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Peláez R, Pariente A, Pérez-Sala Á, et al. Integrins: Moonlighting Proteins in Invadosome Formation. Cancers (Basel). 2019;11(5)doi: 10.3390/cancers11050615.
Peláez, R., Pariente, A., Pérez-Sala, �. �., & Larrayoz, I. M. (2019). Integrins: Moonlighting Proteins in Invadosome Formation. Cancers, 11(5), . https://doi.org/10.3390/cancers11050615
Peláez, Rafael, et al. "Integrins: Moonlighting Proteins in Invadosome Formation." Cancers vol. 11,5 (2019). doi: https://doi.org/10.3390/cancers11050615
Peláez R, Pariente A, Pérez-Sala Á, Larrayoz IM. Integrins: Moonlighting Proteins in Invadosome Formation. Cancers (Basel). 2019 May 02;11(5). doi: 10.3390/cancers11050615. PMID: 31052560; PMCID: PMC6562994.
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Cancers (Basel). 2019 May 02;11(5). doi: 10.3390/cancers11050615.

Integrins: Moonlighting Proteins in Invadosome Formation.

Cancers

Rafael Peláez, Ana Pariente, Álvaro Pérez-Sala, Ignacio M Larrayoz

Affiliations

  1. Biomarkers and Molecular Signaling Group, Neurodegenerative Diseases Area Center for Biomedical Research of La Rioja, CIBIR, c.p., 26006. Logroño, Spain. [email protected].
  2. Biomarkers and Molecular Signaling Group, Neurodegenerative Diseases Area Center for Biomedical Research of La Rioja, CIBIR, c.p., 26006. Logroño, Spain. [email protected].
  3. Biomarkers and Molecular Signaling Group, Neurodegenerative Diseases Area Center for Biomedical Research of La Rioja, CIBIR, c.p., 26006. Logroño, Spain. [email protected].
  4. Biomarkers and Molecular Signaling Group, Neurodegenerative Diseases Area Center for Biomedical Research of La Rioja, CIBIR, c.p., 26006. Logroño, Spain. [email protected].

PMID: 31052560 PMCID: PMC6562994 DOI: 10.3390/cancers11050615

Abstract

Invadopodia are actin-rich protrusions developed by transformed cells in 2D/3D environments that are implicated in extracellular matrix (ECM) remodeling and degradation. These structures have an undoubted association with cancer invasion and metastasis because invadopodium formation in vivo is a key step for intra/extravasation of tumor cells. Invadopodia are closely related to other actin-rich structures known as podosomes, which are typical structures of normal cells necessary for different physiological processes during development and organogenesis. Invadopodia and podosomes are included in the general term 'invadosomes,' as they both appear as actin puncta on plasma membranes next to extracellular matrix metalloproteinases, although organization, regulation, and function are slightly different. Integrins are transmembrane proteins implicated in cell-cell and cell-matrix interactions and other important processes such as molecular signaling, mechano-transduction, and cell functions, e.g., adhesion, migration, or invasion. It is noteworthy that integrin expression is altered in many tumors, and other pathologies such as cardiovascular or immune dysfunctions. Over the last few years, growing evidence has suggested a role of integrins in the formation of invadopodia. However, their implication in invadopodia formation and adhesion to the ECM is still not well known. This review focuses on the role of integrins in invadopodium formation and provides a general overview of the involvement of these proteins in the mechanisms of metastasis, taking into account classic research through to the latest and most advanced work in the field.

Keywords: cancer; forces; integrins; invadopodia; matrix; microenvironment; podosome; signaling; stromal cells

Conflict of interest statement

The authors declare no conflict of interest.

