Regulation of invadopodia formation and activity by CD147

Journal of Cell Science

Volumn 125, Issue 3, 2012, Pages 777-788

  Daniel Grass, G ^a   Bratoeva, Momka ^a   Toole, Bryan P ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Breast cancer; Cd147; Invadopodia; Invasion; MT1 MMP (MMP14)

Indexed keywords

CD147 ANTIGEN; MATRIX METALLOPROTEINASE 14;

ARTICLE; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL STRUCTURE; CELL TRANSFORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INVADOPODIA; LIPID RAFT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION;

ANTIGENS, CD147; BASE SEQUENCE; BREAST; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL SURFACE EXTENSIONS; EPITHELIAL CELLS; FEMALE; HUMANS; MATRIX METALLOPROTEINASE 14; MEMBRANE MICRODOMAINS; NEOPLASM INVASIVENESS; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84858135267     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.097956     Document Type: Article

References (61)

1. Annabi, B., Lachambre, M., Bousquet-Gagnon, N., Page, M., Gingras, D. and Beliveau, R. (2001). Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem. J. 353, 547-553.
2. Artym, V. V., Zhang, Y., Seillier-Moiseiwitsch, F., Yamada, K. M. and Mueller, S. C. (2006). Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 66, 3034-3043.
3. Artym, V. V., Yamada, K. M. and Mueller, S. C. (2009). ECM degradation assays for analyzing local cell invasion. Methods Mol. Biol. 522, 211-219.
4. Belton, R. J., Jr, Chen, L., Mesquita, F. S. and Nowak, R. A. (2008). Basigin-2 is a cell surface receptor for soluble basigin ligand. J. Biol. Chem. 283, 17805-17814.
5. Berditchevski, F., Chang, S., Bodorova, J. and Hemler, M. E. (1997). Generation of monoclonal antibodies to integrin-associated proteins. Evidence that alpha3beta1 complexes with EMMPRIN/basigin/OX47/M6. J. Biol. Chem. 272, 29174-29180.
6. Biswas, C., Zhang, Y., DeCastro, R., Guo, H., Nakamura, T., Kataoka, H. and Nabeshima, K. (1995). The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res. 55, 434-439.
7. Caudroy, S., Polette, M., Nawrocki-Raby, B., Cao, J., Toole, B. P., Zucker, S. and Birembaut, P. (2002). Emmprin-mediated MMP regulation in tumor and endothelial cells. Clin. Exp. Metastasis 19, 697-702.
8. Clark, E. S., Whigham, A. S., Yarbrough, W. G. and Weaver, A. M. (2007). Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res. 67, 4227-4235.
9. Curtin, K. D., Meinertzhagen, I. A. and Wyman, R. J. (2005). Basigin (EMMPRIN/CD147) interacts with integrin to affect cellular architecture. J. Cell Sci. 118, 2649-2660.
10. Davidson, B., Konstantinovsky, S., Nielsen, S., Dong, H. P., Berner, A., Vyberg, M. and Reich, R. (2004). Altered expression of metastasis-associated and regulatory molecules in effusions from breast cancer patients: a novel model for tumor progression. Clin. Cancer Res. 10, 7335-7346.
11. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L. and Yang, J. (2011). Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386.
12. Egawa, N., Koshikawa, N., Tomari, T., Nabeshima, K., Isobe, T. and Seiki, M. (2006). Membrane type 1 matrix metalloproteinase (MT1-MMP/MMP-14) cleaves and releases a 22-kDa extracellular matrix metalloproteinase inducer (EMMPRIN) fragment from tumor cells. J. Biol. Chem. 281, 37576-37585.
13. Ellis, S. M., Nabeshima, K. and Biswas, C. (1989). Monoclonal antibody preparation and purification of a tumor cell collagenase-stimulatory factor. Cancer Res. 49, 3385-3391.
