Dynamin2 organizes lamellipodial actin networks to orchestrate lamellar actomyosin

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Menon, Manisha ^a   Askinazi, Olga L ^a   Schafer, Dorothy A ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CORTACTIN; DYNAMIN II; F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; ACTIN; GUANOSINE TRIPHOSPHATE;

ACTIN FILAMENT; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; CYTOARCHITECTURE; ENDOCYTOSIS; ENZYME ACTIVITY; FOCAL ADHESION; LAMELLAR BODY; LAMELLIPODIUM; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; ANIMAL; CELL ADHESION; CELL LINE; CHEMISTRY; HYDROLYSIS; METABOLISM; PROTEIN TERTIARY STRUCTURE; PSEUDOPODIUM; RAT;

ACTIN CYTOSKELETON; ACTINS; ACTOMYOSIN; ANIMALS; CELL ADHESION; CELL LINE; DYNAMIN II; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PSEUDOPODIA; RATS;

EID: 84899456284     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094330     Document Type: Article

References (64)

1. Heath JP (1983) Behaviour and structure of the leading lamella in moving fibroblasts. I. Occurrence and centripetal movement of arc-shaped microfilament bundles beneath the dorsal cell surface. J Cell Sci 60: 331-354.
2. Hotulainen P, Lappalainen P (2006) Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173: 383-394.
3. Tojkander S, Gateva G, Lappalainen P (2012) Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 125: 1855-1864.
4. Anderson TW, Vaughan AN, Cramer LP (2008) Retrograde flow and myosin II activity within the leading cell edge deliver F-actin to the lamella to seed the formation of graded polarity actomyosin II filament bundles in migrating fibroblasts. Mol Biol Cell 19: 5006-5018.
5. Nemethova M, Auinger S, Small JV (2008) Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J Cell Biol 180: 1233-1244. (Pubitemid 351468477)
6. Burnette DT, Manley S, Sengupta P, Sougrat R, Davidson MW, et al. (2011) A role for actin arcs in the leading-edge advance of migrating cells. Nat Cell Biol 13: 371-381.
7. Alexandrova AY, Arnold K, Schaub S, Vasiliev JM, Meister JJ, et al. (2008) Comparative dynamics of retrograde actin flow and focal adhesions: formation of nascent adhesions triggers transition from fast to slow flow. PLoS One 3: e3234.
8. Gardel ML, Sabass B, Ji L, Danuser G, Schwarz US, et al. (2008) Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J Cell Biol 183: 999-1005.
9. Thievessen I, Thompson PM, Berlemont S, Plevock KM, Plotnikov SV, et al. (2013) Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J Cell Biol 202: 163-177.
10. Choi CK, Vicente-Manzanares M, Zareno J, Whitmore LA, Mogilner A, et al. (2008) Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat Cell Biol.
11. Kruchten AE, McNiven MA (2006) Dynamin as a mover and pincher during cell migration and invasion. J Cell Sci 119: 1683-1690. (Pubitemid 43810995)
12. Menon M, Schafer DA (2013) Dynamin: expanding its scope to the cytoskeleton. International Review of Cell and Molecular Biology 302: 188-219.
13. Tanabe K, Takei K (2009) Dynamic instability of microtubules requires dynamin 2 and is impaired in a Charcot-Marie-Tooth mutant. J Cell Biol 185: 939-948.
14. Thompson HM, Cao H, Chen J, Euteneuer U, McNiven MA (2004) Dynamin 2 binds gamma-tubulin and participates in centrosome cohesion. Nat Cell Biol 6: 335-342. (Pubitemid 38584823)
15. Hamao K, Morita M, Hosoya H (2009) New function of the proline rich domain in dynamin-2 to negatively regulate its interaction with microtubules in mammalian cells. Exp Cell Res 315: 1336-1345.
16. Henmi Y, Tanabe K, Takei K (2011) Disruption of microtubule network rescues aberrant actin comets in dynamin2-depleted cells. PLoS One 6: e28603.
