Invadopodia, regulation, and assembly in cancer cell invasion

Cell Communication and Adhesion

Volumn 21, Issue 4, 2014, Pages 207-212

  Saykali, Bechara A ^a   El Sibai, Mirvat ^a  

^a LEBANESE AMERICAN UNIVERSITY   (Lebanon)

Author keywords

3D motility; Cancer motility; Invadopodia; Podosome; Signaling

Indexed keywords

ACTIN; FOCAL ADHESION KINASE; PHOSPHATIDYLINOSITOL 3 KINASE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; CANCER CELL; CELL INVASION; CELL MOTILITY; CELL MOTION; CELL STRUCTURE; DISSOLUTION; FOCAL ADHESION; HUMAN; INVADOPODIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TURNOVER TIME; ACTIN CYTOSKELETON; CELL ADHESION; CELL MEMBRANE STRUCTURES; CELL MOVEMENT; CELL POLARITY; HUMANS; METABOLISM; NEOPLASM INVASIVENESS; NEOPLASMS; PATHOLOGY; PHYSIOLOGY;

ACTIN CYTOSKELETON; CELL ADHESION; CELL MEMBRANE STRUCTURES; CELL MOVEMENT; CELL POLARITY; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84904989024     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.3109/15419061.2014.923845     Document Type: Review

References (67)