14. Eyster, C. A., Higginson, J. D., Huebner, R., Porat-Shliom, N., Weigert, R., Wu, W. W., Shen, R. F. and Donaldson, J. G. (2009). Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 10, 590-599.
15. Friedl, P. and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
16. Frittoli, E., Palamidessi, A., Disanza, A. and Scita, G. (2010). Secretory and endo/exocytic trafficking in invadopodia formation: The MT1-MMP paradigm. Eur. J. Cell Biol. 90, 108-114.
17. Gabison, E. E., Huet, E., Baudouin, C. and Menashi, S. (2009). Direct epithelialstromal interaction in corneal wound healing: Role of EMMPRIN/CD147 in MMPs induction and beyond. Prog. Retin. Eye Res. 28, 19-33.
18. Ghatak, S., Misra, S. and Toole, B. P. (2005). Hyaluronan regulates constitutive ErbB2 phosphorylation and signal complex formation in carcinoma cells. J. Biol. Chem. 280, 8875-8883.
19. Guo, H., Zucker, S., Gordon, M. K., Toole, B. P. and Biswas, C. (1997). Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J. Biol. Chem. 272, 24-27.
20. Hagemann, T., Wilson, J., Kulbe, H., Li, N. F., Leinster, D. A., Charles, K., Klemm, F., Pukrop, T., Binder, C. and Balkwill, F. R. (2005). Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. J. Immunol. 175, 1197-1205.
21. Halestrap, A. P. and Meredith, D. (2004). The SLC16 gene family - from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch. 447, 619-628.
22. Hotary, K., Li, X. Y., Allen, E., Stevens, S. L. and Weiss, S. J. (2006). A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 20, 2673-2686.
23. Hu, J., Mukhopadhyay, A., Truesdell, P., Chander, H., Mukhopadhyay, U. K., Mak, A. S. and Craig, A. W. (2011). Cdc42-interacting protein 4 is a Src substrate that regulates invadopodia and invasiveness of breast tumors by promoting MT1-MMP endocytosis. J. Cell Sci. 124, 1739-1751.
24. Jiang, A., Lehti, K., Wang, X., Weiss, S. J., Keski-Oja, J. and Pei, D. (2001). Regulation of membrane-type matrix metalloproteinase 1 activity by dynaminmediated endocytosis. Proc. Natl. Acad. Sci. USA 98, 13693-13698.
25. Kataoka, H., DeCastro, R., Zucker, S. and Biswas, C. (1993). Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin, and 72-kDa gelatinase. Cancer Res. 53, 3154-3158.
26. Kawakami, T., Sameshima, T., Hojo, H., Koga, K., Nakahara, Y., Toole, B. P., Suzumiya, J., Okada, Y., Iwasaki, A. and Nabeshima, K. (2011). Synthetic emmprin peptides with chitobiose substitution stimulate MMP-2 production by fibroblasts. BMC Cancer 11, 300.
27. Klein, C. A., Seidl, S., Petat-Dutter, K., Offner, S., Geigl, J. B., Schmidt-Kittler, O., Wendler, N., Passlick, B., Huber, R. M., Schlimok, G. et al. (2002). Combined transcriptome and genome analysis of single micrometastatic cells. Nat. Biotechnol. 20, 387-392.
28. Li, R., Huang, L., Guo, H. and Toole, B. P. (2001). Basigin (murine EMMPRIN) stimulates matrix metalloproteinase production by fibroblasts. J. Cell. Physiol. 186, 371-379.
29. Liao, C. G., Kong, L. M., Song, F., Xing, J. L., Wang, L. X., Sun, Z. J., Tang, H., Yao, H., Zhang, Y., Wang, L. et al. (2011). Characterization of basigin isoforms and the inhibitory function of basigin-3 in human hepatocellular carcinoma proliferation and invasion. Mol. Cell. Biol. 31, 2591-2604.
30. Lim, M., Martinez, T., Jablons, D., Cameron, R., Guo, H., Toole, B., Li, J. D. and Basbaum, C. (1998). Tumor-derived EMMPRIN (extracellular matrix metalloproteinase inducer) stimulates collagenase transcription through MAPK p38. FEBS Lett. 441, 88-92.
