The role of dynamin in the assembly and function of podosomes and invadopodia

Frontiers in Bioscience

Volumn 9, Issue , 2004, Pages 1944-1953

  McNiven, Mark A ^a   Baldassarre, Massimiliano ^b   Buccione, Roberto ^b  

^a MAYO GRADUATE SCHOOL   (United States)

^b Laboratorio Angela Valenti dei Fattori Genetici e Ambientali di Rischio Trombotico   (Italy)

Author keywords

Cell invasion; Dynamin; Invadopodia; Podosomes; Review

Indexed keywords

ACTIN; CORTACTIN; DYNAMIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PROFILIN; ACTIN BINDING PROTEIN;

CANCER CELL; CELL ADHESION; CELL MOTILITY; CELL STRUCTURE; EXTRACELLULAR MATRIX; HUMAN; LAMELLIPODIA; MELANOMA CELL; MONOCYTE; PODOSOME; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; ANIMAL; CANCER INVASION; CELL MOTION; MEMBRANE STRUCTURE; METABOLISM; NEOPLASM; OSTEOCLAST; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; CELL ADHESION; CELL MEMBRANE STRUCTURES; CELL MOVEMENT; DYNAMINS; HUMANS; MICROFILAMENT PROTEINS; MONOCYTES; NEOPLASM INVASIVENESS; NEOPLASMS; OSTEOCLASTS;

EID: 2442664415     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1348     Document Type: Review

References (85)

