1,403
Views
19
CrossRef citations to date
0
Altmetric
Commentary

RABGTPases in MT1-MMP trafficking and cell invasion: Physiology versus pathology

&
Pages 145-152 | Received 30 Sep 2014, Accepted 05 Nov 2014, Published online: 30 Jul 2015

References

  • Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7:678-89; PMID:17717539; http://dx.doi.org/10.1038/nri2156
  • Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013; 229:176-85; PMID:23096265; http://dx.doi.org/10.1002/path.4133
  • Caldieri G, Ayala I, Attanasio F, Buccione R. Cell and molecular biology of invadopodia. Int Rev Cell Mol Biol 2009; 275:1-34; PMID:19491051; http://dx.doi.org/10.1016/S1937-6448(09)75001-4
  • Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003; 3:362-74; PMID:12724734; http://dx.doi.org/10.1038/nrc1075
  • Bravo-Cordero JJ, Hodgson L, Condeelis J. Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 2012; 24:277-83; PMID:22209238; http://dx.doi.org/10.1016/j.ceb.2011.12.004
  • Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol 2010; 188:11-9; PMID:19951899; http://dx.doi.org/10.1083/jcb.200909003
  • Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le Cabec V. Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol 2010; 184:1049-61; PMID:20018633; http://dx.doi.org/10.4049/jimmunol.0902223
  • Wolf K, Friedl P. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol 2011; 21:736-44; PMID:22036198; http://dx.doi.org/10.1016/j.tcb.2011.09.006
  • Wiesner C, Le-Cabec V, El Azzouzi K, Maridonneau-Parini I, Linder S. Podosomes in space: macrophage migration and matrix degradation in 2D and 3D settings. Cell Adh Migr 2014; 8(3):179-91; PMID:24713854; http://dx.doi.org/10.4161/cam.28116
  • Petrie RJ, Koo H, Yamada KM. Generation of compartmentalized pressure by a nuclear piston governs cell motility in a 3D matrix. Science 2014; 345:1062-5; PMID:25170155; http://dx.doi.org/10.1126/science.1256965
  • van Hinsbergh VW, Engelse MA, Quax PH. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler Thromb Vasc Biol 2006; 26:716-28; PMID:16469948; http://dx.doi.org/10.1161/01.ATV.0000209518.58252.17
  • Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer 2007; 7:800-8; PMID:17851543; http://dx.doi.org/10.1038/nrc2228
  • Roycik MD, Fang X, Sang QX. A fresh prospect of extracellular matrix hydrolytic enzymes and their substrates. Curr Pharm Des 2009; 15:1295-308; PMID:19355969; http://dx.doi.org/10.2174/138161209787846676
  • Itoh Y, Seiki M. MT1-MMP: an enzyme with multidimensional regulation. Trends Biochem Sci 2004; 29:285-9; PMID:15276180; http://dx.doi.org/10.1016/j.tibs.2004.04.001
  • Barbolina MV, Stack MS. Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Seminars Cell Dev Biol 2008; 19:24-33; PMID:17702616; http://dx.doi.org/10.1016/j.semcdb.2007.06.008
  • Kajita M, Itoh Y, Chiba T, Mori H, Okada A, Kinoh H, Seiki M. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 2001; 153:893-904; PMID:11381077; http://dx.doi.org/10.1083/jcb.153.5.893
  • Endo K, Takino T, Miyamori H, Kinsen H, Yoshizaki T, Furukawa M, Sato H. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem 2003; 278:40764-70; PMID:12904296; http://dx.doi.org/10.1074/jbc.M306736200
  • Frittoli E, Palamidessi A, Disanza A, Scita G. Secretory and endo/exocytic trafficking in invadopodia formation: the MT1-MMP paradigm. Eur J Cell Biol 2011; 90:108-14; PMID:20605060; http://dx.doi.org/10.1016/j.ejcb.2010.04.007
  • Remacle A, Murphy G, Roghi C. Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J Cell Sci 2003; 116:3905-16; PMID:12915589; http://dx.doi.org/10.1242/jcs.00710
  • Wiesner C, Faix J, Himmel M, Bentzien F, Linder S. KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 2010; 116:1559-69; PMID:20505159; http://dx.doi.org/10.1182/blood-2009-12-257089
  • Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, Rottner K, Galli T, Chavrier P. MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol 2008; 18:926-31; PMID:18571410; http://dx.doi.org/10.1016/j.cub.2008.05.044
  • Hutagalung AH, Novick PJ. Role of rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011; 91:119-49; PMID:21248164; http://dx.doi.org/10.1152/physrev.00059.2009
  • Bravo-Cordero JJ, Marrero-Diaz R, Megias D, Genis L, Garcia-Grande A, Garcia MA, Arroyo AG, Montoya MC. MT1-MMP proinvasive activity is regulated by a novel rab8-dependent exocytic pathway. EMBO J 2007; 26:1499-510; PMID:17332756; http://dx.doi.org/10.1038/sj.emboj.7601606