References

  1. Cell. 1999 Feb 5;96(3):319-28 - PubMed
  2. Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9648-53 - PubMed
  3. J Biol Chem. 1999 Aug 27;274(35):24947-52 - PubMed
  4. Exp Cell Res. 2001 Feb 15;263(2):209-23 - PubMed
  5. FASEB J. 2001 Jun;15(8):1389-97 - PubMed
  6. Clin Exp Metastasis. 2003;20(3):203-13 - PubMed
  7. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1557-61 - PubMed
  8. Eur J Immunol. 2003 Nov;33(11):3038-48 - PubMed
  9. Biophys J. 2004 Jan;86(1 Pt 1):617-28 - PubMed
  10. Matrix Biol. 2004 Jan;22(7):521-38 - PubMed
  11. Exp Cell Res. 2004 May 1;295(2):360-74 - PubMed
  12. Mol Biol Cell. 2004 Aug;15(8):3829-40 - PubMed
  13. Am J Respir Cell Mol Biol. 2004 Oct;31(4):413-22 - PubMed
  14. Mol Cell Biol. 2004 Sep;24(17):7578-97 - PubMed
  15. J Biol Chem. 2005 Jan 21;280(3):2055-64 - PubMed
  16. J Cell Biol. 2005 Jan 31;168(3):441-52 - PubMed
  17. Mol Biol Cell. 2005 Apr;16(4):1901-12 - PubMed
  18. Am J Physiol Heart Circ Physiol. 2005 Jun;288(6):H3001-5 - PubMed
  19. Cell. 2005 May 6;121(3):335-48 - PubMed
  20. J Cell Sci. 2005 May 15;118(Pt 10):2079-82 - PubMed
  21. J Cell Sci. 2005 Dec 1;118(Pt 23):5479-87 - PubMed
  22. Eur J Cell Biol. 2006 Apr;85(3-4):311-7 - PubMed
  23. Blood. 2006 Jul 1;108(1):134-40 - PubMed
  24. Eur J Cell Biol. 2006 Apr;85(3-4):151-7 - PubMed
  25. Mol Cell Biol. 2006 May;26(9):3582-94 - PubMed
  26. Br J Cancer. 2006 Jun 5;94(11):1621-6 - PubMed
  27. Int J Biochem Cell Biol. 2006;38(11):1875-92 - PubMed
  28. Biochim Biophys Acta. 2007 May;1773(5):642-52 - PubMed
  29. Oncogene. 2007 Apr 19;26(18):2563-73 - PubMed
  30. Trends Cell Biol. 2007 Mar;17(3):107-17 - PubMed
  31. J Cell Biol. 2007 Mar 12;176(6):877-88 - PubMed
  32. Cancer Res. 2007 Mar 15;67(6):2649-56 - PubMed
  33. Clin Cancer Res. 2007 Apr 1;13(7):2128-35 - PubMed
  34. Immunity. 2007 Jun;26(6):784-97 - PubMed
  35. Cancer Res. 2007 Aug 1;67(15):7194-202 - PubMed
  36. J Cell Biol. 2007 Sep 10;178(6):1053-64 - PubMed
  37. Mol Biol Cell. 2007 Dec;18(12):4899-910 - PubMed
  38. Int J Cancer. 2008 Mar 1;122(5):1019-29 - PubMed
  39. Nat Cell Biol. 2007 Dec;9(12):1392-400 - PubMed
  40. J Pathol. 2008 Feb;214(3):357-67 - PubMed
  41. J Cell Sci. 2008 Feb 1;121(Pt 3):369-78 - PubMed
  42. Eur J Cell Biol. 2008 Sep;87(8-9):581-90 - PubMed
  43. Eur J Cell Biol. 2008 Sep;87(8-9):555-67 - PubMed
  44. BMC Med. 2008 Apr 28;6:11 - PubMed
  45. J Clin Neurosci. 2008 Jul;15(7):725-37 - PubMed
  46. Biophys J. 2008 Sep;95(5):2203-18 - PubMed
  47. J Cell Biol. 1991 Aug;114(3):567-76 - PubMed
  48. J Leukoc Biol. 2008 Nov;84(5):1306-15 - PubMed
  49. Curr Biol. 2008 Sep 9;18(17):1295-1299 - PubMed