1. Abram C , Seals DF , Pass I , Salinsky D , Maurer L , Roth TM , Courtneidge SA (2003). The adaptor protein fi sh associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J Biol Chem. 278 : 16844-16851. (Pubitemid 36799554)
2. Baldassarre M , Ayala I , Beznoussenko G , Giacchetti G , Machesky LM , Luini A , Buccione R (2006). Actin dynamics at sites of extracellular matrix degradation. Eur J Cell Biol. 85 : 1217-1231. (Pubitemid 44780616)
3. Bear J , Gertler F (2009). Ena/VASP: towards resolving a pointed controversy at the barbed end. J Cell Sci. 122 : 1947-1953.
4. Block M , Badowski C , Millon-Fremillon A , Bouvard D , Bouin AP , Faurobert E , Gerber-Scokaert D , Planus E , Albiges-Rizo C (2008). Podosome-type adhesions and focal adhesions, so alike yet so different. Eur J Cell Biol. 87 : 491-506.
5. 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 : 4440-4449. (Pubitemid 29396652)
6. Breitsprecher D , Kiesewetter AK , Linkner J , Vinzenz M , Stradal TE , Small JV , Curth U , Dickinson RB , Faix J (2011). Molecular mechanism of Ena/VASP-mediated actin-fi lament elongation. EMBO J. 30 : 456-467.
7. Buschman MD , Bromann PA , Cejudo-Martin P , Wen F , Pass I , Courtneidge SA (2009). The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol Biol Cell. 20 : 1302-1311.
8. Calle Y , Carragher N , Thrasher A , Jones G (2006). Inhibition of calpain stabilises podosomes and impairs dendritic cell motility. J Cell Sci. 119 : 2375-2385. (Pubitemid 43960326)
9. Campellone K , Welch M (2010). A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol. 11 : 237-251.
10. Cantley LC (2002). The phosphoinositide 3-kinase pathway. Science. 296 : 1655-1657. (Pubitemid 34579158)
11. Chan K , Cortesio C , Huttenlocher A (2009). FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J Cell Biol. 185 : 357-370.
12. Chen W (1989). Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool. 251 : 167-185. (Pubitemid 19216054)
13. Chen W-T , Chen J-M , Parsons S , Parsons T (1985). Local degradation of fi bronectin at sites of expression of the transforming gene product pp60src. Nature. 316 : 156-158. (Pubitemid 15073680)
14. Clark ES , Weaver AM (2008). new role for cortactin in invadopodia: regulation of protease secretion. Cell Biol. 87 : 581-590.
15. Clark ES , Whigham AS , Yarbrough WG , Weaver AM (2007). Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67 : 4227-4435.
16. Courtneidge S , Azucena EF , Pass I , Seals DF , Tesfay L (2005). The SRC substrate Tks5, podosomes (invadopodia), and cancer cell invasion. Cold Spring Harb Symp Quant Biol. 70 : 167-171. (Pubitemid 44124868)
17. DesMarais V , Yamaguchi H , Oser M , Soon L , Mouneimne G , Sarmiento C , Eddy R , Condeelis J (2009). N-WASP and cortactin are involved in invadopodium-dependent chemotaxis to EGF in breast tumor cells. Cell Motil Cytoskeleton. 66 : 303-316.
18. Destaing O , Sanjay A , Itzstein C , Horne WC , Toomre D , De Camilli P , Baron R (2008). The tyrosine kinase activity of cSrc regulates actin dynamics and organization of podosomes in osteoclasts. Mol Biol Cell. 19 : 394-404. (Pubitemid 351186162)
19. El-Sibai M , Pertz O , Pang H , Yip SC , Lorenz M , Symons M , Condeelis JS , Hahn KM , Backer JM (2008). RhoA/ROCKmediated switching between Cdc42-and Rac1-dependent protrusion in MTLn3 carcinoma cells. Exp Cell Res. 314 : 1540-52.
20. Ferguson G , Milne L , Kulkarni S , Sasaki T , Walker S , Andrews S , Crabbe T , Finan P , Jones G , Jackson S , Camps M , Rommel C , Wymann M , Hirsch E , Hawkins P , Stephens L (2007). PI(3)Kgamma has an important context-dependent role in neutrophil chemokinesis. Nat Cell Biol. 9 : 86-91. (Pubitemid 46024201)
21. Fruman A , Meyers RE , Cantley LC (1998). Phosphoinositide kinases. Annu Rev Biochem. 67 : 481-507. (Pubitemid 28411136)
22. Gatesman A. , Walker VG , Baisden JM , Weed SA , Flynn DC (2004). Protein kinase Cactivates cSrc and induces podosome formation via AFAP110. Mol Cell Biol. 24 : 7578-7597. (Pubitemid 39121485)
23. Gianni D , Diaz B , Taulet N , Fowler B , Courtneidge SA , Bokoch GM (2009). Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal. 2 : ra54.
24. Gimona M , Buccione R , Courtneidge S , Linder S (2008). Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol. 20 : 235-241.
25. Hall A (2009). The cytoskeleton and cancer. Cancer Metastasis Rev. 28 : 5-14.
26. Hoshino D , Jourquin J , Emmons SW , Miller T , Goldgof M , Costello K , Tyson DR , Brown B , Lu Y , Prasad NK , Zhang B , Mills GB , Yarbrough WG , Quaranta V , Seiki M , Weaver AM (2012). Network analysis of the focal adhesion to invadopodia transition identifi es a PI3K-PKCa invasive signaling axis. Sci Signal. 5 : ra66.
27. Iijima M , Huang Y , Devreotes P (2002). Temporal and spatial regulation of chemotaxis. Dev Cell. 3 : 469-478. (Pubitemid 35252257)
28. Insall R, Machesky L (2009). Actin dynamics at the leading edge: from simple machinery to complex networks. Dev Cell. 17 : 310-322.
29. Kamimura Y , Xiong Y , Iglesias PA , Hoeller O , Bolourani P , Devreotes PN (2008). PIP3-independent activation of TorC2 and PKB at the cell ' s leading edge mediates chemotaxis. Curr Biol. 18 : 1034-1043.
30. Lambrechts A , Van Troys M , Ampe C (2004). The actin cytoskelyon in normal and pathological cell motility. Int J Biochem Cell Biol. 36 : 1890-1909. (Pubitemid 38760020)
31. Lapetina S , Mader CC , Machida K , Mayer BJ , Koleske AJ (2009). Arg interacts with cortactin to promote adhesion-dependent cell edge protrusion. J Cell Biol. 185 : 503-519.
32. Lock P , Abrahm LC , Gibson T , Courtneidge S (1998). A new method for isolating tyrosine kinase substrates used to identify fi sh, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 17 : 4346-4357. (Pubitemid 28362625)
