Essential function of dynamin in the invasive properties and actin architecture of v-Src induced podosomes/invadosomes

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Destaing, Olivier ^a,b   Ferguson, Shawn M ^b   Grichine, Alexei ^a   Oddou, Christiane ^a   De Camilli, Pietro ^b,d   Albiges Rizo, Corinne ^a,d   Baron, Roland ^c,d  

^a INSTITUT ALBERT BONNIOT   (France)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DYNAMIN; F ACTIN; PROTEIN KINASE P60;

ANIMAL CELL; ARTICLE; CELL COMPONENT; CELL INVASION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENZYME ACTIVITY; FIBROBLAST; FOCAL ADHESION; INVADOSOME; MOUSE; NONHUMAN; PODOSOME; PROTEIN DEPLETION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

ACTINS; ANIMALS; CELLS, CULTURED; DYNAMINS; FIBROBLASTS; MICE; ONCOGENE PROTEIN PP60(V-SRC);

EID: 84892574066     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077956     Document Type: Article

References (69)

1. 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.
2. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12: 517-533.
3. Schmid SL, Frolov VA (2011) Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol 27: 79-105.
4. Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9: e1000604.
5. Schafer DA (2004) Regulating actin dynamics at membranes: a focus on dynamin. Traffic 5: 463-469.
6. Gomez TS, Hamann MJ, McCarney S, Savoy DN, Lubking CM, et al. (2005) Dynamin 2 regulates T cell activation by controlling actin polymerization at the immunological synapse. Nat Immunol 6: 261-270.
7. Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414.
8. Orth JD, Krueger EW, Cao H, McNiven MA (2002) The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci U S A 99: 167-172.
9. Lee E, De Camilli P (2002) Dynamin at actin tails. Proc Natl Acad Sci U S A 99: 161-166.
10. Orth JD, Krueger EW, Weller SG, McNiven MA (2006) A novel endocytic mechanism of epidermal growth factor receptor sequestration and internalization. Cancer Res 66: 3603-3610.
11. Yamada H, Abe T, Li SA, Masuoka Y, Isoda M, et al. (2009) Dynasore, a dynamin inhibitor, suppresses lamellipodia formation and cancer cell invasion by destabilizing actin filaments. Biochem Biophys Res Commun 390: 1142-1148.
12. 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.
13. 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.
14. Bruzzaniti A, Neff L, Sanjay A, Horne WC, De Camilli P, et al. (2005) Dynamin forms a Src kinase-sensitive complex with Cbl and regulates podosomes and osteoclast activity. Mol Biol Cell 16: 3301-3313.
15. Baldassarre M, Pompeo A, Beznoussenko G, Castaldi C, Cortellino S, et al. (2003) Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell 14: 1074-1084.
16. 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 106: 20770-20775.
17. Grabs D, Slepnev VI, Songyang Z, David C, Lynch M, et al. (1997) The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J Biol Chem 272: 13419-13425.
18. 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.
19. Salazar MA, Kwiatkowski AV, Pellegrini L, Cestra G, Butler MH, et al. (2003) Tuba, a novel protein containing bin/amphiphysin/Rvs and Dbl homology domains, links dynamin to regulation of the actin cytoskeleton. J Biol Chem 278: 49031-49043.
20. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, et al. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9: 791-804.
21. Mooren OL, Kotova TI, Moore AJ, Schafer DA (2009) Dynamin2 GTPase and cortactin remodel actin filaments. J Biol Chem 284: 23995-24005.
22. 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.
23. Shen H, Ferguson SM, Dephoure N, Park R, Yang Y, et al. (2011) Constitutive activated Cdc42-associated kinase (Ack) phosphorylation at arrested endocytic clathrin-coated pits of cells that lack dynamin. Mol Biol Cell 22: 493-502.
24. Destaing O, Block MR, Planus E, Albiges-Rizo C (2011) Invadosome regulation by adhesion signaling. Curr Opin Cell Biol.
25. Linder S (2009) Invadosomes at a glance. J Cell Sci 122: 3009-3013.
26. Saltel F, Daubon T, Juin A, Ganuza IE, Veillat V, et al. (2011) Invadosomes: intriguing structures with promise. Eur J Cell Biol 90: 100-107.
27. Luxenburg C, Geblinger D, Klein E, Anderson K, Hanein D, et al. (2007) The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS ONE 2: e179.
28. Winograd-Katz SE, Brunner MC, Mirlas N, Geiger B (2011) Analysis of the signaling pathways regulating Src-dependent remodeling of the actin cytoskeleton. Eur J Cell Biol 90: 143-156.
29. Destaing O, Saltel F, Geminard JC, Jurdic P, Bard F (2003) Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol Biol Cell 14: 407-416.
30. Badowski C, Pawlak G, Grichine A, Chabadel A, Oddou C, et al. (2008) Paxillin Phosphorylation Controls Invadopodia/Podosomes Spatiotemporal Organization. Mol Biol Cell 19: 633-645.
31. Albiges-Rizo C, Destaing O, Fourcade B, Planus E, Block MR (2009) Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J Cell Sci 122: 3037-3049.
32. Jurdic P, Saltel F, Chabadel A, Destaing O (2006) Podosome and sealing zone: specificity of the osteoclast model. Eur J Cell Biol 85: 195-202.