  50. Curr Biol. 2008 Sep 9;18(17):1288-94 - PubMed
  51. Oncogene. 2009 Jan 29;28(4):587-98 - PubMed
  52. Methods Mol Biol. 2009;472:343-60 - PubMed
  53. Nat Rev Cancer. 2009 Apr;9(4):239-52 - PubMed
  54. Cancer Epidemiol Biomarkers Prev. 2009 May;18(5):1584-90 - PubMed
  55. Mol Biol Cell. 2009 Aug;20(16):3763-71 - PubMed
  56. J Cell Mol Med. 2010 Jun;14(6B):1569-93 - PubMed
  57. J Cell Sci. 2009 Sep 1;122(Pt 17):3037-49 - PubMed
  58. J Cell Biol. 2009 Aug 24;186(4):571-87 - PubMed
  59. Sci Signal. 2009 Sep 15;2(88):ra53 - PubMed
  60. Cancer Res. 2009 Nov 15;69(22):8594-602 - PubMed
  61. Cell. 2009 Nov 25;139(5):891-906 - PubMed
  62. Nat Rev Cancer. 2010 Jan;10(1):9-22 - PubMed
  63. J Cell Physiol. 2010 Apr;223(1):134-42 - PubMed
  64. Cancer. 2010 Mar 15;116(6):1526-34 - PubMed
  65. J Cell Biol. 2010 Apr 5;189(1):13-22 - PubMed
  66. Cancer Res. 2010 Jun 1;70(11):4327-34 - PubMed
  67. FASEB J. 2010 Oct;24(10):3903-15 - PubMed
  68. J Exp Clin Cancer Res. 2010 Jul 11;29:93 - PubMed
  69. J Biol Chem. 2010 Sep 24;285(39):29911-24 - PubMed
  70. FASEB J. 2010 Dec;24(12):4782-92 - PubMed
  71. Exp Cell Res. 2010 Oct 15;316(17):2922-31 - PubMed
  72. Eur J Cell Biol. 2011 Feb-Mar;90(2-3):224-36 - PubMed
  73. Mol Biol Cell. 2010 Dec;21(23):4108-19 - PubMed
  74. Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21016-21 - PubMed
  75. Biophys J. 2011 Feb 2;100(3):573-582 - PubMed
  76. J Cell Biol. 2011 Mar 7;192(5):883-97 - PubMed
  77. Int J Biochem Cell Biol. 2011 Jun;43(6):928-35 - PubMed
  78. Nat Cell Biol. 2011 Apr;13(4):383-93 - PubMed
  79. Nat Rev Mol Cell Biol. 2011 Jun 23;12(7):413-26 - PubMed
  80. PLoS One. 2011;6(7):e22499 - PubMed
  81. J Natl Cancer Inst. 2011 Oct 19;103(20):1513-28 - PubMed
  82. Exp Cell Res. 2011 Nov 1;317(18):2562-72 - PubMed
  83. J Cell Biol. 2011 Nov 28;195(5):903-20 - PubMed
  84. Mol Biol Cell. 2012 Jan;23(2):297-309 - PubMed
  85. J Cell Sci. 2012 Apr 1;125(Pt 7):1666-72 - PubMed
  86. J Cell Sci. 2012 May 1;125(Pt 9):2300-14 - PubMed
  87. J Cell Sci. 2012 Feb 1;125(Pt 3):724-34 - PubMed
  88. Trends Mol Med. 2012 Apr;18(4):224-32 - PubMed
  89. J Cell Sci. 2012 Apr 1;125(Pt 7):1621-6 - PubMed
  90. Cell Adh Migr. 2012 May-Jun;6(3):249-60 - PubMed
  91. PLoS One. 2012;7(5):e36753 - PubMed
  92. Eur J Cell Biol. 2012 Nov-Dec;91(11-12):908-22 - PubMed
  93. Nat Rev Mol Cell Biol. 2012 Jun 22;13(7):448-62 - PubMed
  94. J Cell Physiol. 2013 Feb;228(2):416-27 - PubMed
  95. Nat Mater. 2012 Jul 01;11(8):734-41 - PubMed
  96. J Cell Sci. 2012 Jul 1;125(Pt 13):3025-38 - PubMed
  97. Exp Cell Res. 2012 Nov 1;318(18):2312-23 - PubMed
  98. J Biol Chem. 2012 Sep 21;287(39):32981-92 - PubMed
