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Short Communications

Calpain2 mediates Rab5-driven focal adhesion disassembly and cell migration

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Pages 185-194 | Received 16 Jun 2017, Accepted 04 Sep 2017, Published online: 06 Nov 2017

References

  • Webb DJ, Parsons JT, Horwitz AF. Adhesion assembly, disassembly and turnover in migrating cells – over and over and over again. Nat Cell Biol. 2002;4:E97-100. doi:10.1038/ncb0402-e97. PMID:11944043
  • Broussard JA, Webb DJ, Kaverina I. Asymmetric focal adhesion disassembly in motile cells. Curr Opin Cell Biol. 2008;20:85-90. doi:10.1016/j.ceb.2007.10.009. PMID:18083360
  • Bhatt A, Kaverina I, Otey C, Huttenlocher A. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J Cell Sci. 2002;115:3415-25. PMID:12154072
  • Franco SJ, Rodgers MA, Perrin BJ, Han J, Bennin DA, Critchley DR, Huttenlocher A. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat Cell Biol. 2004;6:977-83. doi:10.1038/ncb1175. PMID:15448700
  • Cortesio CL, Boateng LR, Piazza TM, Bennin DA, Huttenlocher A. Calpain-mediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J Biol Chem. 2011;286:9998-10006. doi:10.1074/jbc.M110.187294. PMID:21270128
  • Perrin BJ, Amann KJ, Huttenlocher A. Proteolysis of cortactin by calpain regulates membrane protrusion during cell migration. Mol Biol Cell. 2006;17:239-50. doi:10.1091/mbc.E05-06-0488. PMID:16280362
  • Chan KT, Bennin DA, Huttenlocher A. Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). J Biol Chem. 2010;285:11418-26. doi:10.1074/jbc.M109.090746. PMID:20150423
  • Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature. 2008;456:409–12. doi:10.1038/nature07451. PMID:19020623
  • Moldoveanu T, Gehring K, Green DR. Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature. 2008;456:404-8. doi:10.1038/nature07353. PMID:19020622
  • Reverter D, Strobl S, Fernandez-Catalan C, Sorimachi H, Suzuki K, Bode W. Structural basis for possible calcium-induced activation mechanisms of calpains. Biol Chem. 2001;382:753-66. doi:10.1515/bchm.2001.382.5.753. PMID:11517928
  • Storr SJ, Carragher NO, Frame MC, Parr T, Martin SG. The calpain system and cancer. Nat Rev Cancer. 2011;11:364-74. doi:10.1038/nrc3050. PMID:21508973
  • Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. 2003;83:731-801. doi:10.1152/physrev.00029.2002. PMID:12843408
  • Hoshino D, Nagano M, Saitoh A, Koshikawa N, Suzuki T, Seiki M. The phosphoinositide-binding protein ZF21 regulates ECM degradation by invadopodia. PLoS One. 2013;8:e50825. doi:10.1371/journal.pone.0050825. PMID:23382803
  • Nagano M, Hoshino D, Sakamoto T, Akizawa T, Koshikawa N, Seiki M. ZF21 is a new regulator of focal adhesion disassembly and a potential member of the spreading initiation center. Cell Adh Migr. 2011;5:23-8. doi:10.4161/cam.5.1.13492. PMID:20890123
  • Sato K, Saito Y, Kawashima S. Identification and characterization of membrane-bound calpains in clathrin-coated vesicles from bovine brain. Eur J Biochem 1995;230:25-31. doi:10.1111/j.1432-1033.1995.tb20529.x. PMID:7601107
  • Su W, Kowalczyk AP. The VE-cadherin cytoplasmic domain undergoes proteolytic processing during endocytosis. Mol Biol Cell. 2017;28:76-84. doi:10.1091/mbc.E16-09-0658. PMID:27798242
