Rho/ROCK pathway inhibition by the CDK inhibitor p27kip1 participates in the onset of macrophage 3D-mesenchymal migration

Journal of Cell Science

Volumn 127, Issue 18, 2014, Pages 4009-4023

  Gui, Philippe ^a,b   Labrousse, Arnaud ^a,b   van Goethem, Emeline ^a,b   Besson, Arnaud ^c   Maridonneau Parini, Isabelle ^a,b   Le Cabec, Véronique ^a,b  

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

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

3D migration; Amoeboid; CDKN1B; Macrophage; Mesenchymal; P27kip1; Rho ROCK pathway

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FIBRILLAR COLLAGEN; RHO KINASE; SMALL INTERFERING RNA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CYTOPLASM; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MACROPHAGE; MESENCHYMAL TO AMOEBOID MIGRATION; MESENCHYME CELL; MONOCYTE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; UPREGULATION; ANIMAL; CELL CULTURE; CELL MOTION; CYTOLOGY; ENZYMOLOGY; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P27; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES;

EID: 84907050547     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.150987     Document Type: Article

References (51)

1. Baldassarre, G., Belletti, B., Nicoloso, M. S., Schiappacassi, M., Vecchione, A., Spessotto, P., Morrione, A., Canzonieri, V. and Colombatti, A. (2005). p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7, 51-63.
2. Berton, S., Belletti, B., Wolf, K., Canzonieri, V., Lovat, F., Vecchione, A., Colombatti, A., Friedl, P. and Baldassarre, G. (2009). The tumor suppressor functions of p27(kip1) include control of the mesenchymal/amoeboid transition. Mol. Cell. Biol. 29, 5031-5045.
3. Besson, A., Assoian, R. K. and Roberts, J. M. (2004a). Regulation of the cytoskeleton: an oncogenic function for CDK inhibitors? Nat. Rev. Cancer 4, 948-955.
4. Besson, A., Gurian-West, M., Schmidt, A., Hall, A. and Roberts, J. M. (2004b). p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18, 862-876.
5. Besson, A., Gurian-West, M., Chen, X., Kelly-Spratt, K. S., Kemp, C. J. and Roberts, J. M. (2006). A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev. 20, 47-64.
6. Besson, A., Hwang, H. C., Cicero, S., Donovan, S. L., Gurian-West, M., Johnson, D., Clurman, B. E., Dyer, M. A. and Roberts, J. M. (2007). Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev. 21, 1731-1746.
7. Biswas, S. K., Gangi, L., Paul, S., Schioppa, T., Saccani, A., Sironi, M., Bottazzi, B., Doni, A., Vincenzo, B., Pasqualini, F. et al. (2006). A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 107, 2112-2122.
8. Carragher, N. O. (2006). Calpain inhibition: a therapeutic strategy targeting multiple disease states. Curr. Pharm. Des. 12, 615-638.
9. Carragher, N. O., Walker, S. M., Scott Carragher, L. A., Harris, F., Sawyer, T. K., Brunton, V. G., Ozanne, B. W. and Frame, M. C. (2006). Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene 25, 5726-5740.
10. Cougoule, C., Le Cabec, V., Poincloux, R., Al Saati, T., Me´ge, J. L., Tabouret, G., Lowell, C. A., Laviolette-Malirat, N. and Maridonneau-Parini, I. (2010). Three-dimensional migration of macrophages requires Hck for podosome organization and extracellular matrix proteolysis. Blood 115, 1444-1452.
11. Cougoule, C., Van Goethem, E., Le Cabec, V., Lafouresse, F., Dupre?, L., Mehraj, V., Me´ge, J. L., Lastrucci, C. and Maridonneau-Parini, I. (2012). Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and to migrate in 3D environments. Eur. J. Cell Biol. 91