1. Adams, J. C: Regulation of protrusive and contractile cell-matrix contacts. J Cell Sci 115, 257 (2002)
2. Adams, J.C: Cell-matrix contact structures. Cell Mol Life Sci 58, 371 (2001)
3. Linder, S., M. Aepfelbacher: Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 13, 376 (2003)
4. Gavazzi, I., M. V. Nermut, P. C. Marchisio: Ultrastructure and gold-immunolabelling of cell-substratum adhesions (podosomes) in RSV-transformed BHK cells. J Cell Sci 94, 85 (1989)
5. S. C. Mueller, W. T. Chen: Cellular invasion into matrix beads: localization of beta 1 integrins and fibronectin to the invadopodia. J Cell Sci 99, 213 (1991)
6. Bowden, E. T., P. J. Coopman, S. C. Mueller: Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol 63, 613 (2001)
7. Baldassarre, M., A. Pompeo, G. Beznoussenko, C. Castaldi, S. Cortellino, M. A. McNiven, A. Luini, R. Buccione: Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell 14, 1074 (2003)
8. Mueller, S. C., Y. Yeh, W. T. Chen: Tyrosine phosphorylation of membrane proteins mediates cellular invasion by transformed cells. J Cell Biol 119, 1309 (1992)
9. Monsky, W. L., C. Y. Lin, A. Aoyama, T. Kelly, S. K. Akiyama, S. C. Mueller, W. T. Chen: A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res 54, 5702 (1994)
10. Nakahara, H., S. C. Mueller, M. Nomizu, Y. Yamada, Y. Yeh, W. T. Chen: Activation of betal integrin signaling stimulates tyrosine phosphorylation of p190RhoGAP and membrane-protrusive activities at invadopodia. J Biol Chem 273, 9 (1998)
11. Bowden, E. T., M. Barth, D. Thomas, R. I. Glazer, S. C. Mueller: An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 18, 4440 (1999)
12. Chen, W. T: Proteases associated with invadopodia, and their role in degradation of extracellular matrix. Enzyme Protein 49, 59 (1996)
13. Chen, W. T., J. Y. Wang: Specialized surface protrusions of invasive cells, invadopodia and lamellipodia, have differential MT1-MMP, MMP-2, and TIMP-2 localization. Ann N Y Acad Sci 878, 361 (1999)
14. Teti, A., H. C. Blair, P. Schlesinger, M. Grano, A. Zambonin-Zallone, A. J. Kahn, S. L. Teitelbaum, K. A. Hruska: Extracellular protons acidify osteoclasts, reduce cytosolic calcium, and promote expression of cell-matrix attachment structures. J Clin Invest 84, 773 (1989)
15. Zambonin-Zallone, A., A. Teti, A. Carano, P. C. Marchisio: The distribution of podosomes in osteoclasts cultured on bone laminae: effect of retinol. J Bone Miner Res 3, 517 (1988)
16. Sato, T., M. del Carmen Ovejero, P. Hou, A. M. Heegaard, M. Kumegawa, N. T. Foged, J. M. Delaisse: Identification of the membrane-type matrix metalloproteinase MTl-MMP in osteoclasts. J Cell Sci 110, 589 (1997)
17. Orth, J. D., M. A. McNiven: Dynamin at the actin-membrane interface. Curr Opin Cell Biol 15, 31 (2003)
18. Ochoa, G. C., V. I. Slepnev, L. Neff, N. Ringstad, K. Takei, L. Daniell, W. Kim, H. Cao, M. McNiven, R. Baron, P. De Camilli: A functional link between dynamin and the actin cytoskeleton at podosomes. J Cell Biol 150, 377 (2000)
19. Hinshaw, J. E: Dynamin and Its Role in Membrane Fission. Annu Rev Cell Dev Biol 483 (2000)
20. Oh, P., D. P. McIntosh, J. E. Schnitzer: Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141, 101 (1998)
21. Jones, S. M., K. E. Howell, J. R. Henley, H. Cao, M. A. McNiven: Role of dynamin in the formation of transport vesicles from the trans- Golgi network. Science 279, 573 (1998)
22. Gold, E. S., D. M. Underhill, N. S. Morrissette, J. Guo, M. A. McNiven, A. Aderem: Dynamin 2 is required for phagocytosis in macrophages. J Exp Med 190, 1849 (1999)
23. Krueger, E. W., J. D. Orth, H. Cao, M. A. McNiven: A Dynamin-Cortactin- Arp2/3 Complex Mediates Actin Reorganization in Growth Factor-stimulated Cells. Mol Biol Cell 14, 1085 (2003)
24. McNiven, M. A., L. Kimn, E. W. Krueger, J. D. Orth, H. Cao, T. W. Wong: Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151, 187 (2000)
25. Schmid, S. L., M. A. McNiven, P. De Camilli: Dynamin and its partners: a progress report. Curr Opin Cell Biol 10, 504 (1998)
26. McNiven, M. A., H. Cao, K. R. Pitts, Y. Yoon: The dynamin family of mechanoenzymes: pinching in new places. Trends Biochem Sci 25, 115 (2000)
27. Sever, S., H. Damke, S. L. Schmid: Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1, 385 (2000)
28. Muhlberg, A. B., S. L. Schmid: Domain structure and function of dynamin probed by limited proteolysis. Methods 20, 475 (2000)
29. Muhlberg, A. B., D. E. Warnock, S. L. Schmid: Domain structure and intramolecular regulation of dynamin GTPase. Embo J 16, 6676 (1997)
30. Sever, S., H. Damke, S. L. Schmid: Dynamin: GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol 150, 1137 (2000)
