A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages

Journal of Cell Science

Volumn 126, Issue 13, 2013, Pages 2820-2833

  Wiesner , Christiane ^a   El Azzouzi, Karim ^a   Linder, Stefan ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Cell invasion; Extracellular matrix; MT1 MMP; Podosomes; RabGTPases

Indexed keywords

MATRIX METALLOPROTEINASE; RAB PROTEIN; RAB14 PROTEIN; RAB22A PROTEIN; RAB5A PROTEIN; RAB8A PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL INVASION; CELL MIGRATION; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MACROPHAGE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

CELL INVASION; EXTRACELLULAR MATRIX; MT1-MMP; PODOSOMES; RABGTPASES;

CELL MOVEMENT; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASE 14; MOLECULAR IMAGING; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTEOLYSIS; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; TRANSPORT VESICLES;

EID: 84880662092     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122358     Document Type: Article

References (77)

1. Agola, J. O., Jim, P. A., Ward, H. H., Basuray, S. and Wandinger-Ness, A. (2011). Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin. Genet. 80, 305-318.
2. Barbarin, A. and Frade, R. (2011). Procathepsin L secretion, which triggers tumour progression, is regulated by Rab4a in human melanoma cells. Biochem. J. 437, 97-107.
3. Barbolina, M. V. and Stack, M. S. (2008). Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Semin. Cell Dev. Biol. 19, 24-33.
4. Bravo-Cordero, J. J., Marrero-Diaz, R., Megias, D., Gems, L., Garcia-Grande, A., Garcia, M. A., Arroyo, A. G.Montoya, M. C. (2007). MT1-MMP preinvasive activity is regulatedby a novel Rab8-dependent exocytic pathway. EMBO J. 26, 1499-1510.
5. Bravo-Cordero, J. J., Hodgson, L. and Condeelis, J. (2012). Directed cell invasion and migration during metastasis. Curr. Opin. Cell Biol. 24, 277-283.
6. Burns, S., Thrasher, A. J., Blundell, M. P., Machesky, L. and Jones, G. E. (2001). Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142-1149.
7. Caswell, P. T., Vadrevu, S. and Norman, J. C. (2009). Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853.
8. Chen, W. T., Yeh, Y. and Nakahara, H. (1994). An in vitro cell invasion assay: determination of cell surface proteolytic activity that degrades extracellular matrix. J. Tissue Cult. Methods 16, 177-181.
9. Christoforidis, S., McBride, H. M., Burgoyne, R. D. and Zerial, M. (1999). The Rab5 effector EEA1 is a core component of endosome docking. Nature 397, 621-625.
10. Delaisse, J. M., Andersen, T. L., Engsig, M. T., Henriksen, K., Troen, T. and Blavier, L. (2003). Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc. Res. Tech. 61,504-513.
11. Destaing, O., Saltel, F., Geminard, J. C., Jurdic, P. and Bard, F. (2003). Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin- green fluorescent protein. Mol. Biol. Cell 14, 407-416.
12. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M. and Sato,H.(2003). Cleavage of syndecan-1 by membranetype matrixmetalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764-40770.
13. Friedl, P. and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
14. Friedl, P. and Wolf, K. (2008). Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 68, 7247-7249.
15. Friedl, P. and Wolf, K. (2009). Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev. 28, 129-135.
16. Frittoli, E., Palamidessi, A., Disanza, A. and Scita, G. (2011). Secretory and endo/ exocytic trafficking in invadopodia formation: the MT1-MMP paradigm. Eur. J. Cell Biol. 90, 108-114.
17. Gitler, A. D., Bevis, B. J., Shorter, J., Strathearn, K. E., Hamamichi, S., Su, L. J., Caldwell, K. A., Caldwell, G. A., Rochet, J. C., McCaffery, J. M. et al. (2008). The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc. Natl. Acad. Sci. USA 105, 145-150.
18. Grant, B. D. and Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608.
19. Guiet, R., Van Goethem, E., Cougoule, C., Balor, S., Valette, A., Al Saati, T., Lowell, C. A., Le Cabec, V. and Maridonneau-Parini, I. (2011). The process of macrophage migration promotes matrix metalloproteinase-independent invasion by tumor cells. J. Immunol. 187, 3806-3814.
20. Henry, L. and Sheff, D. R. (2008). Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol. Biol. Cell 19, 2059-2068.
21. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W. and Weiss, S. J. (2003). Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45.
22. Humphries, M. J. (2009). Cell adhesion assays. Methods Mol. Biol. 522, 203-210.