  • Williams KC, Coppolino MG. Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J Biol Chem 2011; 286:43405-16; PMID:22002060; http://dx.doi.org/10.1074/jbc.M111.297069
  • Wiesner C, El Azzouzi K, Linder S. A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages. J Cell Sci 2013; 126:2820-33; PMID:23606746; http://dx.doi.org/10.1242/jcs.122358
  • Frittoli E, Palamidessi A, Marighetti P, Confalonieri S, Bianchi F, Malinverno C, Mazzarol G, Viale G, Martin-Padura I, Garre M, et al. A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination. J Cell Biol 2014; 206:307-28; PMID:25049275; http://dx.doi.org/10.1083/jcb.201403127
  • Linder S, Wiesner C, Himmel M. Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 2011; 27:185-211; PMID:21801014; http://dx.doi.org/10.1146/annurev-cellbio-092910-154216
  • Monteiro P, Rosse C, Castro-Castro A, Irondelle M, Lagoutte E, Paul-Gilloteaux P, Desnos C, Formstecher E, Darchen F, Perrais D, et al. Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol 2013; 203:1063-79; PMID:24344185; http://dx.doi.org/10.1083/jcb.201306162
  • Hoshino D, Kirkbride KC, Costello K, Clark ES, Sinha S, Grega-Larson N, Tyska MJ, Weaver AM. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep 2013; 5:1159-68; PMID:24290760; http://dx.doi.org/10.1016/j.celrep.2013.10.050
  • Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 2007; 17:107-17; PMID:17275303; http://dx.doi.org/10.1016/j.tcb.2007.01.002
  • Murphy DA, Courtneidge SA. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 2011; 12:413-26; PMID:21697900; http://dx.doi.org/10.1038/nrm3141
  • Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009; 10:513-25; PMID:19603039; http://dx.doi.org/10.1038/nrm2728
  • Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107-17; PMID:11252952; http://dx.doi.org/10.1038/35052055
  • Yamamoto H, Koga H, Katoh Y, Takahashi S, Nakayama K, Shin HW. Functional cross-talk between rab14 and rab4 through a dual effector, RUFY1/Rabip4. Mol Biol Cell 2010; 21:2746-55; PMID:20534812; http://dx.doi.org/10.1091/mbc.E10-01-0074
  • Hoshino D, Koshikawa N, Suzuki T, Quaranta V, Weaver AM, Seiki M, Ichikawa K. Establishment and validation of computational model for MT1-MMP dependent ECM degradation and intervention strategies. PLoS Comput Biol 2012; 8:e1002479; PMID:22511862; http://dx.doi.org/10.1371/journal.pcbi.1002479
  • Watanabe A, Hoshino D, Koshikawa N, Seiki M, Suzuki T, Ichikawa K. Critical role of transient activity of MT1-MMP for ECM degradation in invadopodia. PLoS Comput Biol 2013; 9:e1003086; PMID:23737743; http://dx.doi.org/10.1371/journal.pcbi.1003086
  • Vitale G, Rybin V, Christoforidis S, Thornqvist P, McCaffrey M, Stenmark H, Zerial M. Distinct rab-binding domains mediate the interaction of rabaptin-5 with GTP-bound rab4 and rab5. EMBO J 1998; 17:1941-51; PMID:9524117; http://dx.doi.org/10.1093/emboj/17.7.1941
  • Van Goethem E, Guiet R, Balor S, Charriere GM, Poincloux R, Labrousse A, Maridonneau-Parini I, Le Cabec V. Macrophage podosomes go 3D. Eur J Cell Biol 2011; 90:224-36; PMID:20801545; http://dx.doi.org/10.1016/j.ejcb.2010.07.011
  • Schlierf B, Fey GH, Hauber J, Hocke GM, Rosorius O. Rab11b is essential for recycling of transferrin to the plasma membrane. Exp Cell Res 2000; 259:257-65; PMID:10942597; http://dx.doi.org/10.1006/excr.2000.4947
  • Cougoule C, Le Cabec V, Poincloux R, Al Saati T, Mege JL, Tabouret G, Lowell CA, Laviolette-Malirat N, Maridonneau-Parini I. Three-dimensional migration of macrophages requires hck for podosome organization and extracellular matrix proteolysis. Blood 2010; 115:1444-52; PMID:19897576; http://dx.doi.org/10.1182/blood-2009-04-218735
  • Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP. Endocytic trafficking of rac is required for its activation and for the spatial restriction of signaling in cell migration. Cell 2008; 134:135-47; PMID:18614017; http://dx.doi.org/10.1016/j.cell.2008.05.034
  • Liu SS, Chen XM, Zheng HX, Shi SL, Li Y. Knockdown of rab5a expression decreases cancer cell motility and invasion through integrin-mediated signaling pathway. J Biomed Sci 2011; 18:58; PMID:21849022; http://dx.doi.org/10.1186/1423-0127-18-58
  • Yu L, Hui-chen F, Chen Y, Zou R, Yan S, Chun-xiang L, Wu-ru W, Li P. Differential expression of RAB5A in human lung adenocarcinoma cells with different metastasis potential. Clin Exp Metastasis 1999; 17:213-9; PMID:10432006; http://dx.doi.org/10.1023/A:1006617016451