33. Destaing O, Saltel F, Gilquin B, Chabadel A, Khochbin S, et al. (2005) A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 118: 2901-2911.
34. Marchisio PC, Cirillo D, Naldini L, Primavera MV, Teti A, et al. (1984) Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J Cell Biol 99: 1696-1705.
35. Destaing O, Planus E, Bouvard D, Oddou C, Badowski C, et al. (2010) β1A integrin is a master regulator of invadosome organization and function. Mol Biol Cell 21: 4108-4119.
36. Cao H, Garcia F, McNiven MA (1998) Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 9: 2595-2609.
37. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, et al. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316: 570-574.
38. Tarone G, Cirillo D, Giancotti FG, Comoglio PM, Marchisio PC (1985) Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp Cell Res 159: 141-157.
39. 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.
40. Sever S, Muhlberg AB, Schmid SL (1999) Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398: 481-486.
41. Sever S, Damke H, Schmid SL (2000) Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol 150: 1137-1148.
42. Marks B, Stowell MH, Vallis Y, Mills IG, Gibson A, et al. (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410: 231-235.
43. Kenniston JA, Lemmon MA (2010) Dynamin GTPase regulation is altered by PH domain mutations found in centronuclear myopathy patients. Embo J 29: 3054-3067.
44. Okamoto PM, Herskovits JS, Vallee RB (1997) Role of the basic, proline-rich region of dynamin in Src homology 3 domain binding and endocytosis. J Biol Chem 272: 11629-11635.
45. Bulina ME, Lukyanov KA, Britanova OV, Onichtchouk D, Lukyanov S, et al. (2006) Chromophore-assisted light inactivation (CALI) using the phototoxic fluorescent protein KillerRed. Nat Protoc 1: 947-953.
46. Poincloux R, Lizarraga F, Chavrier P (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122: 3015-3024.
47. Sweitzer SM, Hinshaw JE (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93: 1021-1029.
48. Takei K, Haucke V, Slepnev V, Farsad K, Salazar M, et al. (1998) Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94: 131-141.
49. Destaing O, Sanjay A, Itzstein C, Horne WC, Toomre D, et al. (2008) The Tyrosine Kinase Activity of c-Src Regulates Actin Dynamics and Organization of Podosomes in Osteoclasts. Mol Biol Cell 19: 394-404.
50. Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1: 33-39.
51. Farsad K, Ringstad N, Takei K, Floyd SR, Rose K, et al. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155: 193-200.
52. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, et al. (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495-499.
53. Linder S, Higgs H, Hufner K, Schwarz K, Pannicke U, et al. (2000) The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J Immunol 165: 221-225.
54. Bharti S, Inoue H, Bharti K, Hirsch DS, Nie Z, et al. (2007) Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol Cell Biol 27: 8271-8283.
55. Tsuboi S, Takada H, Hara T, Mochizuki N, Funyu T, et al. (2009) FBP17 mediates a common molecular step in the formation of podosomes and phagocytic cups in macrophages. J Biol Chem 284: 8548-8556.
56. Pichot CS, Arvanitis C, Hartig SM, Jensen SA, Bechill J, et al. (2010) Cdc42-interacting protein 4 promotes breast cancer cell invasion and formation of invadopodia through activation of N-WASp. Cancer Res 70: 8347-8356.
57. Huynh KK, Grinstein S (2008) Phagocytosis: dynamin's dual role in phagosome biogenesis. Curr Biol 18: R563-565.
58. Ho HY, Rohatgi R, Lebensohn AM, Le M, Li J, et al. (2004) Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118: 203-216.
59. Wu H, Parsons JT (1993) Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J Cell Biol 120: 1417-1426.
60. McPherson PS (2002) The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol 12: 312-315.
61. Bian X, Klemm RW, Liu TY, Zhang M, Sun S, et al. (2011) Structures of the atlastin GTPase provide insight into homotypic fusion of endoplasmic reticulum membranes. Proc Natl Acad Sci U S A 108: 3976-3981.
62. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5: 133-147.
63. Low HH, Lowe J (2010) Dynamin architecture-from monomer to polymer. Curr Opin Struct Biol 20: 791-798.
64. Ford MG, Jenni S, Nunnari J (2011) The crystal structure of dynamin. Nature 477: 561-566.
65. Faelber K, Posor Y, Gao S, Held M, Roske Y, et al. (2011) Crystal structure of nucleotide-free dynamin. Nature 477: 556-560.
66. Chappie JS, Acharya S, Leonard M, Schmid SL, Dyda F (2010) G domain dimerization controls dynamin's assembly-stimulated GTPase activity. Nature 465: 435-440.
67. Chappie JS, Mears JA, Fang S, Leonard M, Schmid SL, et al. (2011) A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147: 209-222.
68. Shpetner HS, Vallee RB (1989) Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59: 421-432.
69. Eppinga RD, Krueger EW, Weller SG, Zhang L, Cao H, et al. (2011) Increased expression of the large GTPase dynamin 2 potentiates metastatic migration and invasion of pancreatic ductal carcinoma. Oncogene.