12. Denicourt, C., Saenz, C. C., Datnow, B., Cui, X. S. and Dowdy, S. F. (2007). Relocalized p27Kip1 tumor suppressor functions as a cytoplasmic metastatic oncogene in melanoma. Cancer Res. 67, 9238-9243.
13. Doyle, A. D., Wang, F. W., Matsumoto, K., Yamada, K. M. (2009). Onedimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 184, 481-490.
14. DuFort, C. C., Paszek, M. J. and Weaver, V. M. (2011). Balancing forces: architectural control ofmechanotransduction. Nat. Rev. Mol. Cell Biol. 12, 308-319.
15. Elkington, P. T. and Friedland, J. S. (2006). Matrix metalloproteinases in destructive pulmonary pathology. Thorax 61, 259-266.
16. Even-Ram, S. and Yamada, K. M. (2005). Cell migration in 3D matrix. Curr. Opin. Cell Biol. 17, 524-532.
17. Fero, M. L., Rivkin, M., Tasch, M., Porter, P., Carow, C. E., Firpo, E., Polyak, K., Tsai, L. H., Broudy, V., Perlmutter, R. M. et al. (1996). A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell 85, 733-744.
18. Friedl, P. and Weigelin, B. (2008). Interstitial leukocyte migration and immune function. Nat. Immunol. 9, 960-969.
19. Friedl, P. and Wolf, K. (2003). Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem. Soc. Symp. 70, 277-285.
20. Fuster, J. J., Gonza´lez-Navarro, H., Vinue?, A., Molina-Sa'nchez, P., Andre´s-Manzano, M. J., Nakayama, K. I., Nakayama, K., Di´ez-Juan, A., Bernad, A., Rodri´guez, C. et al. (2011). Deficient p27 phosphorylation at serine 10 increases macrophage foam cell formation and aggravates atherosclerosis through a proliferation-independent mechanism. Arterioscler. Thromb. Vasc. Biol. 31, 2455-2463.
21. 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.
22. Guiet, R., Ve´rollet, C., Lamsoul, I., Cougoule, C., Poincloux, R., Labrousse, A., Calderwood, D. A., Glogauer, M., Lutz, P. G. and Maridonneau-Parini, I. (2012). Macrophage mesenchymal migration requires podosome stabilization by filamin A. J. Biol. Chem. 287, 13051-13062.
23. Ishida, N., Kitagawa, M., Hatakeyama, S. and Nakayama, K. (2000). Phosphorylation at serine 10, a major phosphorylation site of p27(Kip1), increases its protein stability. J. Biol. Chem. 275, 25146-25154.
24. Ishigami, S., Ueno, S., Nishizono, Y., Matsumoto, M., Kurahara, H., Arigami, T., Uchikado, Y., Setoyama, T., Arima, H., Yoshiaki, K. et al. (2011). Prognostic impact of CD168 expression in gastric cancer. BMC Cancer 11, 106.
25. Jevnikar, Z., Mirkovic´, B., Fonovic´, U. P., Zidar, N., Sˇvajger, U. and Kos, J. (2012). Three-dimensional invasion of macrophages is mediated by cysteine cathepsins in protrusive podosomes. Eur. J. Immunol. 42, 3429-3441.
26. Kalluri, R. (2003). Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3, 422-433.
27. Kawauchi, T., Chihama, K., Nabeshima, Y. and Hoshino, M. (2006). Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8, 17-26.
28. Kotake, Y., Nakayama, K., Ishida, N. and Nakayama, K. I. (2005). Role of serine 10 phosphorylation in p27 stabilization revealed by analysis of p27 knock-in mice harboring a serine 10 mutation. J. Biol. Chem. 280, 1095-1102.
29. Luster, A. D., Alon, R. and von Andrian, U. H. (2005). Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6, 1182-1190.
30. Mackay, C. R. (2008). Moving targets: cell migration inhibitors as new antiinflammatory therapies. Nat. Immunol. 9, 988-998.
31. Maruotti, N., Cantatore, F. P., Crivellato, E., Vacca, A. and Ribatti, D. (2007). Macrophages in rheumatoid arthritis. Histol. Histopathol. 22, 581-586.
32. Nagahara, H., Vocero-Akbani, A. M., Snyder, E. L., Ho, A., Latham, D. G., Lissy, N. A., Becker-Hapak, M., Ezhevsky, S. A. and Dowdy, S. F. (1998). Transduction of full-length TAT fusion proteins into mammalian cells: TATp27Kip1 induces cell migration. Nat. Med. 4, 1449-1452.