  99. PLoS Biol. 2012;10(9):e1001386 - PubMed
  100. Curr Opin Cell Biol. 2012 Oct;24(5):600-6 - PubMed
  101. Trends Cell Biol. 2013 Jan;23(1):16-21 - PubMed
  102. Biol Open. 2012 Aug 15;1(8):711-22 - PubMed
  103. Blood. 2013 Mar 28;121(13):2542-52 - PubMed
  104. Am J Respir Cell Mol Biol. 2013 Apr;48(4):503-10 - PubMed
  105. Stem Cells Dev. 2013 Jun 15;22(12):1830-8 - PubMed
  106. Exp Cell Res. 2013 Apr 15;319(7):967-81 - PubMed
  107. Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):E1361-70 - PubMed
  108. Matrix Biol. 2013 Aug 8;32(6):332-41 - PubMed
  109. Oncogene. 2014 Mar 6;33(10):1265-73 - PubMed
  110. J Invest Dermatol. 2013 Sep;133(9):2276-85 - PubMed
  111. Mol Biol Cell. 2013 Jun;24(11):1661-75, S1-11 - PubMed
  112. J Cell Biol. 2013 Apr 15;201(2):279-92 - PubMed
  113. Open Biol. 2013 Jun 05;3(6):120159 - PubMed
  114. Int J Cancer. 2013 Dec 15;133(12):2824-33 - PubMed
  115. Cytoskeleton (Hoboken). 2013 Oct;70(10):572-89 - PubMed
  116. J Cell Sci. 2013 Jul 15;126(Pt 14):2979-89 - PubMed
  117. Transl Res. 2013 Sep;162(3):133-43 - PubMed
  118. Cancer Res. 2013 Oct 15;73(20):6175-84 - PubMed
  119. Elife. 2013 Sep 03;2:e00884 - PubMed
  120. Oncotarget. 2013 Oct;4(10):1686-97 - PubMed
  121. PLoS One. 2013 Sep 24;8(9):e75113 - PubMed
  122. Exp Cell Res. 1985 Jul;159(1):141-57 - PubMed
  123. Matrix Biol. 2014 Feb;34:144-53 - PubMed
  124. J Biol Chem. 2013 Dec 20;288(51):36418-25 - PubMed
  125. Cell Rep. 2013 Dec 12;5(5):1456-68 - PubMed
  126. Cell Rep. 2013 Dec 12;5(5):1159-68 - PubMed
  127. Acta Biomater. 2014 May;10(5):1886-96 - PubMed
  128. Mol Cancer Res. 2014 Mar;12(3):297-312 - PubMed
  129. Int J Biochem Cell Biol. 2014 May;50:47-54 - PubMed
  130. Mol Med Rep. 2014 Apr;9(4):1142-6 - PubMed
  131. Cell Adh Migr. 2014;8(3):179-91 - PubMed
  132. Cell Adh Migr. 2014;8(3):191-204 - PubMed
  133. Cancer Cell. 2014 Jun 16;25(6):719-34 - PubMed
  134. Cell Signal. 2014 Sep;26(9):2008-15 - PubMed
  135. Mol Cancer. 2014 May 19;13:112 - PubMed
  136. J Natl Cancer Inst. 2014 Jun 03;106(8):null - PubMed
  137. J Cell Sci. 2014 Oct 1;127(Pt 19):4213-24 - PubMed
  138. PLoS One. 2014 Aug 04;9(8):e94995 - PubMed
  139. Eur J Cell Biol. 2014 Oct;93(10-12):438-44 - PubMed
  140. Cell Rep. 2014 Sep 11;8(5):1558-70 - PubMed
  141. Mol Cancer Res. 2015 Feb;13(2):273-80 - PubMed
  142. Cancer Chemother Pharmacol. 2014 Nov;74(5):1039-46 - PubMed
  143. Nat Cell Biol. 2014 Oct;16(10):931-41, 1-8 - PubMed
  144. PLoS One. 2014 Sep 26;9(9):e107674 - PubMed
  145. Proteomics. 2015 Jan;15(2-3):272-86 - PubMed
  146. Exp Cell Res. 1989 Jun;182(2):645-52 - PubMed
  147. J Cell Biol. 2014 Nov 24;207(4):517-33 - PubMed