33. Machesky L , Li A (2010). Fascin: Invasive fi lopodia promoting metastasis. Commun Integr Biol. 3 : 263-270.
34. Magalhaes MA, Larson DR, Mader CC, Bravo-Cordero JJ, Gil-Henn H , Oser M , Chen X , Koleske AJ , Condeelis J (2011). Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J Cell Biol. 195 : 903-920.
35. McNiven MA (2013). Breaking away: matrix remodeling from the leading edge. Trends Cell Biol. 23 : 16-21.
36. Millius A , Dandekar S , Houk A , Weiner O (2009). Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. Curr Biol. 19 : 253-259.
37. Mullins R , Heuser J , Pollard T (1998). The interaction of Arp2/3 complex with actin: nucleation, high affi nity pointed end capping, and formation of branching networks of fi laments. Proc Natl Acad Sci USA. 95 : 6181-6186. (Pubitemid 28248985)
38. Murphy D, Courtneidge S (2011). The ' ins' and ' outs' of podosomes and invadopodia: characteristics, formation and function. Nature. 12 : 413-426.
39. Oikawa T , Itoh T , Takenawa T (2008). Sequential signals toward podosome formation in NIH-src cells. J Cell Biol. 182 : 157-169. (Pubitemid 352008629)
40. Olson M , Sahai E (2009). The actin cytoskeleton in cancer cell motility. Clin Exp Metastasis. 26 : 273-287.
41. Oser M , Dovas A , Cox D , Condeelis J (2011). Nck1 and Grb2 localization patterns can distinguish invadopodia from podosomes. Eur J Cell Biol. 90 : 181-188.
42. Oser M , Mader CC , Gil-Henn H , Magalhaes M , Bravo-Cordero JJ, Koleske AJ, Condeelis J (2010). Specifi c tyrosine phosphorylation sites on cortactin regulate Nck1-dependent actin polymerization in invadopodia. J Cell Sci. 123: 3662-3673.
43. Parker SB , Sukumar S (2003). Distant metastasis in breast cancer. Cancer Biol Ther. 2 : 14-21.
44. Pertz O , Hodgson L , Klemke RL , Hahn KM (2006). Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440 : 1069-72.
45. Pollard TD , Borisy GG (2003). Cellular motility driven by assembly and dissassembly of actin fi laments. Cell. 112 : 453-465. (Pubitemid 36263079)
46. 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)
47. Qin Y , Fu M, Takahashi M, Iwanami A, Kuga D, Rao RG (2014). Epithelial Membrane Protein-2 (EMP2) Activates Src and is a Novel Therapeutic Target for GBM. J Biol Chem. 00 : 1-10 (accessed 6 January 2013).
48. Ricono JM , Huang M , Barnes LA , Lau SK , Weis SM , Schlaepfer DD , Hanks SK , Cheresh DA (2009). Specifi c cross-talk between epidermal growth factor receptor and integrin alphavbeta5 promotes carcinoma cell invasion and metastasis. Cancer Res. 69 : 1383-1391.
49. Ridley AJ (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle traffi cking. Trends Cell Biol. 16: 522-29. (Pubitemid 44444995)
50. Ridley A (2011). Life at the leading edge. Cell. 145 : 1012-1023.
51. Schachtner H , Calaminus S , Thomas S , Machesky L (2013). Podosomes in adhesion, migration, mechanosensing and matrix remodeling. Cell Motil Cytoskeleton. 70 : 572-589.
52. Schneider I , Haugh J (2006). Mechanisms of gradient sensing and chemotaxis: conserved pathways, diverse regulation. Cell Cycle. 5 : 1130-1134. (Pubitemid 43845368)
53. Seals DF , Azucena EF Jr , Pass I , Tesfay L , Gordon R , Woodrow M , Resau JH , Courtneidge SA (2005). The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell. 7 : 155-165. (Pubitemid 40248341)
54. Sharma VP , Eddy R , Entenberg D , Kai M , Gertler FB , Condeelis J (2013). Tks5 and SHIP2 Regulate Invadopodium Maturation, but Not Initiation, in Breast Carcinoma Cells. Curr Biol. 23 : 2079-2089.
55. Singer S , David-Pfeuty T (1980). Altered distribution of the cytoskeleton proteins vinculin and alfa-actinin in cultured fi broblasts transformed by Rous sarcoma virus. Proc Natl Acad Sci USA. 77 : 6687-6691. (Pubitemid 11163465)
56. Small V (1994). Lamellipodia architecture: Actin fi lament turnover and the lateral fl ow of actin fi lamens durings motility. Semin Cell Biol. 5 : 157-163.
57. Stylli S , Stacey TT , Verhagen AM , Xu SS , Pass I , Courtneidge SA , Lock P (2009). Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation. J Cell Sci. 122 : 2727-2740.
58. Takenawa T , Suetsugu S (2007). The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol. 8 : 37-48. (Pubitemid 46012013)
59. Tarone G , Cirillo D , Giancotti FG , Comoglio PM , Marchisio PC (1985). Rous sarcoma virus-transformed fi broblasts adhere primarily at discrete protrusions of the ventral membrane called podosomes. Exp Cell Res. 159 : 141-157. (Pubitemid 16247561)
60. Tatin F. , Varon C. , Genot E , Moreau V (2006). A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci. 119 : 769-781.
61. Tomar A , Schlaepfer DD (2009). Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol. 21 : 676-683.
62. Vitale S. , Avizienyte E. , Brunton V , Frame M (2008). Focal adhesion kinase is not required for Src-induced formation of invadopodia in KM12C colon cancer cells and can interfere with their assembly. Eur J Cell Biol. 87 : 569-579.
63. Wang X , He L , Wu YI , Hahn KM , Montell DJ (2010). ight-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol. 12 : 591-597.
64. Wang Y , McNiven MA (2012). Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J Cell Biol. 196 : 375-385.
65. Wolf K , Friedl P (2009). Mapping proteolytic cancer cellextracellular matrix interfaces. Clin Exp Metastasis. 26 : 289-298.
66. Yamaguchi H , Yoshida S , Muroi E , Yoshida N , Kawamura M , Kouchi Z , Nakamura Y , Sakai R , Fukami K (2011). Phosphoinositide 3-kinase signaling pathway mediated by p110a regulates invadopodia formation. J Cell Biol. 193 : 1275-1288.
67. Yang C , Czech L , Gerboth S , Kojima S , Scita G , Svitkina T (2007). Novel roles of formin mDia2 in lamellipodia and fi lopodia formation in motile cells. PLoS Biol. 5 : 2624-2645. (Pubitemid 350276935)