  • Franco S, Perrin B, Huttenlocher A. Isoform specific function of calpain 2 in regulating membrane protrusion. Exp Cell Res. 2004;299:179-87. doi:10.1016/j.yexcr.2004.05.021. PMID:15302585
  • Rintanen N, Karjalainen M, Alanko J, Paavolainen L, Maki A, Nissinen L, et al. Calpains promote alpha2beta1 integrin turnover in nonrecycling integrin pathway. Mol Biol Cell. 2012;23:448-63. doi:10.1091/mbc.E11-06-0548. PMID:22160595
  • Mendoza P, Ortiz R, Diaz J, Quest AF, Leyton L, Stupack D, Torres VA. Rab5 activation promotes focal adhesion disassembly, migration and invasiveness in tumor cells. J Cell Sci. 2013;126:3835-47. doi:10.1242/jcs.119727. PMID:23813952
  • Leloup L, Shao H, Bae YH, Deasy B, Stolz D, Roy P, Wells A. m-Calpain activation is regulated by its membrane localization and by its binding to phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 2010;285:33549-66. doi:10.1074/jbc.M110.123604. PMID:20729206
  • Nuzzi PA, Senetar MA, Huttenlocher A. Asymmetric localization of calpain 2 during neutrophil chemotaxis. Mol Biol Cell. 2007;18:795-805. doi:10.1091/mbc.E06-09-0876. PMID:17192410
  • Palamidessi A, Frittoli E, Ducano N, Offenhauser N, Sigismund S, Kajiho H, Parazzoli D, Oldani A, Gobbi M, Serini G, et al. The GTPase-activating protein RN-tre controls focal adhesion turnover and cell migration. Curr Biol. 2013;23:2355-64. doi:10.1016/j.cub.2013.09.060. PMID:24239119
  • Torres VA, Mielgo A, Barbero S, Hsiao R, Wilkins JA, Stupack DG. Rab5 mediates caspase-8-promoted cell motility and metastasis. Mol Biol Cell. 2010;21:369-76. doi:10.1091/mbc.E09-09-0769. PMID:19923319
  • Rosser BG, Powers SP, Gores GJ. Calpain activity increases in hepatocytes following addition of ATP. Demonstration by a novel fluorescent approach. J Biol Chem 1993;268:23593-600. PMID:8226886
  • Niapour M, Berger S. Flow cytometric measurement of calpain activity in living cells. Cytometry A. 2007;71:475-85. doi:10.1002/cyto.a.20399. PMID:17458879
  • Farr C, Berger S. Measuring calpain activity in fixed and living cells by flow cytometry. J Vis Exp. 2010. doi:10.3791/2050. PMID:20644512
  • Friedrich P. The intriguing Ca2+ requirement of calpain activation. Biochem Biophys Res Commun. 2004;323:1131-3. doi:10.1016/j.bbrc.2004.08.194. PMID:15451413
  • Mackay L, Mikolajewicz N, Komarova SV, Khadra A. Systematic Characterization of Dynamic Parameters of Intracellular Calcium Signals. Front Physiol. 2016;7:525. doi:10.3389/fphys.2016.00525. PMID:27891096
  • Lee KC, Chang HT, Chou KJ, Tang KY, Wang JL, Lo YK, Huang JK, Chen WC, Su W, Law YP, et al. Mechanism underlying histamine-induced intracellular Ca2+ movement in PC3 human prostate cancer cells. Pharmacol Res. 2001;44:547-52. doi:10.1006/phrs.2001.0891. PMID:11735364
  • Zhou MH, Zheng H, Si H, Jin Y, Peng JM, He L, Zhou Y, Muñoz-Garay C, Zawieja DC, Kuo L, et al. Stromal interaction molecule 1 (STIM1) and Orai1 mediate histamine-evoked calcium entry and nuclear factor of activated T-cells (NFAT) signaling in human umbilical vein endothelial cells. J Biol Chem. 2014;289:29446-56. doi:10.1074/jbc.M114.578492. PMID:25190815
  • Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 1999;146:1033–44. doi:10.1083/jcb.146.5.1033. PMID:10477757
  • Ezratty EJ, Partridge MA, Gundersen GG. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol. 2005;7:581-90. doi:10.1038/ncb1262. PMID:15895076