23. Hutagalung, A. H. and Novick, P. J. (2011). Role ofRab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119-149.
24. Itoh, Y. and Seiki, M. (2004). MT1-MMP: an enzyme with multidimensional regulation. Trends Biochem. Sci. 29, 285-289.
25. Junutula, J. R., De Maziere, A. M., Peden, A. A., Ervin, K. E., Advani, R. J., van Dijk, S. M., Klumperman, J. and Scheller, R. H. (2004). Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol. Biol. Cell 15, 2218-2229.
26. Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H. and Seiki, M. (2001). Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153, 893-904.
27. Kauppi, M., Simonsen, A., Bremnes, B., Vieira, A., Callaghan, J., Stenmark, H. and Olkkonen, V. M. (2002). The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J. Cell Sci. 115, 899-911.
28. Kopp, P., Lammers, R., Aepfelbacher, M., Woehlke, G., Rudel, T., Machuy, N., Steffen, W. and Linder, S. (2006). The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol. Biol. Cell 17, 2811-2823.
29. Lammermann, T. and Sixt, M. (2009). Mechanical modes of 'amoeboid' cell migration. Curr. Opin. Cell Biol. 21, 636-644.
30. Lehti, K., Lohi, J., Valtanen, H. and Keski-Oja, J. (1998). Proteolytic processing of membrane-type-1 matrix metalloproteinase is associated with gelatinase A activation at the cell surface. Biochem. J. 334, 345-353.
31. Ley, K., Laudanna, C., Cybulsky, M. I. and Nourshargh, S. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol.7, 678689.
32. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117.
33. Linder, S., Nelson, D., Weiss, M. and Aepfelbacher, M. (1999). Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA 96, 9648-9653.
34. Linder, S., Wiesner, C. and Himmel, M. (2011). Degrading devices: invadosomes in proteolytic cell invasion. Annu. Rev. Cell Dev. Biol. 27, 185-211.
35. Linford, A., Yoshimura, S., Nunes Bastos, R., Langemeyer, L., Gerondopoulos, A., Rigden, D. J. and Barr, F. A. (2012). Rab14 and its exchange factor FAM116 link endocytic recycling and adherens junction stability in migrating cells. Dev. Cell 22, 952-966.
36. Liu, S. S., Chen, X. M., Zheng, H. X., Shi, S. L. and Li, Y. (2011). Knockdown of Rab5a expression decreases cancer cell motility and invasion through integrin-mediated signaling pathway. J. Biomed. Sci. 18, 58.
37. Matias-Roman, S., Galvez, B. G., Genis, L., Yanez-Mo, M., de la Rosa, G., Sanchez-Mateos,P., Sanchez-Madrid, F. and Arroyo, A. G. (2005). Membrane type 1-matrix metalloproteinaseis involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood 105, 39563964.
38. Meyer, A. S., Hughes-Alford, S. K., Kay, J. E., Castillo, A., Wells, A., Gertler, F. B.and Lauffenburger, D. A. (2012). 2D protrusion but not motility predicts growth factor-induced cancer cell migration in 3D collagen. J. Cell Biol. 197, 721-729.
39. Murphy, D. A. and Courtneidge, S. A. (2011). The 'ins' and 'outs' ofpodosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426.
40. Nakada, M., Miyamori, H., Yamashita, J. and Sato, H. (2003). Testican 2 abrogates inhibition of membrane-type matrix metalloproteinases by other testican family proteins. Cancer Res. 63, 3364-3369.
41. Nourshargh, S., Hordijk, P. L. and Sixt, M. (2010). Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 11, 366-378.
42. Olkkonen, V. M., Dupree, P., Killisch, I., Lutcke, A., Zerial, M. and Simons, K (1993). Molecular cloning and subcellular localization of three GTP-binding proteins ofthe rab subfamily. J. Cell Sci. 106, 1249-1261.
43. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J. A. and Ivaska, J. (2006). Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173, 767-780.
44. Petrie, R. J., Gavara, N., Chadwick, R. S. and Yamada, K. M. (2012). Nonpolarized signaling reveals two distinct modes of 3D cell migration. J. Cell Biol. 197, 439-455.
45. Pixley, F. J. (2012). Macrophage migration and its regulation by CSF-1. Int. J. Cell Biol. 2012, 501962.
46. Poincloux, R., Lizarraga, F. and Chavrier, P. (2009). Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122, 3015-3024.
47. Remacle, A., Murphy, G. and Roghi, C. (2003). Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J. Cell Sci. 116, 3905-3916.
48. Remacle, A. G., Rozanov, D. V., Fugere, M., Day, R. and Strongin, A. Y. (2006). Furin regulates the intracellular activation and the uptake rate of cell surface- associated MT1-MMP. Oncogene 25, 5648-5655.
49. Remacle, A. G., Golubkov, V. S., Shiryaev, S. A., Dahl, R., Stebbins, J. L., Chernov,A. V., Cheltsov, A. V., Pellecchia, M. and Strongin, A. Y. (2012). Novel MT1- MMP small-molecule inhibitors based on insights into hemopexin domain function in tumor growth. Cancer Res. 72, 2339-2349.
