Matrix architecture dictates three-dimensional migration modes of human macrophages: Differential involvement of proteases and podosome-like structures

Journal of Immunology

Volumn 184, Issue 2, 2010, Pages 1049-1061

  Van Goethem, Emeline ^a,b   Poincloux, Renaud ^a,b,c,d   Gauffre, Fabienne ^b   Maridonneau Parini, Isabelle ^a,b   Le Cabec, Véronique ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CNRS   (France)

^d INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; FIBRILLAR COLLAGEN; MATRIGEL; MATRIX METALLOPROTEINASE INHIBITOR; PROTEINASE; COLLAGEN; LAMININ; PEPTIDE HYDROLASE; PROTEOGLYCAN;

ARTICLE; CELL COMPOSITION; CYTOARCHITECTURE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MACROPHAGE MIGRATION; MESENCHYME; MONOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; TUMOR CELL; AMOEBA (LIFE CYCLE STAGE); CELL CULTURE; CELL MOTION; CELL SURFACE; CYTOLOGY; DRUG COMBINATION; DRUG EFFECT; MACROPHAGE; MESENCHYMAL STEM CELL; PHYSIOLOGY; ULTRASTRUCTURE;

AMOEBA; CELL MOVEMENT; CELL SURFACE EXTENSIONS; CELLS, CULTURED; COLLAGEN; COLLAGEN TYPE I; DRUG COMBINATIONS; EXTRACELLULAR MATRIX; HUMANS; LAMININ; MACROPHAGES; MESENCHYMAL STEM CELLS; MONOCYTES; PEPTIDE HYDROLASES; PROTEOGLYCANS;

EID: 76249088362     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902223     Document Type: Article

References (65)