  148. J Transl Med. 2014 Dec 05;12:339 - PubMed
  149. J Clin Invest. 1989 Sep;84(3):773-80 - PubMed
  150. Exp Cell Res. 2015 Mar 1;332(1):78-88 - PubMed
  151. Nat Rev Mol Cell Biol. 2014 Dec;15(12):761-3 - PubMed
  152. J Cell Biol. 2015 Feb 2;208(3):331-50 - PubMed
  153. Front Cell Dev Biol. 2015 Feb 02;3:4 - PubMed
  154. Cell Cycle. 2015;14(9):1370-4 - PubMed
  155. Asian Pac J Cancer Prev. 2015;16(6):2187-91 - PubMed
  156. PLoS One. 2015 Mar 31;10(3):e0121003 - PubMed
  157. PLoS One. 2015 Apr 01;10(4):e0120781 - PubMed
  158. J Neuropathol Exp Neurol. 2015 May;74(5):425-41 - PubMed
  159. Oncogene. 2016 Mar 3;35(9):1099-1110 - PubMed
  160. Clin Exp Metastasis. 2015 Jun;32(5):507-16 - PubMed
  161. Int J Biochem Cell Biol. 2015 Aug;65:52-60 - PubMed
  162. Lab Invest. 2015 Sep;95(9):976-86 - PubMed
  163. Biochim Biophys Acta. 2015 Oct;1853(10 Pt A):2515-25 - PubMed
  164. Biochim Biophys Acta. 2015 Dec;1856(2):178-88 - PubMed
  165. Cancer Discov. 2015 Sep;5(9):932-43 - PubMed
  166. Small GTPases. 2015;6(3):135-44 - PubMed
  167. Hepatology. 2016 Jan;63(1):217-32 - PubMed
  168. Nat Cell Biol. 2015 Dec;17(12):1577-1587 - PubMed
  169. Adv Drug Deliv Rev. 2016 Feb 1;97:28-40 - PubMed
  170. Nature. 2015 Nov 19;527(7578):329-35 - PubMed
  171. Exp Cell Res. 2016 Apr 10;343(1):89-95 - PubMed
  172. Biomaterials. 2016 Apr;84:119-129 - PubMed
  173. Oncotarget. 2016 Jun 7;7(23):35478-89 - PubMed
  174. J Cell Sci. 2016 May 1;129(9):1759-68 - PubMed
  175. Front Biosci (Landmark Ed). 2016 Jun 01;21:1092-117 - PubMed
  176. Science. 2016 Apr 8;352(6282):175-80 - PubMed
  177. Biochem Biophys Res Commun. 2016 Jul 29;476(3):115-20 - PubMed
  178. J Cell Sci. 2016 Jul 1;129(13):2586-98 - PubMed
  179. Oncotarget. 2016 Jul 26;7(30):47904-47917 - PubMed
  180. Sci Rep. 2016 Jun 29;6:28805 - PubMed
  181. Eur J Cell Biol. 2016 Nov;95(11):441-448 - PubMed
  182. Springerplus. 2016 Jul 15;5(1):1094 - PubMed
  183. Handb Exp Pharmacol. 2017;235:123-152 - PubMed
  184. Mol Oncol. 2016 Oct;10(8):1344-62 - PubMed
  185. Oncoimmunology. 2016 Jul 15;5(7):e1196299 - PubMed
  186. Mol Cancer Res. 2016 Dec;14(12):1277-1287 - PubMed
  187. Cell Rep. 2016 Oct 4;17(2):484-500 - PubMed
  188. Exp Cell Res. 2016 Nov 15;349(1):85-94 - PubMed
  189. J Neurooncol. 2017 Jan;131(2):233-244 - PubMed
  190. Oncotarget. 2016 Nov 29;7(48):78473-78486 - PubMed
  191. Sci Rep. 2016 Nov 08;6:36142 - PubMed
  192. Sci Rep. 2016 Nov 30;6:37874 - PubMed
  193. Mol Cell Biol. 2017 Apr 14;37(9): - PubMed
  194. Sci Rep. 2017 Apr 03;7:45895 - PubMed
  195. Trends Cell Biol. 2017 Aug;27(8):595-607 - PubMed
  196. Oncotarget. 2017 May 30;8(22):36099-36114 - PubMed
