirtz D, (2009) Alpha-actinin and filamin cooperatively enhance the stiffness of actin filament networks. PLoS ONE 4: e4411.
32. MacKintosh FC, Kas J, Janmey PA, (1995) Elasticity of semiexible biopolymer networks. Phys Rev Lett 75: 4425-4428.
33. Claessens MM, Bathe M, Frey E, Bausch AR, (2006) Actin-binding proteins sensitively mediate f-actin bundle stiffness. Nat Mater 5: 748-753.
34. Strehle D, Schnauss J, Heussinger C, Alvarado J, Bathe M, et al. (2011) Transiently crosslinked f-actin bundles. Eur Biophys J 40: 93-101.
35. Lieleg O, Bausch AR, (2007) Cross-linker unbinding and self-similarity in bundled cytoskeletal networks. Phys Rev Lett 99: 158105.
36. Stein AM, Vader DA, Jawerth LM, Weitz DA, Sander LM, (2008) An algorithm for extracting the network geometry of three-dimensional collagen gels. J Microsc 232: 463-475.
37. Lindstrom SB, Vader DA, Kulachenko A, Weitz DA, (2010) Biopolymer network geometries: char-acterization, regeneration, and elastic properties. Phys Rev E 82: 051905.
38. Mickel W, Munster S, Jawerth LM, Vader DA, Weitz DA, et al. (2008) Robust pore size analysis of filamentous networks from three-dimensional confocal microscopy. Biophys J 95: 6072-6080.
39. Gardel ML, Nakamura F, Hartwig JH, Crocker JC, Stossel TP, et al. (2006) Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc Natl Acad Sci USA 103: 1762-1767.
40. Storm C, Pastore JJ, MacKintosh FC, Lubensky TC, Janmey PA, (2005) Nonlinear elasticity in biological gels. Nature 435: 191-194.
41. Popowicz GM, Schleicher M, Noegel AA, Holak TA, (2006) Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem Sci 31: 411-419.
42. Lieleg O, Claessens MM, Luan Y, Bausch AR, (2008) Transient binding and dissipation in cross-linked actin networks. Phys Rev Lett 101: 108101.
43. Lieleg O, Schmoller KM, Claessens MM, Bausch AR, (2009) Cytoskeletal polymer networks: vis-coelastic properties are determined by the microscopic interaction potential of cross-links. Biophys J 96: 4725-4732.
44. Borrego-Diaz E, Kerff F, Lee SH, Ferron F, Li Y, et al. (2006) Crystal structure of the actin-binding domain of alpha-actinin 1: evaluating two competing actin-binding models. J Struct Biol 155: 230-238.
45. Mickel W, Munster S, Jawerth LM, Vader DA, Weitz DA, et al. (2008) Robust pore size analysis of filamentous networks from three-dimensional confocal microscopy. Biophys J 95: 6072-6080.