31. Marks, B., M. H. Stowell, Y. Vallis, I. G. Mills, A. Gibson, C. R. Hopkins, H. T. McMahon: GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231 (2001)
32. Zheng, J., S. M. Cahill, M. A. Lemmon, D. Fushman, J. Schlessinger, D. Cowburn: Identification of the binding site for acidic phospholipids on the pH domain of dynamin: implications for stimulation of GTPase activity. J Mol Biol 255, 14 (1996)
33. Jost, M., F. Simpson, J. M. Kavran, M. A. Lemmon, S. L. Schmid: Phosphatidylinositol-4, 5-bisphosphate is required for endocytic coated vesicle formation. Curr Biol 8, 1399 (1998)
34. Gout, I., R. Dhand, I. D. Hiles, M. J. Fry, G. Panayotou, P. Das, O. Truong, N. F. Totty, J. Hsuan, G. W. Booker: The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25 (1993)
35. Seedorf, K., G. Kostka, R. Lammers, P. Bashkin, R. Daly, W. H. Burgess, A. M. van der Bliek, J. Schlessinger, A. Ullrich: Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2. J Biol Chem 269, 16009 (1994)
36. McPherson, P. S: Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal 11, 229 (1999)
37. Grabs, D., V. I. Slepnev, Z. Songyang, C. David, M. Lynch, L. C. Cantley, P. De Camilli: 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 (1997)
38. Ringstad, N., Y. Nemoto, P. De Camilli: The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci USA 94, 8569 (1997)
39. Witke, W., A. V. Podtelejnikov, A. Di Nardo, J. D. Sutherland, C. B. Gurniak, C. Dotti, M. Mann: In: mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. Embo J 17, 967 (1998)
40. Qualmann, B., J. Roos, P. J. DiGregorio, R. B. Kelly: Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10, 501 (1999)
41. Kessels, M. M., A. E. Engqvist-Goldstein, D. G. Drubin, B. Qualmann: Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J Cell Biol 153, 351 (2001)
42. Schluter, K., B. M. Jockusch, M. Rothkegel: Profilins as regulators of actin dynamics. Biochim Biophys Acta 1359, 97 (1997)
43. Higgs, H. N: Actin nucleation: nucleation-promoting factors are not all equal. Curr Biol R1009 (2001)
44. Caron, E: Regulation of Wiskott-Aldrich syndrome protein and related molecules. Curr Opin Cell Biol 14, 82 (2002)
45. Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond, A. Bretscher, C. Boone: Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612 (2002)
46. Sagot, I., A. A. Rodal, J. Moseley, B. L. Goode, D. Pellman: An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4, 626 (2002)
47. Wu, H., A. B. Reynolds, S. B. Kanner, R. R. Vines, J. T. Parsons: Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol Cell Biol 11, 5113 (1991)
48. Lee, E., P. De Camilli: From the Cover: Dynamin at actin tails. Proc Natl Acad Sci USA 99, 161 (2002)
49. Orth, J. D., E. W. Krueger, H. Cao, M. A. McNiven: 〉From the Cover: The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci USA 99, 167 (2002)
50. Li, Y., M. Tondravi, J. Liu, E. Smith, C. C. Haudenschild, M. Kaczmarek, X. Zhan: Cortactin potentiates bone metastasis of breast cancer cells. Cancer Res 61, 6906 (2001)
51. Weed, S. A., J. T. Parsons: Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20, 6418 (2001)
52. Huang, C., Y. Ni, T. Wang, Y. Gao, C. C. Haudenschild, X. Zhan: Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J Biol Chem 272, 13911 (1997)
53. Weaver, A. M., J. E. Heuser, A. V. Karginov, W. L. Lee, J. T. Parsons, J. A. Cooper: Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 12, 1270 (2002)
54. Schafer, D. A., S. A. Weed, D. Binns, A. V. Karginov, J. T. Parsons, J. A. Cooper: Dynamin2 and cortactin regulate actin assembly and filament organization. Curr Biol 12, 1852 (2002)
55. Kessels, M. M., A. E. Engqvist-Goldstein, D. G. Drubin: Association of mouse actin-binding protein 1 (mAbp1/SH3P7), an Src kinase target, with dynamic regions of the cortical actin cytoskeleton in response to Rac1 activation. Mol Biol Cell 11, 393 (2000)
56. Goode, B. L., A. A. Rodal, G. Barnes, D. G. Drubin: Activation of the Arp2/3 complex by the actin filament binding protein Abplp. J Cell Biol 153, 627 (2001)
57. Hussain, N. K., S. Jenna, M. Glogauer, C. C. Quinn, S. Wasiak, M. Guipponi, S. E. Antonarakis, B. K. Kay, T. P. Stossel, N. Lamarche-Vane, P. S. McPherson: Endocytic protein intersectin-1 regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3, 927 (2001)
58. Qualmann, B., R. B. Kelly: Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol 148, 1047 (2000)
59. Miki, H., K. Miura, K. Matuoka, T. Nakata, N. Hirokawa, S. Orita, K. Kaibuchi, Y. Takai, T. Takenawa: Association of Ash/Grb-2 with dynamin through the Src homology 3 domain. J Biol Chem 269, 5489 (1994)
60. Wunderlich, L., A. Farago, L. Buday: Characterization of interactions of Nck with Sos and dynamin. Cell Signal 11, 25 (1999)