  197. J Cell Sci. 2017 Jun 1;130(11):1965-1978 - PubMed
  198. FEBS J. 2018 Jan;285(1):8-27 - PubMed
  199. Immunol Lett. 2017 Sep;189:64-72 - PubMed
  200. Sci Rep. 2017 Jul 5;7(1):4656 - PubMed
  201. Oncogene. 2017 Nov 9;36(45):6244-6261 - PubMed
  202. PLoS One. 2017 Aug 2;12(8):e0181579 - PubMed
  203. J Cell Sci. 2017 Oct 15;130(20):3532-3541 - PubMed
  204. F1000Res. 2017 Aug 31;6:1612 - PubMed
  205. J Cell Biol. 2018 Jan 2;217(1):375-395 - PubMed
  206. Semin Cell Dev Biol. 2019 Jan;85:110-121 - PubMed
  207. Clin Ther. 2017 Dec;39(12):2420-2436 - PubMed
  208. Sci Rep. 2017 Dec 13;7(1):17511 - PubMed
  209. Nat Commun. 2018 Feb 6;9(1):515 - PubMed
  210. Biophys J. 2018 Feb 6;114(3):650-662 - PubMed
  211. Mol Cancer. 2018 Feb 7;17(1):21 - PubMed
  212. Front Cell Dev Biol. 2018 Feb 20;6:18 - PubMed
  213. Int J Mol Sci. 2018 Mar 26;19(4):null - PubMed
  214. Dev Cell. 2018 Apr 9;45(1):132-145.e3 - PubMed
  215. Biochim Biophys Acta Mol Basis Dis. 2018 Jul;1864(7):2395-2408 - PubMed
  216. J Biol Chem. 2018 Jun 29;293(26):10172-10185 - PubMed
  217. Front Immunol. 2018 Apr 30;9:846 - PubMed
  218. Nat Commun. 2018 May 23;9(1):2031 - PubMed
  219. PLoS One. 2018 Jun 20;13(6):e0199128 - PubMed
  220. Nat Rev Cancer. 2018 Sep;18(9):533-548 - PubMed
  221. Curr Opin Cell Biol. 2018 Dec;55:17-23 - PubMed
  222. NPJ Breast Cancer. 2018 Jul 16;4:18 - PubMed
  223. Cell Mol Life Sci. 2018 Oct;75(20):3683-3692 - PubMed
  224. Trends Cancer. 2018 Aug;4(8):537-552 - PubMed
  225. Drug Resist Updat. 2018 Jul;39:1-17 - PubMed
  226. Cell Physiol Biochem. 2018;49(3):848-868 - PubMed
  227. Curr Opin Cell Biol. 2019 Feb;56:14-21 - PubMed
  228. Trends Cell Biol. 2019 Feb;29(2):150-163 - PubMed
  229. Curr Opin Cell Biol. 2019 Feb;56:iii-iv - PubMed
  230. Biochim Biophys Acta Mol Cell Res. 2019 Apr;1866(4):545-553 - PubMed
  231. Biochim Biophys Acta Rev Cancer. 2019 Jan;1871(1):192-198 - PubMed
  232. Mol Cancer Res. 2019 Apr;17(4):987-1001 - PubMed
  233. Biomolecules. 2019 Jan 09;9(1): - PubMed
  234. Oncogene. 2019 May;38(19):3598-3615 - PubMed
  235. Mol Cancer. 2019 Jan 21;18(1):14 - PubMed
  236. Biochim Biophys Acta Gen Subj. 2019 May;1863(5):813-829 - PubMed
  237. Trends Immunol. 2019 Apr;40(4):310-327 - PubMed
  238. Cell Death Dis. 2019 Mar 20;10(4):273 - PubMed
  239. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6687-91 - PubMed
  240. Cancer Res. 1993 Jul 15;53(14):3411-5 - PubMed
  241. Cell. 1996 May 31;85(5):683-93 - PubMed
  242. J Biol Chem. 1996 Nov 1;271(44):27221-4 - PubMed
  243. Front Biosci. 1998 Aug 01;3:d757-68 - PubMed

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