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Cellular Protrusions - Lamellipodia, Filopodia, Invadopodia and Podosomes - and their Roles in Progression of Orofacial Tumours: Current Understanding

  • Alblazi, Kamila Mohamed Om (Department of Oro-Maxillofacial Surgical and Medical Sciences, Faculty of Dentistry, University of Malaya) ;
  • Siar, Chong Huat (Department of Oro-Maxillofacial Surgical and Medical Sciences, Faculty of Dentistry, University of Malaya)
  • Published : 2015.04.03

Abstract

Background: Protrusive structures formed by migrating and invading cells are termed lamellipodia, filopodia, invadopodia and podosomes. Lamellipodia and filopodia appear on the leading edges of migrating cells and function to command the direction of the migrating cells. Invadopodia and podosomes are special F-actin-rich matrix-degrading structures that arise on the ventral surface of the cell membrane. Invadopodia are found in a variety of carcinomatous cells including squamous cell carcinoma of head and neck region whereas podosomes are found in normal highly motile cells of mesenchymal and myelomonocytic lineage. Invadopodia-associated protein markers consisted of 129 proteins belonging to different functional classes including WASP, NWASP, cortactin, Src kinase, Arp 2/3 complex, MT1-MMP and F-actin. To date, our current understanding on the role(s) of these regulators of actin dynamics in tumors of the orofacial region indicates that upregulation of these proteins promotes invasion and metastasis in oral squamous cell carcinoma, is associated with poor/worst prognostic outcome in laryngeal cancers, contributes to the persistent growth and metastasis characteristics of salivary gland adenoid cystic carcinoma, is a significant predictor of increased cancer risk in oral mucosal premalignant lesions and enhances local invasiveness in jawbone ameloblastomas.