61. Scaplehorn, N., A. Holmstrom, V. Moreau, F. Frischknecht, I. Reckmann, M. Way: Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr Biol 12, 740 (2002)
62. Benesch, S., S. Lommel, A. Steffen, T. E. Stradal, N. Scaplehorn, M. Way, J. Wehland, K. Rottner: Phosphatidylinositol 4, 5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J Biol Chem 277, 37771 (2002)
63. Sweitzer, S. M., J. E. Hinshaw: Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021 (1998)
64. Stowell, M. H., B. Marks, P. Wigge, H. T. McMahon: Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring [see comments]. Nat Cell Biol 1, 27 (1999)
65. Tarone, G., D. Cirillo, F. G. Giancotti, P. M. Comoglio, P. C. Marchisio: Rous sarcoma virus-transformed fibroblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp Cell Res 159, 141 (1985)
66. David-Pfeuty, T., S. J. Singer: Altered distributions of the cytoskeletal proteins vinculin and alpha-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proc Natl Acad Sci USA 77, 6687 (1980)
67. Marchisio, P. C., D. Cirillo, L. Naldini, M. V. Primavera, A. Teti, A. Zambonin-Zallone: Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures. J Cell Biol 99, 1696 (1984)
68. Marchisio, P. C., D. Cirillo, A. Teti, A. Zambonin-Zallone, G. Tarone: Rous sarcoma virus-transformed fibroblasts and cells of monocytic origin display a peculiar dot-like organization of cytoskeletal proteins involved in microfilament-membrane interactions. Exp Cell Res 169, 202 (1987)
69. Marchisio, P. C., L. Bergui, G. C. Corbascio, O. Cremona, N. D'Urso, M. Schena, L. Tesio, F. Caligaris-Cappio: Vinculin, talin, and integrins are localized at specific adhesion sites of malignant B lymphocytes. Blood 72, 830 (1988)
70. Stickel, S. K., Y. L. Wang: Alpha-actinin-containing aggregates in transformed cells are highly dynamic structures. J Cell Biol 104, 1521 (1987)
71. Gaidano, G., L. Bergui, M. Schena, M. Gaboli, O. Cremona, P. C. Marchisio, F. Caligaris-Cappio: Integrin distribution and cytoskeleton organization in normal and malignant monocytes. Leukemia 4, 682 (1990)
72. Shaw, L. M., J. M. Messier, A. M. Mercurio: The activation dependent adhesion of macrophages to laminin involves cytoskeletal anchoring and phosphorylation of the alpha 6 beta 1 integrin. J Cell Biol 110, 2167 (1990)
73. Gimona, M., I. Kaverina, G. P. Resch, E. Vignal, G. Burgstaller: Calponin repeats regulate actin filament stability and formation of podosomes in smooth muscle cells. Mol Biol Cell 14, 2482 (2003)
74. Linder, S., D. Nelson, M. Weiss, M. Aepfelbacher: Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci USA 96, 9648 (1999)
75. Linder, S., H. Higgs, K. Hufner, K. Schwarz, U. Pannicke, M. Aepfelbacher: The polarization defect of Wiskott-Aldrich syndrome macrophages is linked to dislocalization of the Arp2/3 complex. J Immunol 165, 221 (2000)
76. Zicha, D., W. E. Allen, P. M. Brickell, C. Kinnon, G. A. Dunn, G. E. Jones, A. J. Thrasher: Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome. Br J Haematol 101, 659 (1998)
77. Lakkakorpi, P., J. Tuukkanen, T. Hentunen, K. Jarvelin, K. Vaananen: Organization of osteoclast microfilaments during the attachment to bone surface in vitro. J Bone Miner Res 4, 817 (1989)
78. Kanehisa, J., T. Yamanaka, S. Doi, K. Turksen, J. N. Heersche, J. E. Aubin, H. Takeuchi: A band of F-actin containing podosomes is involved in bone resorption by osteoclasts. Bone 11, 287 (1990)
79. Teti, A., S. Colucci, M. Grano, L. Argentino, A. Zambonin Zallone: Protein kinase C affects microfilaments, bone resorption, and [Ca2+]o sensing in cultured osteoclasts. Am J Physiol 263, C130 (1992)
80. Duong, L. T., P. T. Lakkakorpi, I. Nakamura, M. Machwate, R. M. Nagy, G. A. Rodan: PYK2 in osteoclasts is an adhesion kinase, localized in the sealing zone, activated by ligation of alpha(v)beta3 integrin, and phosphorylated by src kinase. J Clin Invest 102, 881 (1998)
81. McHugh, K. P., K. Hodivala-Dilke, M. H. Zheng, N. Namba, J. Lam, D. Novack, X. Feng, F. P. Ross, R. O. Hynes, S. L. Teitelbaum: Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 105, 433 (2000)
82. Pfaff, M., P. Jurdic: Podosomes in osteoclast-like cells: structural analysis and cooperative roles of paxillin, proline-rich tyrosine kinase 2 (Pyk2) and integrin alphaVbeta3. J Cell Sci 114, 2775 (2001)
83. Chen, W. T: Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 251, 167 (1989)
84. Basbaum, C. B., Z. Werb: Focalized proteolysis: spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr Opin Cell Biol 8, 731 (1996)
85. Mizutani, K., H. Miki, H. He, H. Maruta, T. Takenawa: Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res 62, 669 (2002)