17. Ferguson SM, De Camilli P (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13: 75-88.
18. Gu C, Yaddanapudi S, Weins A, Osborn T, Reiser J, et al. (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. Embo J 29: 3593-3606.
19. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, et al. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198.
20. Chua J, Rikhy R, Lippincott-Schwartz J (2009) Dynamin 2 orchestrates the global actomyosin cytoskeleton for epithelial maintenance and apical constriction. Proc Natl Acad Sci U S A.
21. Mooren OL, Kotova TI, Moore AJ, Schafer DA (2009) Dynamin2 GTPase and cortactin remodel actin filaments. J Biol Chem 284: 23995-24005.
22. Ferguson SM, Raimondi A, Paradise S, Shen H, Mesaki K, et al. (2009) Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 17: 811-822.
23. Destaing O, Ferguson SM, Grichine A, Oddou C, De Camilli P, et al. (2013) Essential Function of Dynamin in the Invasive Properties and Actin Architecture of v-Src Induced Podosomes/Invadosomes. PLoS One 8: e77956.
24. Kasai K, Shin HW, Shinotsuka C, Murakami K, Nakayama K (1999) Dynamin II is involved in endocytosis but not in the formation of transport vesicles from the trans-Golgi network. J Biochem (Tokyo) 125: 780-789. (Pubitemid 29192500)
25. Moravec R, Conger KK, D'Souza R, Allison AB, Casanova JE (2012) BRAG2/GEP100/IQSec1 interacts with clathrin and regulates alpha5beta1 integrin endocytosis through activation of ADP ribosylation factor 5 (Arf5). J Biol Chem 287: 31138-31147.
26. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
27. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, et al. (2005) Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 15: 1276-1285. (Pubitemid 41026593)
28. Watanabe N, Mitchison TJ (2002) Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295: 1083-1086. (Pubitemid 34132240)
29. Krueger EW, Orth JD, Cao H, McNiven MA (2003) A dynamin-cortactin-Arp2/3 complex mediates actin reorganization in growth factor-stimulated cells. Mol Biol Cell 14: 1085-1096. (Pubitemid 36337454)
30. Schafer DA, Weed SA, Binns D, Karginov AV, Parsons JT, et al. (2002) Dynamin2 and cortactin regulate actin assembly and filament organization. Curr Biol 12: 1852-1857. (Pubitemid 35273906)
31. Razidlo GL, Wang Y, Chen J, Krueger EW, Billadeau DD, et al. (2013) Dynamin 2 Potentiates Invasive Migration of Pancreatic Tumor Cells through Stabilization of the Rac1 GEF Vav1. Dev Cell 24: 573-585.
32. Aratyn-Schaus Y, Oakes PW, Gardel ML (2011) Dynamic and structural signatures of lamellar actomyosin force generation. Mol Biol Cell 22: 1330-1339.
33. Oakes PW, Beckham Y, Stricker J, Gardel ML (2012) Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J Cell Biol 196: 363-374.
34. Naumanen P, Lappalainen P, Hotulainen P (2008) Mechanisms of actin stress fibre assembly. J Microsc 231: 446-454.
35. Burridge K, Wittchen ES (2013) The tension mounts: stress fibers as force-generating mechanotransducers. J Cell Biol 200: 9-19.
36. Rossier OM, Gauthier N, Biais N, Vonnegut W, Fardin MA, et al. (2010) Force generated by actomyosin contraction builds bridges between adhesive contacts. EMBO J 29: 1055-1068.
37. Liu YW, Surka MC, Schroeter T, Lukiyanchuk V, Schmid SL (2008) Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol Biol Cell 19: 5347-5359.
38. Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691-698. (Pubitemid 34993705)
39. Orth JD, McNiven MA (2003) Dynamin at the actin-membrane interface. Curr Opin Cell Biol 15: 31-39. (Pubitemid 36044712)
40. Wang Y, Cao H, Chen J, McNiven MA (2011) A direct interaction between the large GTPase dynamin-2 and FAK regulates focal adhesion dynamics in response to active Src. Mol Biol Cell 22: 1529-1538.
41. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305: 1782-1786. (Pubitemid 39249647)
42. Giannone G, Dubin-Thaler BJ, Rossier O, Cai Y, Chaga O, et al. (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128: 561-575. (Pubitemid 46198897)
43. Shemesh T, Verkhovsky AB, Svitkina TM, Bershadsky AD, Kozlov MM (2009) Role of focal adhesions and mechanical stresses in the formation and progression of the lamellipodium-lamellum interface [corrected]. Biophys J 97: 1254-1264.
44. Brown CM, Hebert B, Kolin DL, Zareno J, Whitmore L, et al. (2006) Probing the integrin-actin linkage using high-resolution protein velocity mapping. J Cell Sci 119: 5204-5214. (Pubitemid 46085198)
45. Hu K, Ji L, Applegate KT, Danuser G, Waterman-Storer CM (2007) Differential transmission of actin motion within focal adhesions. Science 315: 111-115. (Pubitemid 46196992)
46. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, et al. (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468: 580-584.
47. Taylor MJ, Lampe M, Merrifield CJ (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10: e1001302.
48. Song BD, Leonard M, Schmid SL (2004) Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J Biol Chem 279: 40431-40436. (Pubitemid 39287632)
49. Lee E, De Camilli P (2002) Dynamin at actin tails. Proc Natl Acad Sci U S A 99: 161-166. (Pubitemid 34060334)
50. Ochoa GC, Slepnev VI, Neff L, Ringstad N, Takei K, et al. (2000) A functional link between dynamin and the actin cytoskeleton at podosomes. J Cell Biol 150: 377-389. (Pubitemid 30491360)
51. Risca VI, Wang EB, Chaudhuri O, Chia JJ, Geissler PL, et al. (2012) Actin filament curvature biases branching direction. Proc Natl Acad Sci U S A 109: 2913-2918.
52. 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. (Pubitemid 23206054)
53. Courson DS, Rock RS (2010) Actin cross-link assembly and disassembly mechanics for alpha-Actinin and fascin. J Biol Chem 285: 26350-26357.
54. Tojkander S, Gateva G, Schevzov G, Hotulainen P, Naumanen P, et al. (2011) A molecular pathway for myosin II recruitment to stress fibers. Curr Biol 21: 539-550.
55. Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM (2010) Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Dev Biol 26: 315-333.
56. Giannone G, Mege RM, Thoumine O (2009) Multi-level molecular clutches in motile cell processes. Trends Cell Biol 19: 475-486.
57. Schwarz US, Gardel ML (2012) United we stand: integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J Cell Sci 125: 3051-3060.
58. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF (2007) Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 176: 573-580. (Pubitemid 46333973)
59. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, et al. (2000) Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150: 797-806. (Pubitemid 30663416)
60. Chrzanowska-Wodnicka M, Burridge K (1996) Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 133: 1403-1415. (Pubitemid 26192339)
61. Stricker J, Beckham Y, Davidson MW, Gardel ML (2013) Myosin II-mediated focal adhesion maturation is tension insensitive. PLoS One 8: e70652.
62. Meyer RK, Aebi U (1990) Bundling of actin filaments by alpha-actinin depends on its molecular length. J Cell Biol 110: 2013-2024.
63. Maciver SK, Wachsstock DH, Schwarz WH, Pollard TD (1991) The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with alpha-actinin. J Cell Biol 115: 1621-1628. (Pubitemid 21910002)
64. Reymann AC, Boujemaa-Paterski R, Martiel JL, Guerin C, Cao W, et al. (2012) Actin network architecture can determine myosin motor activity. Science 336: 1310-1314.