Keywords

References

  1. Aihara T, Oda, T (2013). Cooperative and non-cooperative conformational changes of F-actin induced by cofilin. Biochem Biophys Res Commun, 435, 229-33. https://doi.org/10.1016/j.bbrc.2013.04.076
  2. Ambrosio EP, Rosa FE, Domingues MA, et al (2011) Cortactin is associated with perineural invasion in the deep invasive front area of laryngeal carcinomas. Hum Pathol, 42, 1221-9. https://doi.org/10.1016/j.humpath.2010.05.030
  3. Ammer AG, Weed SA (2008). Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton, 65, 687-707. https://doi.org/10.1002/cm.20296
  4. 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, 3034-43. https://doi.org/10.1158/0008-5472.CAN-05-2177
  5. Ayala I, Baldassarre M, Giacchetti G, et al (2008). Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci, 121, 369-78. https://doi.org/10.1242/jcs.008037
  6. Baldwin GS, Lio DS-S, Ferrand A, et al (2014). Activation of Src family tyrosine kinases by ferric ions. Biochim Biophys Acta, 1844, 487-96. https://doi.org/10.1016/j.bbapap.2013.12.004
  7. Bryce NS, Clark ES, Leysath JML, et al (2005). Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol, 15, 1276-85. https://doi.org/10.1016/j.cub.2005.06.043
  8. Buccione R, Caldieri G, Avala I (2009). Invadopodia: specialized tumor cells structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev, 28, 137-49. https://doi.org/10.1007/s10555-008-9176-1
  9. Buccione R, Orth JD, McNiven, MA (2004). Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol, 5, 647-57. https://doi.org/10.1038/nrm1436
  10. Buday L, Downward J (2007). Roles of cortactin in tumor pathogenesis. Biochim Biophys Acta, 1775, 263-73.
  11. Condeelis J, Segall, JE (2003). Intravital imaging of cell movement in tumours. Nat Rev Cancer, 3, 921-30. https://doi.org/10.1038/nrc1231
  12. David-Pfeuty T, Singer SJ (1980). Altered distributions of the cytoskeletal proteins vinculin and alpha-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proc Natl Acad Sci USA, 77, 6687-91. https://doi.org/10.1073/pnas.77.11.6687
  13. de Vicente JC, Rosado P, Lequerica-Fernandez P, et al (2013). Focal adhesion kinase overexpression: correlation with lymph node metastasis and shorter survival in oral squamous cell carcinoma. Head Neck, 35, 826-30. https://doi.org/10.1002/hed.23038
  14. Destaing O, Block MR, Planus E, Albiges-Rizo C (2011). Invadosome regulation by adhesion signaling. Curr Opin Cell Biol, 23, 597-606. https://doi.org/10.1016/j.ceb.2011.04.002
  15. Eckert MA, Yang J (2011). Targeting invadopodia to block breast cancer metastasis. Oncotarget, 2, 562-8 https://doi.org/10.18632/oncotarget.301
  16. Elsberger B (2014). Translational evidence on the role of Src kinase and activated Src kinase in invasive breast cancer. Crit Rev Oncol Hematol, 89, 343-51. https://doi.org/10.1016/j.critrevonc.2013.12.009
  17. Gagat M, Grzanka D, Izdebska M, et al (2014). Tropomyosin-1 protects endothelial cell-cell junctions against cigarette smoke extract through F-actin stabilization in EA.hy926 cell line. Acta Histochem, 116, 606-18. https://doi.org/10.1016/j.acthis.2013.11.013
  18. Garcia E, Jonesb GE, Macheskyc LM, Antona IM (2012). WIP: WASP-interacting proteins at invadopodia and podosomes. Eur J Cell Biol, 9, 869-77.
  19. Genot E, Gligorijevic B (2014). Invadosomes in their natural habitat. Eur J Cell Biol, 93, 367-79. https://doi.org/10.1016/j.ejcb.2014.10.002
  20. Greer RO Jr, Said S, Shroyer KR, Marileila VG, Weed SA (2007). Overexpression of cyclin D1 and cortactin is primarily independent of gene amplification in salivary gland adenoid cystic carcinoma. Oral Oncol, 43, 735-41. https://doi.org/10.1016/j.oraloncology.2006.09.007
  21. Grigera PR, Ma L, Borgman CA, et al (2012). Mass spectrometric analysis identifies a cortactin-RCC2/TD60 interaction in mitotic cells. J Proteomics, 75, 2153-9. https://doi.org/10.1016/j.jprot.2012.01.012
  22. Hauck CR, Hsia DA, Ilic D, Schlaepfer DD (2002) v-Src SH3-enhanced interaction with focal adhesion kinase at beta 1 integrin-containing invadopodia promotes cell invasion. J Biol Chem, 277, 12487-90. https://doi.org/10.1074/jbc.C100760200
  23. Hong BH, Wu CH, Yeh CT, Yen GC (2013). Invadopodia-associated proteins blockade as a novel mechanism for 6-shogaol and pterostilbene to reduce breast cancer cell motility and invasion. Mol Nutr Food Res, 57, 886-95. https://doi.org/10.1002/mnfr.201200715
  24. Hwang YS, Park KK, Chung WY (2012). Invadopodia formation in oral squamous cell carcinoma: the role of epidermal growth factor receptor signalling. Arch Oral Biol, 57, 335-43 https://doi.org/10.1016/j.archoralbio.2011.08.019
