Biochemical evidence of the interactions of membrane type-1 matrix metalloproteinase (MT1-MMP) with adenine nucleotide translocator (ANT): potential implications linking proteolysis with energy metabolism in cancer cells.
Radichev, I. A.; Remacle, A. G.; Sounni, Nor Eddineet al.
[en] Invasion-promoting MT1-MMP (membrane type-1 matrix metalloproteinase) is a key element in cell migration processes. To identify the proteins that interact and therefore co-precipitate with this proteinase from cancer cells, we used the proteolytically active WT (wild-type), the catalytically inert E240A and the C-end truncated (tailless; ΔCT) MT1-MMP–FLAG constructs as baits. The identity of the pulled-down proteins was determined by LC-MS/MS (liquid chromatography tandem MS) and then confirmed by Western blotting using specific antibodies. We determined that, in breast carcinoma MCF cells (MCF-7 cells), ANT (adenine nucleotide translocator) efficiently interacted with the WT, E240A and ΔCT constructs. The WT and E240A constructs also interacted with α-tubulin, an essential component of clathrin-mediated endocytosis. In turn, tubulin did not co-precipitate with the ΔCT construct because of the inefficient endocytosis of the latter, thus suggesting a high level of selectivity of our test system. To corroborate these results, we then successfully used the ANT2–FLAG construct as a bait to pull-down MT1-MMP, which was naturally produced by fibrosarcoma HT1080 cells. We determined that the presence of the functionally inert catalytic domain alone was sufficient to cause the proteinase to interact with ANT2, thus indicating that there is a non-proteolytic mode of these interactions. Overall, it is tempting to hypothesize that by interacting with pro-invasive MT1-MMP, ANT plays a yet to be identified role in a coupling mechanism between energy metabolism and pericellular proteolysis in migrating cancer cells.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Radichev, I. A.
Remacle, A. G.
Sounni, Nor Eddine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Shiryaev, S. A.
Rozanov, D. V.
Zhu, W.
Golubkova, N. V.
Postnova, T. I.
Golubkov, V. S.
Strongin, A. Y.
Language :
English
Title :
Biochemical evidence of the interactions of membrane type-1 matrix metalloproteinase (MT1-MMP) with adenine nucleotide translocator (ANT): potential implications linking proteolysis with energy metabolism in cancer cells.
Lopez-Otin, C. and Bond, J. S. (2008) Proteases: multifunctional enzymes in life and disease. J. Biol. Chem. 283, 30433-30437
Seiki, M. and Yana, I. (2003) Roles of pericellular proteolysis by membrane type-1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Sci. 94, 569-574
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
Strongin, A. Y. (2006) Mislocalization and unconventional functions of cellular MMPs in cancer. Cancer Metastasis Rev. 25, 87-98
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
Itoh, Y. (2006) MT1-MMP: a key regulator of cell migration in tissue. IUBMB Life 58, 589-596
Li, X. Y., Ota, I., Yana, I., Sabeh, F. and Weiss, S. J. (2008) Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol. Biol. Cell 19, 3221-3233
Egeblad, M. and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174
Wolf, K. and Friedl, P. (2009) Mapping proteolytic cancer cell-extracellular matrix interfaces. Clin. Exp. Metastasis 26, 289-298
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
Rozanov, D. V., Savinov, A. Y., Williams, R., Liu, K., Golubkov, V. S., Krajewski, S. and Strongin, A. Y. (2008) Molecular signature of MT1-MMP: transactivation of the downstream universal gene network in cancer. Cancer Res. 68, 4086-4096
Detke, S. and Elsabrouty, R. (2008) Identification of a mitochondrial ATP synthase-adenine nucleotide translocator complex in Leishmania. Acta Trop. 105, 16-20