1. Yiangou, Y., P. Facer, P. Durrenberger, I. P. Chessell, A. Naylor, C. Bountra, R. R. Banati, and P. Anand. 2006. COX-2, CB2 and P2X7- immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol. 6: 12-26.
2. Condeelis, J., and J. W. Pollard. 2006. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266.
3. Friedl, P., and B. Weigelin. 2008. Interstitial leukocyte migration and immune function. Nat. Immunol. 9: 960-969.
4. Mackay,C.R. 2008.Moving targets: cell migration inhibitors as new anti-inflammatory therapies. Nat. Immunol. 9: 988-998.
5. von Andrian, U. H., and C. R. Mackay. 2000. T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 343: 1020-1034.
6. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated.Nat. Rev. Immunol. 7: 678-689.
7. Kalluri, R. 2003. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3: 422-433.
8. Schindler, M., A. Nur-E-Kamal, I. Ahmed, J. Kamal, H. Y. Liu, N. Amor, A. S. Ponery, D. P. Crockett, T. H. Grafe, H. Y. Chung, et al. 2006. Living in three dimensions: 3D nanostructured environments for cell culture and regenerative medicine. Cell Biochem. Biophys. 45: 215-227.
9. Even-Ram, S., and K. M. Yamada. 2005. Cell migration in 3D matrix. Curr. Opin. Cell Biol. 17: 524-532.
10. Butcher, E. C. 1991. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67: 1033-1036.
11. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314.
12. Hooper, S., J. F. Marshall, and E. Sahai. 2006. Tumor cell migration in three dimensions. Methods Enzymol. 406: 625-643.
13. Doyle, A. D., F.W. Wang, K .Matsumoto, and K.M. Yamada. 2009. One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 184: 481-490.
14. Sahai, E. 2005. Mechanisms of cancer cell invasion. Curr. Opin. Genet. Dev. 15: 87-96.
15. Wolf, K., and P. Friedl. 2006. Molecular mechanisms of cancer cell invasion and plasticity. Br. J. Dermatol. 154(Suppl. 1): 11-15.
16. Sabeh, F., R. Shimizu-Hirota, and S. J. Weiss. 2009. Protease-dependent versus - independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185: 11-19.
17. Sahai, E., and C. J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5: 711-719.
18. Carragher, N. O., S. M. Walker, L. A. Scott Carragher, F. Harris, T. K. Sawyer, V. G. Brunton, B. W. Ozanne, and M. C. Frame. 2006. Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene 25: 5726-5740.
19. Larsen, M., V. V. Artym, J. A. Green, and K. M. Yamada. 2006. The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18: 463-471.
20. Wolf, K., I. Mazo, H. Leung, K. Engelke, U. H. von Andrian, E. I. Deryugina, A. Y. Strongin, E. B. Bröcker, and P. Friedl. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160: 267-277.
21. Sanz-Moreno, V., G. Gadea, J. Ahn, H. Paterson, P. Marra, S. Pinner, E. Sahai, and C. J. Marshall. 2008. Rac activation and inactivation control plasticity of tumor cell movement. Cell 135: 510-523.
22. Wolf, K., R. Müller, S. Borgmann, E. B. Bröcker, and P. Friedl. 2003. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 102: 3262-3269.
23. Gong, Y., E. Hart, A. Shchurin, and J. Hoover-Plow. 2008. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J. Clin. Invest. 118: 3012-3024.
24. Deguchi, J. O., E. Aikawa, P. Libby, J. R. Vachon, M. Inada, S. M. Krane, P. Whittaker, and M. Aikawa. 2005. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 112: 2708-2715.
25. Schneider, F., G. K. Sukhova, M. Aikawa, J. Canner, N. Gerdes, S. M. Tang, G. P. Shi, S. S. Apte, and P. Libby. 2008. Matrix-metalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation 117: 931-939.
26. Xiong, W., R. Knispel, J. MacTaggart, T. C. Greiner, S. J. Weiss, and B. T. Baxter. 2009. Membrane-type 1 matrix metalloproteinase regulates macrophage-dependent elastolytic activity and aneurysm formation in vivo. J. Biol. Chem. 284: 1765-1771.
27. Tomlinson, M. L., C. Garcia-Morales, M. Abu-Elmagd, and G. N. Wheeler. 2008. Three matrix metalloproteinases are required in vivo for macrophage migration during embryonic development. Mech. Dev. 125: 1059-1070.
28. Zhang, Y., X. T. Bai, K. Y. Zhu, Y. Jin, M. Deng, H. Y. Le, Y. F. Fu, Y. Chen, J. Zhu, A. T. Look, et al. 2008. In vivo interstitial migration of primitive macrophages mediated by JNK-matrix metalloproteinase 13 signaling in response to acute injury. J. Immunol. 181: 2155-2164.
29. Sakamoto, T., and M. Seiki. 2009. Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity. Genes Cells 14: 617-626.
30. Astarie-Dequeker, C., E. N. N'Diaye, V. Le Cabec, M. G. Rittig, J. Prandi, and I. Maridonneau-Parini. 1999. The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect. Immun. 67: 469-477.
31. Zaman, M. H., L. M. Trapani, A. L. Sieminski, D. Mackellar, H. Gong, R. D. Kamm, A. Wells, D. A. Lauffenburger, and P. Matsudaira. 2006. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA 103: 10889-10894.
32. Lizárraga, F., R. Poincloux, M. Romao, G. Montagnac, G. Le Dez, I. Bonne, G. Rigaill, G. Raposo, and P. Chavrier. 2009. Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res. 69: 2792-2800.
33. Rossner, M., and K. M. Yamada. 2004. What's in a picture? The temptation of image manipulation. J. Cell Biol. 166: 11-15.