  25. Isaac BM, Ishihara D, Nusblat LM, et al (2010). N-WASP has the ability to compensate for the loss of WASP in macrophage podosome formation and chemotaxis. Exp Cell Res, 316, 3406-16. https://doi.org/10.1016/j.yexcr.2010.06.011
  26. Jimenez L, Sharma, VP, Lim J, et al (2014). MicroRNA-375 impairs head and neck squamous cell carcinoma invasion by suppressing invadopodia activity. Cancer Res, 74, 1452. https://doi.org/10.1158/0008-5472.CAN-13-2171
  27. Linder S (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol, 17, 107-17. https://doi.org/10.1016/j.tcb.2007.01.002
  28. Murphy DA, Courtneidge SA (2011). The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol, 12, 413-26. https://doi.org/10.1038/nrm3141
  29. Nascimento CF, Gama-De-Souza LN, Freitas VM, Jaeger RG (2010). Role of MMP9 on invadopodia formation in cells from adenoid cystic carcinoma. Study by laser scanning confocal microscopy. Microsc Res Tech, 273, 99-108.
  30. Nakane K, Fujita Y, Terazawa R, et al (2012). Inhibition of cortactin and SIRT1 expression attenuates migration and invasion of prostate cancer DU145 cells. Int J Urol, 19, 71-9. https://doi.org/10.1111/j.1442-2042.2011.02888.x
  31. Noh SJ, Baek HA, Park HS, et al (2013). Expression of SIRT1 and cortactin is associated with progression of non-small cell lung cancer. Pathol Res Pract, 209, 365-70. https://doi.org/10.1016/j.prp.2013.03.011
  32. Pinheiro JJV, Nascimento CF, Freitas VM, et al (2011). Invadopodia proteins, cortactin and membrane type I matrix metalloproteinase (MT1-MMP) are expressed in ameloblastoma. Histopathol, 59, 1261-79.
  33. Saltel F, Daubon T, Juin A, et al (2011). Invadosomes: intriguing structures with promise. Eur J Cell Biol, 90, 100-7. https://doi.org/10.1016/j.ejcb.2010.05.011
  34. Seano G, Daubon T, Genot E, Primo L (2014). Podosomes as novel players in endothelial biology. Eur J Cell Biol, 93, 405-12. https://doi.org/10.1016/j.ejcb.2014.07.009
  35. Seltana A, Guezguez A, Lepage, M, Basora, N, Beaulieu, J-F (2013). Src family kinase inhibitor PP2 accelerates differentiation in human intestinal epithelial cells. Biochem Biophys Res Commun, 430, 1195-200. https://doi.org/10.1016/j.bbrc.2012.12.085
  36. Shields MA, Krantz SB, Bentrem DJ, Dangi-Garimella S, Munshi HG (2012). Interplay between ${\beta}1$-integrin and Rho signaling regulates differential scattering and motility of pancreatic cancer cells by snail and Slug proteins. J Biol Chem, 287, 6218-29. https://doi.org/10.1074/jbc.M111.308940
  37. Shvetsov A, Berkane E, Chereau D, Dominguez R, Reisler E (2009). The actin-binding domain of cortactin is dynamic and unstructured and affects lateral and longitudinal contacts in F-actin. Cell Motil Cytoskeleton, 66, 90-8. https://doi.org/10.1002/cm.20328
  38. Sibony-Benyamini H, Gil-Henn H (2012). Invadopodia: The leading force. Eur J Cell Biol, 91, 896-901. https://doi.org/10.1016/j.ejcb.2012.04.001
  39. Spinardi L, Rietdorf J, Nitsch L, et al (2004). A dynamic podosome-like structure of epithelial cells. Exp Cell Res, 295, 360-74. https://doi.org/10.1016/j.yexcr.2004.01.007
  40. Stevenson RP, Veltman D, Machesky LM (2012). Actin-bundling proteins in cancer progression at a glance. J Cell Sci, 125, 1073-9. https://doi.org/10.1242/jcs.093799
  41. Stylli SS, Kaye, AH, Lock P (2008). Invadopodia: At the cutting edge of tumour invasion. J Clin Neurosci, 15, 725-37. https://doi.org/10.1016/j.jocn.2008.03.003
  42. Suraneni P, Rubinstein B, Unruh JR, et al (2012). The Arp2/3 complex is required for lamellipodia extension and directional fibroblast cell migration. J Cell Biol, 197, 239-51. https://doi.org/10.1083/jcb.201112113
  43. Weaver AM (2008). Cortactin in tumor invasiveness. Cancer Lett, 265, 157-66. https://doi.org/10.1016/j.canlet.2008.02.066
  44. Weaver AM, Heuser JE, Karginov AV, et al (2002). Interaction of cortactin and N-WASP with Arp2/3 complex. Curr Biol, 12, 1270-8. https://doi.org/10.1016/S0960-9822(02)01035-7
  45. Webb BA, Eves R, Mak AS (2006). Cortactin regulates podosome formation: roles of the protein interaction domains. Exp Cell Res, 312, 760-9. https://doi.org/10.1016/j.yexcr.2005.11.032
  46. Yamada S, Yanamoto S, Kawasaki G, Mizuno A, Nemoto TK (2010). Overexpression of cortactin increases invasion potential in oral squamous cell carcinoma. Pathol Oncol Res, 16, 523-31. https://doi.org/10.1007/s12253-009-9245-y
  47. Yamaguchi H, Condeelis, J (2007). Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta, 1773, 642-52. https://doi.org/10.1016/j.bbamcr.2006.07.001

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