Detke, S. and Elsabrouty, R. (2008) Leishmania mexicana amazonensis: plasma membrane adenine nucleotide translocator and chemotaxis. Exp. Parasitol. 118, 408-419
Golubkov, V. S., Chekanov, A. V., Shiryaev, S. A., Aleshin, A. E., Ratnikov, B. I., Gawlik, K., Radichev, I., Motamedchaboki, K., Smith, J. W. and Strongin, A. Y. (2007) Proteolysis of the membrane type-1 matrix metalloproteinase prodomain: implications for a two-step proteolytic processing and activation. J. Biol. Chem. 282, 36283-36291
Ratnikov, B., Deryugina, E., Leng, J., Marchenko, G., Dembrow, D. and Strongin, A. (2000) Determination of matrix metalloproteinase activity using biotinylated gelatin. Anal. Biochem. 286, 149-155
Rozanov, D. V., Deryugina, E. I., Monosov, E. Z., Marchenko, N. D. and Strongin, A. Y. (2004) Aberrant, persistent inclusion into lipid rafts limits the tumorigenic function of membrane type-1 matrix metalloproteinase in malignant cells. Exp. Cell Res. 293, 81-95
Rozanov, D. V., Deryugina, E. I., Ratnikov, B. I., Monosov, E. Z., Marchenko, G. N., Quigley, J. P. and Strongin, A. Y. (2001) Mutation analysis of membrane type-1 matrix metalloproteinase (MT1-MMP). The role of the cytoplasmic tail Cys(574), the active site Glu(240), and furin cleavage motifs in oligomerization, processing, and self-proteolysis of MT1-MMP expressed in breast carcinoma cells. J. Biol. Chem. 276, 25705-25714
Golubkov, V. S., Boyd, S., Savinov, A. Y., Chekanov, A. V., Osterman, A. L., Remacle, A., Rozanov, D. V., Doxsey, S. J. and Strongin, A. Y. (2005) Membrane type-1 matrix metalloproteinase (MT1-MMP) exhibits an important intracellular cleavage function and causes chromosome instability. J. Biol. Chem. 280, 25079-25086
Remacle, A. G., Rozanov, D. V., Baciu, P. C., Chekanov, A. V., Golubkov, V. S. and Strongin, A. Y. (2005) The transmembrane domain is essential for the microtubular trafficking of membrane type-1 matrix metalloproteinase (MT1-MMP). J. Cell Sci. 118, 4975-4984
Deryugina, E. I., Bourdon, M. A., Jungwirth, K., Smith, J. W. and Strongin, A. Y. (2000) Functional activation of integrin alpha V beta 3 in tumor cells expressing membrane-type 1 matrix metalloproteinase. Int. J. Cancer 86, 15-23
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 dynamin-mediated endocytosis. Proc. Natl. Acad. Sci. U.S.A. 98, 13693-13698
Lehti, K., Valtanen, H., Wickstrom, S. A., Lohi, J. and Keski-Oja, J. (2000) Regulation of membrane-type-1 matrix metalloproteinase activity by its cytoplasmic domain. J. Biol. Chem. 275, 15006-15013
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
Maquoi, E., Frankenne, F., Baramova, E., Munaut, C., Sounni, N. E., Remacle, A., Noel, A., Murphy, G. and Foidart, J. M. (2000) Membrane type 1 matrix metalloproteinase-associated degradation of tissue inhibitor of metalloproteinase 2 in human tumor cell lines. J. Biol. Chem. 275, 11368-11378
Osenkowski, P., Toth, M. and Fridman, R. (2004) Processing, shedding, and endocytosis of membrane type 1-matrix metalloproteinase (MT1-MMP). J. Cell Physiol. 200, 2-10
Zamora, M., Granell, M., Mampel, T. and Vinas, O. (2004) Adenine nucleotide translocase 3 (ANT3) overexpression induces apoptosis in cultured cells. FEBS Lett. 563, 155-160
Yang, Z., Cheng, W., Hong, L., Chen, W., Wang, Y., Lin, S., Han, J., Zhou, H. and Gu, J. (2007) Adenine nucleotide (ADP/ATP) translocase 3 participates in the tumor necrosis factor induced apoptosis of MCF-7 cells. Mol. Biol. Cell 18, 4681-4689
Chevrollier, A., Loiseau, D., Chabi, B., Renier, G., Douay, O., Malthiery, Y. and Stepien, G. (2005) ANT2 isoform required for cancer cell glycolysis. J. Bioenerg. Biomembr. 37, 307-316
Giraud, S., Bonod-Bidaud, C., Wesolowski-Louvel, M. and Stepien, G. (1998) Expression of human ANT2 gene in highly proliferative cells: GRBOX, a new transcriptional element, is involved in the regulation of glycolytic ATP import into mitochondria. J. Mol. Biol. 281, 409-418