34. Wolf, K., and P. Friedl. 2009. Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin. Exp. Metastasis 26: 289-298.
35. LeBleu, V. S., B. Macdonald, and R. Kalluri. 2007. Structure and function of basement membranes. Exp. Biol. Med. (Maywood) 232: 1121-1129.
36. Sabeh, F., X. Y. Li, T. L. Saunders, R. G. Rowe, and S. J. Weiss. 2009. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J. Biol. Chem. 284: 23001-23011.
37. Yoshida, D., and A. Teramoto. 2007. The use of 3-D culture in peptide hydrogel for analysis of discoidin domain receptor 1-collagen interaction. Cell Adh. Migr. 1: 92-98.
38. Stratman, A. N., W. B. Saunders, A. Sacharidou, W. Koh, K. E. Fisher, D. C. Zawieja, M. J. Davis, and G. E. Davis. 2009. Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices. Blood 114: 237-247.
39. Friedl, P., and K. Wolf. 2008. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 68: 7247-7249.
40. Fackler, O. T., and R. Grosse. 2008. Cell motility through plasma membrane blebbing. J. Cell Biol. 181: 879-884.
41. Charras, G., and E. Paluch. 2008. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 9: 730-736.
42. Féréol, S., R. Fodil, B. Labat, S. Galiacy, V. M. Laurent, B. Louis, D. Isabey, and E. Planus. 2006. Sensitivity of alveolar macrophages to substrate mechanical and adhesive properties. Cell Motil. Cytoskeleton 63: 321-340.
43. Guarnieri, D., S. Battista, A. Borzacchiello, L. Mayol, E. De Rosa, D. R. Keene, L. Muscariello, A. Barbarisi, and P. A. Netti. 2007. Effects of fibronectin and laminin on structural, mechanical and transport properties of 3D collageneous network. J. Mater. Sci. Mater. Med. 18: 245-253.
44. Linder, S., and M. Aepfelbacher. 2003. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 13: 376-385.
45. Evans, J. G., and P. Matsudaira. 2006. Structure and dynamics of macrophage podosomes. Eur. J. Cell Biol. 85: 145-149.
46. Buccione, R., G. Caldieri, and I. Ayala. 2009. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev. 28: 137-149.
47. Gimona, M., R. Buccione, S. A. Courtneidge, and S. Linder. 2008. Assembly and biological role of podosomes and invadopodia. Curr. Opin. Cell Biol. 20: 235-241.
48. Clark, E. S., A. S. Whigham, W. G. Yarbrough, and A. M. Weaver. 2007. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67: 4227-4235.
49. Discher, D. E., P. Janmey, and Y. L. Wang. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143.
50. Berrier, A. L., and K. M. Yamada. 2007. Cell-matrix adhesion. J. Cell. Physiol. 213: 565-573.
51. Bowden, E. T., E. Onikoyi, R. Slack, A. Myoui, T. Yoneda, K. M. Yamada, and S. C. Mueller. 2006. Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp. Cell Res. 312: 1240-1253.
52. Spinardi, L., and P. C. Marchisio. 2006. Podosomes as smart regulators of cellular adhesion. Eur. J. Cell Biol. 85: 191-194.
53. Block, M. R., C. Badowski, A. Millon-Fremillon, D. Bouvard, A. P. Bouin, E. Faurobert, D. Gerber-Scokaert, E. Planus, and C. Albiges-Rizo. 2008. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur. J. Cell Biol. 87: 491-506.
54. Abram, C. L., and C. A. Lowell. 2009. The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 27: 339-362.
55. 1 is required for the invasive behaviour but not proliferation of squamous cell carcinoma cells in vivo. Br. J. Cancer 92: 102-112.
56. Friedl, P., and K. Wolf. 2009. Proteolytic interstitial cell migration: a five-step process. Cancer Metastasis Rev. 28: 129-135.
57. Lämmermann, T., B. L. Bader, S. J. Monkley, T. Worbs, R. Wedlich-Söldner, K. Hirsch, M. Keller, R. Förster, D. R. Critchley, R. Fässler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453: 51-55.
58. Denys, H., G. Braems, K. Lambein, P. Pauwels, A. Hendrix, A. De Boeck, V. Mathieu, M. Bracke, and O. De Wever. 2009. The extracellular matrix regulates cancer progression and therapy response: implications for prognosis and treatment. Curr. Pharm. Des. 15: 1373-1384.
59. Geiger, B., J. P. Spatz, and A. D. Bershadsky. 2009. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10: 21-33.
60. Collin, O., P. Tracqui, A. Stephanou, Y. Usson, J. Clément- Lacroix, and E. Planus. 2006. Spatiotemporal dynamics of actin-rich adhesion microdomains: influence of substrate flexibility. J. Cell Sci. 119: 1914-1925.
61. Collin, O., S. Na, F. Chowdhury, M. Hong, M. E. Shin, F. Wang, and N. Wang. 2008. Self-organized podosomes are dynamic mechanosensors. Curr. Biol. 18: 1288-1294.
62. Cukierman, E., R. Pankov, D. R. Stevens, and K. M. Yamada. 2001. Taking cell-matrix adhesions to the third dimension. Science 294: 1708-1712.
63. Tu, C., C. F. Ortega-Cava, G. Chen, N. D. Fernandes, D. Cavallo-Medved, B. F. Sloane, V. Band, and H. Band. 2008. Lysosomal cathepsin B participates in the podosome-mediated extracellular matrix degradation and invasion via secreted lysosomes in v-Src fibroblasts. Cancer Res. 68: 9147-9156.
64. Baron, R. 1989. Polarity and membrane transport in osteoclasts. Connect. Tissue Res. 20: 109-120.
65. Cougoule, C., S. Carréno, J. Castandet, A. Labrousse, C. Astarie-Dequeker, R. Poincloux, V. Le Cabec, and I. Maridonneau-Parini. 2005. Activation of the lysosome-associated p61Hck isoform triggers the biogenesis of podosomes. Traffic 6: 682-694.