  • Onodera Y, Nam JM, Hashimoto A, Norman JC, Shirato H, Hashimoto S, Sabe H. Rab5c promotes AMAP1-PRKD2 complex formation to enhance beta1 integrin recycling in EGF-induced cancer invasion. J Cell Biol 2012; 197:983-96; PMID:22734003; http://dx.doi.org/10.1083/jcb.201201065
  • 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; PMID:19923319; http://dx.doi.org/10.1091/mbc.E09-09-0769
  • Torres VA, Stupack DG. Rab5 in the regulation of cell motility and invasion. Curr Protein Pept Sci 2011; 12:43-51; PMID:21190523; http://dx.doi.org/10.2174/138920311795659461
  • Miller FR, Santner SJ, Tait L, Dawson PJ. MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J Natl Cancer Inst 2000; 92:1185-6; PMID:10904098; http://dx.doi.org/10.1093/jnci/92.14.1185A
  • Hu M, Yao J, Carroll DK, Weremowicz S, Chen H, Carrasco D, Richardson A, Violette S, Nikolskaya T, Nikolsky Y, et al. Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 2008; 13:394-406; PMID:18455123; http://dx.doi.org/10.1016/j.ccr.2008.03.007
  • Nystrom ML, Thomas GJ, Stone M, Mackenzie IC, Hart IR, Marshall JF. Development of a quantitative method to analyse tumour cell invasion in organotypic culture. J Pathol 2005; 205:468-75; PMID:15685705; http://dx.doi.org/10.1002/path.1716
  • Sabeh F, Shimizu-Hirota R, Weiss SJ. Protease-dependent vs. -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 2009; 185:11-9; PMID:19332889; http://dx.doi.org/10.1083/jcb.200807195
  • Scita G, Di Fiore PP. The endocytic matrix. Nature 2010; 463:464-73; PMID:20110990; http://dx.doi.org/10.1038/nature08910
  • Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, Schwarz JP, Spence H, Futo K, Timpson P, et al. N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 2012; 199:527-44; PMID:23091069; http://dx.doi.org/10.1083/jcb.201203025
  • Parekh A, Weaver AM. Regulation of cancer invasiveness by the physical extracellular matrix environment. Cell Adh Migr 2009; 3:288-92; PMID:19458499; http://dx.doi.org/10.4161/cam.3.3.8888
  • Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, Guelcher SA, Weaver AM. Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 2008; 18:1295-9; PMID:18718759; http://dx.doi.org/10.1016/j.cub.2008.07.090
  • Roberts MS, Woods AJ, Shaw PE, Norman JC. ERK1 associates with α(v)β 3 integrin and regulates cell spreading on vitronectin. J Biol Chem 2003; 278:1975-85; PMID:12393886; http://dx.doi.org/10.1074/jbc.M208607200
  • Roberts M, Barry S, Woods A, van der Sluijs P, Norman J. PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 2001; 11:1392-402; PMID:11566097; http://dx.doi.org/10.1016/S0960-9822(01)00442-0
  • Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, Ostrowski M, Thery C. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 2012; 72:4920-30; PMID:22865453; http://dx.doi.org/10.1158/0008-5472.CAN-12-0925
  • Baldassarre M, Ayala I, Beznoussenko G, Giacchetti G, Machesky LM, Luini A, Buccione R. Actin dynamics at sites of extracellular matrix degradation. Eur J Cell Biol 2006; 85:1217-31; PMID:17010475; http://dx.doi.org/10.1016/j.ejcb.2006.08.003
  • Poincloux R, Lizarraga F, Chavrier P. Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 2009; 122:3015-24; PMID:19692588; http://dx.doi.org/10.1242/jcs.034561
  • Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 2006; 66:3034-43; PMID:16540652; http://dx.doi.org/10.1158/0008-5472.CAN-05-2177
  • Clark ES, Whigham AS, Yarbrough WG, Weaver AM. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res 2007; 67:4227-35; PMID:17483334; http://dx.doi.org/10.1158/0008-5472.CAN-06-3928
  • Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, D'Souza-Schorey C, Chavrier P. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of cdc42 and rhoA. J Cell Biol 2008; 181:985-98; PMID:18541705; http://dx.doi.org/10.1083/jcb.200709076
  • Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, Schwarz JP, Spence H, Futo K, Timpson P, et al. N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 2012; 199:527-44; PMID:23091069; http://dx.doi.org/10.1083/jcb.201203025
  • Muller PAJ, Caswell PY, Doyle B, Iwanicki MP, Tan EH, Karim S, Lukashchuk N, Gillespie DA, Ludwig RL, Gosselin P, et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 2009; 139:1327-41; PMID:20064378; http://dx.doi.org/10.1016/j.cell.2009.11.026

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.