Jang, J. Y., Choi, Y., Jeon, Y. K. and Kim, C. W. (2008) Suppression of adenine nucleotide translocase-2 by vector-based siRNA in human breast cancer cells induces apoptosis and inhibits tumor growth in vitro and in vivo. Breast Cancer Res. 10, R11
Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vieira, H. L., Prevost, M. C., Xie, Z., Matsuyama, S., Reed, J. C. and Kroemer, G. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281, 2027-2031
Verrier, F., Deniaud, A., Lebras, M., Metivier, D., Kroemer, G., Mignotte, B., Jan, G. and Brenner, C. (2004) Dynamic evolution of the adenine nucleotide translocase interactome during chemotherapy-induced apoptosis. Oncogene 23, 8049-8064
Martinez, L. O., Jacquet, S., Esteve, J. P., Rolland, C., Cabezon, E., Champagne, E., Pineau, T., Georgeaud, V., Walker, J. E., Terce, F. et al. (2003) Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 421, 75-79
Wang, T., Chen, Z., Wang, X., Shyy, J. Y. and Zhu, Y. (2006) Cholesterol loading increases the translocation of ATP synthase beta chain into membrane caveolae in vascular endothelial cells. Biochim. Biophys. Acta 1761, 1182-1190
D'Alessio, S., Ferrari, G., Cinnante, K., Scheerer, W., Galloway, A. C., Roses, D. F., Rozanov, D. V., Remacle, A. G., Oh, E. S., Shiryaev, S. A. et al. (2008) Tissue inhibitor of metalloproteinases-2 binding to membrane-type 1 matrix metalloproteinase induces MAPK activation and cell growth by a non-proteolytic mechanism. J. Biol. Chem. 283, 87-99
Takino, T., Watanabe, Y., Matsui, M., Miyamori, H., Kudo, T., Seiki, M. and Sato, H. (2006) Membrane-type 1 matrix metalloproteinase modulates focal adhesion stability and cell migration. Exp. Cell Res. 312, 1381-1389
Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003) Cell migration: integrating signals from front to back. Science 302, 1704-1709
Faure Vigny, H., Heddi, A., Giraud, S., Chautard, D. and Stepien, G. (1996) Expression of oxidative phosphorylation genes in renal tumors and tumoral cell lines. Mol. Carcinog. 16, 165-172
Lunardi, J. and Attardi, G. (1991) Differential regulation of expression of the multiple ADP/ATP translocase genes in human cells. J. Biol. Chem. 266, 16534-16540
Stepien, G., Torroni, A., Chung, A. B., Hodge, J. A. and Wallace, D. C. (1992) Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J. Biol. Chem. 267, 14592-14597
Cozens, A. L., Runswick, M. J. and Walker, J. E. (1989) DNA sequences of two expressed nuclear genes for human mitochondrial ADP/ATP translocase. J. Mol. Biol. 206, 261-280
Dolce, V., Scarcia, P., Iacopetta, D. and Palmieri, F. (2005) A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett. 579, 633-637
Kuan, J. and Saier, Jr, M. H. (1993) The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships. Crit. Rev. Biochem. Mol. Biol. 28, 209-233
Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trezeguet, V., Lauquin, G. J. and Brandolin, G. (2003) Structure of mitochondrial ADP/ ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44
Belzacq, A. S. and Brenner, C. (2003) The adenine nucleotide translocator: a new potential chemotherapeutic target. Curr. Drug Targets 4, 517-524
Le Bras, M., Borgne-Sanchez, A., Touat, Z., El Dein, O. S., Deniaud, A., Maillier, E., Lecellier, G., Rebouillat, D., Lemaire, C., Kroemer, G. et al. (2006) Chemosensitization by knockdown of adenine nucleotide translocase-2. Cancer Res. 66, 9143-9152
Miyazaki, E., Kida, Y., Mihara, K. and Sakaguchi, M. (2005) Switching the sorting mode of membrane proteins from cotranslational endoplasmic reticulum targeting to posttranslational mitochondrial import. Mol. Biol. Cell 16, 1788-1799
Stornaiuolo, M., Lotti, L. V., Borgese, N., Torrisi, M. R., Mottola, G., Martire, G. and Bonatti, S. (2003) KDEL and KKXX retrieval signals appended to the same reporter protein determine different trafficking between endoplasmic reticulum, intermediate compartment, and Golgi complex. Mol. Biol. Cell 14, 889-902
