N-WASP and cortactin are involved in invadopodium-dependent chemotaxis to EGF in breast tumor cells

Cell Motility and the Cytoskeleton

Volumn 66, Issue 6, 2009, Pages 303-316

  DesMarais, Vera ^a   Yamaguchi, Hideki ^b,c   Oser, Matthew ^a   Soon, Lilian ^d   Mouneimne, Ghassan ^e   Sarmiento, Corina ^a   Eddy, Robert ^a   Condeelis, John ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF SYDNEY   (Australia)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Actin; Chemotaxis; Cortactin; Invadopodium; N WASP

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; COFILIN; CORTACTIN; EPIDERMAL GROWTH FACTOR; F ACTIN; GLASS; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; BREAST METASTASIS; BREAST TUMOR; CANCER INFILTRATION; CANCER INHIBITION; CANCER INVASION; CELL MOTILITY; CELLS AND CELL COMPONENTS; CHEMOTAXIS; INNATE IMMUNITY; INVADOPODIUM; LAMELLIPODIUM; MACROPHAGE; MICROSCOPY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; PSEUDOPODIUM; RAT;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; CORTACTIN; DESTRIN; EPIDERMAL GROWTH FACTOR; MICROTUBULES; PSEUDOPODIA; RATS; RNA, SMALL INTERFERING; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 66749140937     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20361     Document Type: Article

References (47)

1. Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, Guelcher SA, Weaver AM. 2008. Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18(17):1295-1299.
2. Araki N, Swanson JA. 1998. Labeling of endocytic vesicles using fluorescent probes for fluid-phase endocytosis. In: Celis JE, editor. Cell Biology: A Laboratory Handbook, vol 2 (second edition). Academic Press.
3. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. 2006. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66(6):3034-3043.
4. Ayala I, Baldassarre M, Giacchetti G, Caldieri G, Tete S, Luini A, Buccione R. 2008. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci 121 (Part 3):369-378.
5. Bailly M, Condeelis JS, Segall JE. 1998a. Chemoattractant-induced lamellipod extension. Microsc Res Tech 43(5):433-443. (Pubitemid 28565790)
6. Bailly M, Yan L, Whitesides GM, Condeelis JS, Segall JE. 1998b. Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp Cell Res 241(2):285-299. (Pubitemid 28366554)
7. Banzai Y, Miki H, Yamaguchi H, Takenawa T. 2000. Essential role of neural Wiskott-Aldrich syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. J Biol Chem 275(16):11987-11992. (Pubitemid 30237771)
8. Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, Wehland J, Rottner K. 2005. N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118 (Part 14):3103-3115. (Pubitemid 41149914)
9. Bowden ET, Barth M, Thomas D, Glazer RI, Mueller SC. 1999. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 18(31):4440-4449. (Pubitemid 29396652)
10. Bowden ET, Coopman PJ, Mueller SC. 2001. Invadopodia: Unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol 63:613-627. (Pubitemid 33797825)
11. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, Weaver AM. 2005. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 15(14):1276-1285. (Pubitemid 41026593)
12. Buccione R, Orth JD, McNiven MA. 2004. Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol 5(8):647-657. (Pubitemid 39025065)
13. Calle Y, Burns S, Thrasher AJ, Jones GE. 2006. The leukocyte podosome. Eur J Cell Biol 85(3-4):151-157.
14. Chan AY, Bailly M, Zebda N, Segall JE, Condeelis JS. 2000. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol 148(3):531-542.
15. Chen WT. 1989. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 251(2):167-185. (Pubitemid 19216054)
16. Condeelis J, Pollard JW. 2006. Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell 124(2):263-266. (Pubitemid 43121975)
17. 2+-dependent myosin II activation is required for uropod retraction during neutrophil migration. J Cell Sci 113:1287-1298.
18. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304(5671):743-746. (Pubitemid 38560882)
19. Gomes ER, Jani S, Gundersen GG. 2005. Nuclear movement regulated by Cdc42. MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121(3):451-463.
20. Kempiak SJ, Yamaguchi H, Sarmiento C, Sidani M, Ghosh M, Eddy RJ, Desmarais V, Way M, Condeelis J, Segall JE. 2005. A neural Wiskott-Aldrich Syndrome protein-mediated pathway for localized activation of actin polymerization that is regulated by cortactin. J Biol Chem 280(7):5836-5842. (Pubitemid 40280065)
21. Kopp P, Lammers R, Aepfelbacher M, Woehlke G, Rudel T, Machuy N, Steffen W, Linder S. 2006. The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol Biol Cell 17(6):2811-2823. (Pubitemid 43825516)
22. Le Clainche CCM. 2008. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 88(2):489-513.
23. Linder S. 2007. The matrix corroded: Podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17(3):107-117. (Pubitemid 46341826)
24. Linder S, Aepfelbacher M. 2003. Podosomes: Adhesion hot-spots of invasive cells. Trends Cell Biol 13(7):376-385. (Pubitemid 36776715)
25. Linder S, Kopp P. 2005. Podosomes at a glance. J Cell Sci 118 (Part 10):2079-2082. (Pubitemid 40872830)
26. Linder S, Nelson D, Weiss M, Aepfelbacher M. 1999. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc Natl Acad Sci U S A 96(17):9648-9653. (Pubitemid 29398786)
27. Linder S, Hufner K, Wintergerst U, Aepfelbacher M. 2000. Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J Cell Sci 113 (Part 23):4165-4176. (Pubitemid 32000684)
28. Lommel S, Benesch S, Rottner K, Franz T, Wehland J, Kuhn R. 2001. Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep 2(9):850-857. (Pubitemid 32982755)
29. Lorenz M, DesMarais V, Macaluso F, Singer RH, Condeelis J. 2004a. Measurement of barbed ends, actin polymerization, and motility in live carcinoma cells after growth factor stimulation. Cell Motil Cytoskeleton 57(4):207-217. (Pubitemid 38419153)
30. Lorenz M, Yamaguchi H, Wang Y, Singer RH, Condeelis J. 2004b. Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Curr Biol 14(8):697-703. (Pubitemid 38503607)
31. Mattila PK, Lappalainen P. 2008. Filopodia: Molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9(6):446-454.
32. Miki H, Miura K, Takenawa T. 1996. N-WASP, a novel actin-depolymerizing protein, regulates the cortical cytoskeletal rearrangement in a PIP2-dependent manner downstream of tyrosine kinases. Embo J 15(19):5326-5335. (Pubitemid 26336215)
33. Mizutani K, Miki H, He H, Maruta H, Takenawa T. 2002. Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res 62(3):669-674. (Pubitemid 34126939)
34. Mouneimne G, Soon L, DesMarais V, Sidani M, Song X, Yip SC, Ghosh M, Eddy R, Backer JM, Condeelis J. 2004. Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J Cell Biol 166(5):697-708. (Pubitemid 39181007)
35. Mouneimne G, DesMarais V, Sidani M, Scemes E, Wang W, Song X, Eddy R, Condeelis J. 2006. Spatial and temporal control of cofilin activity is required for directional sensing in carcinoma cells. Curr Biol 16(5):2193-2205. (Pubitemid 44739276)
36. Mueller SC, Ghersi G, Akiyama SK, Sang QX, Howard L, Pineiro-Sanchez M, Nakahara H, Yeh Y, Chen WT. 1999. A novel protease-docking function of integrin at invadopodia. J Biol Chem 274(35):24947-24952. (Pubitemid 129529386)
37. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M, Desmarais V, Holman HA, Kitchen S, Backer JM, Alberts A, Condeelis J. 2008. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 180(6):1245-1260.
38. Segall JE, Tyerech S, Boselli L, Masseling S, Helft J, Chan A, Jones J, Condeelis J. 1996. EGF stimulates lamellipod extension in metastatic mammary adenocarcinoma cells by an actin-dependent mechanism. Clin Exp Metastasis 14(1):61-72. (Pubitemid 26008960)
39. Sidani M, Wessels D, Mouneimne G, Ghosh M, Goswami S, Sarmiento C, Wang W, Kuhl S, El-Sibai M, Backer JM, Eddy R, Soll D, Condeelis J. 2007. Cofilin determines the migration behavior and turning frequency of metastatic cancer cells. J Cell Biol 179(4):777-791. (Pubitemid 350146261)
40. Snapper SB, Takeshima F, Anton I, Liu CH, Thomas SM, Nguyen D, Dudley D, Fraser H, Purich D, Lopez-Ilasaca M, Klein C, Davidson L, Bronson R, Mulligan RC, Southwick F, Geha R, Goldberg MB, Rosen FS, Hartwig JH, Alt FW. 2001. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat Cell Biol 3(10):897-904. (Pubitemid 32952254)
41. Soon L, Mouneimne G, Segall J, Wyckoff J, Condeelis J. 2005. Description and characterization of a chamber for viewing and quantifying cancer cell chemotaxis. Cell Motil Cytoskeleton 62(1):27-34. (Pubitemid 41254608)
42. Uruno T, Liu J, Li Y, Smith N, Zhan X. 2003. Sequential interaction of actin-related proteins 2 and 3 (Arp2/3) complex with neural Wiscott-Aldrich syndrome protein (N-WASP) and cortactin during branched actin filament network formation. J Biol Chem 278(28):26086-26093. (Pubitemid 36835377)
43. van Rheenen J, Song X, van Roosmalen W, Cammer M, Chen X, Desmarais V, Yip SC, Backer JM, Eddy RJ, Condeelis JS. 2007. EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol 179(6):1247-1259. (Pubitemid 350277742)
44. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, Cooper JA. 2001. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11(5):370-374. (Pubitemid 32200742)
45. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, Segall J, Eddy R, Miki H, Takenawa T, Condeelis J. 2005. Molecular mechanisms of invadopodium formation: The role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168(3):441-452. (Pubitemid 40205066)
46. Yu N, Atienza JM, Bernard J, Blanc S, Zhu J, Wang X, Xu X, Abassi YA. 2006. Real-time monitoring of morphological changes in living cells by electronic cell sensor arrays: An approach to study G protein-coupled receptors. Anal Chem 78(1):35-43. (Pubitemid 43050137)
47. Zicha D, Allen WE, Brickell PM, Kinnon C, Dunn GA, Jones GE, Thrasher AJ. 1998. Chemotaxis of macrophages is abolished in the Wiskott-Aldrich syndrome. Br J Haematol 101(4):659-665. (Pubitemid 28308514)