  • Chao WT, Kunz J. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett. 2009;583:1337-43. doi:10.1016/j.febslet.2009.03.037. PMID:19306879
  • Liu G, Meng X, Jin Y, Bai J, Zhao Y, Cui X, Chen F, Fu S. Inhibitory role of focal adhesion kinase on anoikis in the lung cancer cell A549. Cell Biol Int. 2008;32:663-70. doi:10.1016/j.cellbi.2008.01.292. PMID:18343694
  • Kogan TV, Jadoun J, Mittelman L, Hirschberg K, Osherov N. Involvement of secreted Aspergillus fumigatus proteases in disruption of the actin fiber cytoskeleton and loss of focal adhesion sites in infected A549 lung pneumocytes. J Infect Dis. 2004;189:1965-73. doi:10.1086/420850. PMID:15143461
  • Beinke C, Van Beuningen D, Cordes N. Ionizing radiation modules of the expression and tyrosine phosphorylation of the focal adhesion-associated proteins focal adhesion kinase (FAK) and its substrates p130cas and paxillin in A549 human lung carcinoma cells in vitro. Int J Radiat Biol. 2003;79:721-31. doi:10.1080/09553000310001610231. PMID:14703945
  • Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature. 1998;394:494-8. doi:10.1038/28879. PMID:9697774
  • Christoforidis S, McBride HM, Burgoyne RD, Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature. 1999;397:621-5. doi:10.1038/17618. PMID:10050856
  • Christoforidis S, Zerial M. Purification of EEA1 from bovine brain cytosol using Rab5 affinity chromatography and activity assays. Methods Enzymol. 2001;329:120-32. doi:10.1016/S0076-6879(01)29073-9. PMID:11210528
  • Murray DH, Jahnel M, Lauer J, Avellaneda MJ, Brouilly N, Cezanne A, Morales-Navarrete H, Perini ED, Ferguson C, Lupas AN, et al. An endosomal tether undergoes an entropic collapse to bring vesicles together. Nature. 2016;537:107-11. doi:10.1038/nature19326. PMID:27556945
  • Jacquemet G, Baghirov H, Georgiadou M, Sihto H, Peuhu E, Cettour-Janet P, He T, Perälä M, Kronqvist P, Joensuu H, et al. L-type calcium channels regulate filopodia stability and cancer cell invasion downstream of integrin signalling. Nat Commun. 2016;7:13297. doi:10.1038/ncomms13297. PMID:27910855
  • Fiorio Pla A, Gkika D. Emerging role of TRP channels in cell migration: from tumor vascularization to metastasis. Front Physiol. 2013;4:311. doi:10.3389/fphys.2013.00311. PMID:24204345
  • Schwab A, Stock C. Ion channels and transporters in tumour cell migration and invasion. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130102. doi:10.1098/rstb.2013.0102. PMID:24493750
  • Caceres M, Ortiz L, Recabarren T, Romero A, Colombo A, Leiva-Salcedo E, Varela D, Rivas J, Silva I, Morales D, et al. TRPM4 Is a Novel Component of the Adhesome Required for Focal Adhesion Disassembly, Migration and Contractility. PLoS One. 2015;10:e0130540. doi:10.1371/journal.pone.0130540. PMID:26110647
  • Pardo LA, Stuhmer W. The roles of K(+) channels in cancer. Nat Rev Cancer. 2014;14:39-48. doi:10.1038/nrc3635. PMID:24336491
  • Huang X, Jan LY. Targeting potassium channels in cancer. J Cell Biol. 2014;206:151-62. doi:10.1083/jcb.201404136. PMID:25049269
  • Torres VA, Mielgo A, Barila D, Anderson DH, Stupack D. Caspase 8 promotes peripheral localization and activation of Rab5. J Biol Chem. 2008;283:36280-9. doi:10.1074/jbc.M805878200. PMID:18974049

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