33. Pollard, J. W. (2009). Trophic macrophages in development and disease. Nat. Rev. Immunol. 9, 259-270.
34. Porta, C., Riboldi, E., Totaro, M. G., Strauss, L., Sica, A. and Mantovani, A. (2011). Macrophages in cancer and infectious diseases: the 'good' and the 'bad'. Immunotherapy 3, 1185-1202.
35. Qualls, J. E. and Murray, P. J. (2010). A double agent in cancer: stopping macrophages wounds tumors. Nat. Med. 16, 863-864.
36. Rodier, G., Montagnoli, A., Di Marcotullio, L., Coulombe, P., Draetta, G. F., Pagano, M. and Meloche, S. (2001). p27 cytoplasmic localization is regulated by phosphorylation on Ser10 and is not a prerequisite for its proteolysis. EMBO J. 20, 6672-6682.
37. Ruhrberg, C. and De Palma, M. (2010). A double agent in cancer: deciphering macrophage roles in human tumors. Nat. Med. 16, 861-862.
38. Sahai, E. and Marshall, C. J. (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5, 711-719.
39. Schindler, M., Nur-E-Kamal, A., Ahmed, I., Kamal, J., Liu, H. Y., Amor, N., Ponery, A. S., Crockett, D. P., Grafe, T. H., Chung, H. Y. et al. (2006). Living in three dimensions: 3D nanostructured environments for cell culture and regenerative medicine. Cell Biochem. Biophys. 45, 215-227.
40. Serres, M. P., Zlotek-Zlotkiewicz, E., Concha, C., Gurian-West, M., Daburon, V., Roberts, J. M. and Besson, A. (2011). Cytoplasmic p27 is oncogenic and cooperates with Ras both in vivo and in vitro. Oncogene 30, 2846-2858.
41. Shabo, I., Sta˚l, O., Olsson, H., Dore´, S. and Svanvik, J. (2008). Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int. J. Cancer 123, 780-786.
42. Sherr, C. J. and Roberts, J. M. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
43. Takai, Y., Sasaki, T. and Matozaki, T. (2001). Small GTP-binding proteins. Physiol. Rev. 81, 153-208.
44. Tanaka, T., Nishimura, D., Wu, R. C., Amano, M., Iso, T., Kedes, L., Nishida, H., Kaibuchi, K. and Hamamori, Y. (2006). Nuclear Rho kinase, ROCK2, targets p300 acetyltransferase. J. Biol. Chem. 281, 15320-15329.
45. Ueno, S., Sakoda, M., Kurahara, H., Iino, S., Minami, K., Ando, K., Mataki, Y., Maemura, K., Ishigami, S., Shinchi, H. et al. (2011). Safety and efficacy of early postoperative hyperbaric oxygen therapy with restriction of transfusions in patients with HCC who have undergone partial hepatectomy. Langenbecks Arch. Surg. 396, 99-106.
46. Van Goethem, E., Poincloux, R., Gauffre, F., Maridonneau-Parini, I. and Le Cabec, V. (2010). Matrix architecture dictates three-dimensional migrationmodes of human macrophages: differential involvement of proteases and podosome-like structures. J. Immunol. 184, 1049-1061.
47. Van Goethem, E., Guiet, R., Balor, S., Charrie´re, G. M., Poincloux, R., Labrousse, A., Maridonneau-Parini, I. and Le Cabec, V. (2011). Macrophage podosomes go 3D. Eur. J. Cell Biol. 90, 224-236.
48. Vlach, J., Hennecke, S. and Amati, B. (1997). Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16, 5334-5344.
49. Weber, C., Zernecke, A. and Libby, P. (2008). The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat. Rev. Immunol. 8, 802-815.
50. Wiesner, C., El Azzouzi, K. and Linder, S. (2013). A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and three-dimensional invasion of macrophages. J. Cell Sci. 126, 2820-2833.
51. Wiesner, C., Le-Cabec, V., El Azzouzi, K., Maridonneau-Parini, I. and Linder, S. (2014). Podosomes in space: Macrophage migration and matrix degradation in 2D and 3D settings. Cell Adh. Migr. 8, 8.