31. Liu, J., Yue, P., Artym, V. V., Mueller, S. C. and Guo, W. (2009). The role of the exocyst in matrix metalloproteinase secretion and actin dynamics during tumor cell invadopodia formation. Mol. Biol. Cell 20, 3763-3771.
32. Menashi, S., Serova, M., Ma, L., Vignot, S., Mourah, S. and Calvo, F. (2003). Regulation of extracellular matrix metalloproteinase inducer and matrix metalloproteinase expression by amphiregulin in transformed human breast epithelial cells. Cancer Res. 63, 7575-7580.
33. Murphy, D. A. and Courtneidge, S. A. (2011). The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12, 413-426.
34. Nabeshima, K., Iwasaki, H., Koga, K., Hojo, H., Suzumiya, J. and Kikuchi, M. (2006). Emmprin (basigin/CD147): matrix metalloproteinase modulator and multifunctional cell recognition molecule that plays a critical role in cancer progression. Pathol. Int. 56, 359-367.
35. Niiya, D., Egawa, N., Sakamoto, T., Kikkawa, Y., Shinkawa, T., Isobe, T., Koshikawa, N. and Seiki, M. (2009). Identification and characterization of Lutheran blood group glycoprotein as a new substrate of membrane-type 1 matrix metalloproteinase 1 (MT1-MMP): a systemic whole cell analysis of MT1-MMPassociating proteins in A431 cells. J. Biol. Chem. 284, 27360-27369.
36. Oser, M., Yamaguchi, H., Mader, C. C., Bravo-Cordero, J. J., Arias, M., Chen, X., Desmarais, V., van Rheenen, J., Koleske, A. J. and Condeelis, J. (2009). Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 186, 571-587.
37. Pituch-Noworolska, A., Drabik, G., Szatanek, R., Bialas, M., Kolodziejczyk, P., Szczepanik, A., Stachura, J. and Zembala, M. (2007). Immunophenotype of isolated tumour cells in the blood, bone marrow and lymph nodes of patients with gastric cancer. Pol. J. Pathol. 58, 93-97.
38. 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.
39. Qian, A. R., Zhang, W., Cao, J. P., Yang, P. F., Gao, X., Wang, Z., Xu, H. Y., Weng, Y. Y. and Shang, P. (2008). Downregulation of CD147 expression alters cytoskeleton architecture and inhibits gelatinase production and SAPK pathway in human hepatocellular carcinoma cells. J. Exp. Clin. Cancer Res. 27, 50.
40. Ramos, D. M. and Dang, D. (2011). EMMPRIN expression in oral SCC is regulated by FYN kinase. Anticancer Res. 31, 1205-1209.
41. Reddy, V. S., Prabhu, S. D., Mummidi, S., Valente, A. J., Venkatesan, B., Shanmugam, P., Delafontaine, P. and Chandrasekar, B. (2010). Interleukin-18 induces EMMPRIN expression in primary cardiomyocytes via JNK/Sp1 signaling and MMP-9 in part via EMMPRIN and through AP-1 and NF-kappaB activation. Am. J. Physiol. Heart Circ. Physiol. 299, H1242-H1254.
42. Reimers, N., Zafrakas, K., Assmann, V., Egen, C., Riethdorf, L., Riethdorf, S., Berger, J., Ebel, S., Janicke, F., Sauter, G. et al. (2004). Expression of extracellular matrix metalloprotease inducer on micrometastatic and primary mammary carcinoma cells. Clin. Cancer Res. 10, 3422-3428.
43. Rowe, R. G. and Weiss, S. J. (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol. 18, 560-574.
44. Rucci, N., Millimaggi, D., Mari, M., Del Fattore, A., Bologna, M., Teti, A., Angelucci, A. and Dolo, V. (2010). Receptor activator of NF-kappaB ligand enhances breast cancer-induced osteolytic lesions through upregulation of extracellular matrix metalloproteinase inducer/CD147. Cancer Res. 70, 6150-6160.
45. Schlosshauer, B., Bauch, H. and Frank, R. (1995). Neurothelin: amino acid sequence, cell surface dynamics and actin colocalization. Eur. J. Cell Biol. 68, 159-166.