50. Sabeh, F., Shimizu-Hirota, R. and Weiss, S. J. (2009). Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185, 11-19.
51. Sakurai-Yageta, M., Recchi, C., Le Dez, G., Sibarita, J. B., Daviet, L., Camonis, J., D'Souza-Schorey, C. and Chavrier, P. (2008). The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181, 985-998.
52. Sato, H., Kinoshita, T., Takino, T., Nakayama, K. andSeiki, M. (1996). Activationof a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP)-2. FEBS Lett. 393, 101-104.
53. Schlierf, B., Fey, G. H., Hauber, J., Hocke, G. M. and Rosorius, O. (2000). Rab11bis essential forrecyclingoftransferrintotheplasmamembrane. Exp. CellRes. 259, 257265.
54. Schwartz, S. L., Cao, C., Pylypenko, O., Rak, A. and Wandinger-Ness, A. (2007). Rab GTPases at a glance. J. Cell Sci. 120, 3905-3910.
55. Simpson, J. C., Griffiths, G., Wessling-Resnick, M., Fransen, J. A., Bennett, H. and Jones, A. T. (2004). A role for the small GTPase Rab21 in the early endocytic pathway. J. Cell Sci. 117, 6297-6311.
56. Sithu, S. D., English, W. R., Olson, P., Krubasik, D., Baker, A. H., Murphy, G. and D'Souza, S. E. (2007). Membrane-type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J. Biol. Chem. 282, 25010-25019.
57. Sonnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J. and Zerial, M. (2000).Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
58. Stanton, H., Gavrilovic, J., Atkinson, S. J., d'Ortho, M. P., Yamada, K. M., Zardi, L. and Murphy, G. (1998). The activation of ProMMP-2 (gelatinase A) by HT1080 fibrosarcoma cells is promoted by culture on a fibronectin substrate and is concomitant with an increase in processing of MT1-MMP (MMP-14) to a 45 kDa form. J. Cell Sci. 111, 2789-2798.
59. Steffen, A., Le Dez, G., Poincloux, R., Recchi, C., Nassoy, P., Rottner, K., Galli, T. and Chavrier, P. (2008). MT1-MMP-dependent invasion is regulated by TI-VAMP/ VAMP7. Curr. Biol. 18, 926-931.
60. Stein, M. P., Dong, J. and Wandinger-Ness, A. (2003). Rab proteins and endocytic trafficking: potential targets for therapeutic intervention. Adv. Drug Deliv. Rev. 55, 1421-1437.
61. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
62. Stenmark, H., Parton, R. G., Steele-Mortimer, O., Lutcke, A., Gruenberg, J. and Zerial, M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296.
63. Tatin, F., Varon, C., Genot, E. and 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.
64. van der Sluijs, P., Mohrmann, K., Deneka, M. and Jongeneelen, M. (2001). Expression and properties of Rab4 and its effector rabaptin-4 in endocytic recycling. Methods Enzymol. 329, 111-119.
65. Van Goethem, E., Poincloux, R., Gauffre, F., Maridonneau-Parini, I. and Le Cabec, V. (2010). Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. 184, 1049-1061.
66. van Hinsbergh, V. W., Engelse, M. A. and Quax, P. H. (2006). Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 26,716-728.
67. Verollet, C., Charriere, G. M., Labrousse, A., Cougoule, C., Le Cabec, V. and Maridonneau-Parini, I. (2011). Extracellular proteolysis in macrophage migration: losing grip for a breakthrough. Eur. J. Immunol. 41, 2805-2813.
68. Wiesner, C., Faix, J., Himmel, M., Bentzien, F. and Linder, S. (2010). KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 116, 1559-1569.
69. Williams, K. C. and Coppolino, M. G. (2011). 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. 286, 43405-43416.
70. Wolf, K. and Friedl, P. (2005). Functional imaging ofpericellularproteolysis incancercell invasion. Biochimie. 87, 315-320.
71. Wolf, K. and Friedl, P. (2009). Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin. Exp. Metastasis 26, 289-298.
72. Wolf, K. and Friedl, P. (2011). Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21, 736-744.
73. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B. and Friedl, P. (2003). Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking ofpericellular proteolysis. J. Cell Biol. 160, 267-277.
74. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., Stack, M. S. and Friedl,P. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893-904.
75. Yamamoto, H., Koga, H., Katoh, Y., Takahashi, S., Nakayama, K. and Shin, H. W. (2010). Functional cross-talk between Rab14 and Rab4 through a dual effector, RUFY1/Rabip4. Mol. Biol. Cell 21, 2746-2755.
76. Yudowski, G. A., Puthenveedu, M. A., Henry, A. G. and von Zastrow, M. (2009). Cargo-mediated regulation of a rapid Rab4-dependent recycling pathway. Mol. Biol. Cell 20, 2774-2784.
77. Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.