46. Schoumacher, M., Goldman, R. D., Louvard, D. and Vignjevic, D. M. (2010). Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 189, 541-556.
47. Schwab, W., Harada, H., Goetz, W., Nowicki, M., Witt, M., Kasper, M. and Barth, K. (2007). Immunocytochemical and biochemical detection of EMMPRIN in the rat tooth germ: differentiation-dependent co-expression with MMPs and co-localization with caveolin-1 in membrane rafts of dental epithelial cells. Histochem. Cell Biol. 128, 195-203.
48. Slomiany, M. G., Grass, G. D., Robertson, A. D., Yang, X. Y., Maria, B. L., Beeson, B. and Toole, B. P. (2009). Hyaluronan, CD44 and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells. Cancer Res. 69, 1293-1301.
49. Soderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G. et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000.
50. Sun, J. and Hemler, M. E. (2001). Regulation of MMP-1 and MMP-2 production through CD147/extracellular matrix metalloproteinase inducer interactions. Cancer Res. 61, 2276-2281.
51. Sung, Y. M., Xu, X., Sun, J., Mueller, D., Sentissi, K., Johnson, P., Urbach, E., Seillier-Moiseiwitsch, F., Johnson, M. D. and Mueller, S. C. (2009). Tumor suppressor function of Syk in human MCF10A in vitro and normal mouse mammary epithelium in vivo. PLoS One 4, e7445.
52. Tang, J., Wu, Y. M., Zhao, P., Yang, X. M., Jiang, J. L. and Chen, Z. N. (2008). Overexpression of HAb18G/CD147 promotes invasion and metastasis via alpha3-beta1 integrin mediated FAK-paxillin and FAK-PI3K-Ca2+ pathways. Cell. Mol. Life Sci. 65, 2933-2942.
53. Tang, W. and Hemler, M. E. (2004). Caveolin-1 regulates matrix metalloproteinases-1 induction and CD147/EMMPRIN cell surface clustering. J. Biol. Chem. 279, 11112-11118.
54. Tang, W., Chang, S. B. and Hemler, M. E. (2004a). Links between CD147 function, glycosylation, and caveolin-1. Mol. Biol. Cell 15, 4043-4050.
55. Tang, Y., Kesavan, P., Nakada, M. T. and Yan, L. (2004b). Tumor-stroma interaction: positive feedback regulation of extracellular matrix metalloproteinase inducer (EMMPRIN) expression and matrix metalloproteinase-dependent generation of soluble EMMPRIN. Mol. Cancer Res. 2, 73-80.
56. Thankamony, S. P. and Knudson, W. (2006). Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J. Biol. Chem. 281, 34601-34609.
57. Venkatesan, B., Valente, A. J., Prabhu, S. D., Shanmugam, P., Delafontaine, P. and Chandrasekar, B. (2010). EMMPRIN activates multiple transcription factors in cardiomyocytes, and induces interleukin-18 expression via Rac1-dependent PI3K/ Akt/IKK/NF-kappaB and MKK7/JNK/AP-1 signaling. J. Mol. Cell. Cardiol. 49, 655-663.
58. Yamaguchi, H., Takeo, Y., Yoshida, S., Kouchi, Z., Nakamura, Y. and Fukami, K. (2009). Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res. 69, 8594-8602.
59. Yan, L., Zucker, S. and Toole, B. P. (2005). Roles of the multifunctional glycoprotein, emmprin (basigin; CD147), in tumour progression. Thromb. Haemost. 93, 199-204.
60. Yang, J. M., O'Neill, P., Jin, W., Foty, R., Medina, D. J., Xu, Z., Lomas, M., Arndt, G. M., Tang, Y., Nakada, M. et al. (2006). Extracellular matrix metalloproteinase inducer (CD147) confers resistance of breast cancer cells to anoikis through inhibition of Bim. J. Biol. Chem. 281, 9719-9727.
61. Zucker, S., Hymowitz, M., Rollo, E. E., Mann, R., Conner, C. E., Cao, J., Foda, H. D., Tompkins, D. C. and Toole, B. P. (2001). Tumorigenic potential of extracellular matrix metalloproteinase inducer (EMMPRIN). Am. J. Pathol. 158, 1921-1928.