BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Caveolin-1 inhibits membrane-type 1 matrix metalloproteinase activity

  • Published : 2008.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Membrane-type 1 matrix metalloproteinase (MT1-MMP) is a zinc-dependent proteinase found in cholesterol-rich lipid rafts on the plasma membrane. MT1-MMP hydrolyzes extracellular matrix (ECM) proteins, activates pro-matrix metalloproteinase-2 (proMMP-2) and plays an important role in ECM remodeling, cancer cell migration and metastasis. The role of caveolin-1, an integral protein of caveolae, in the activation of MT1-MMP remains largely unknown. Here, we show that the expression of caveolin-1 attenuates the activation of proMMP-2, reduces proteolytic cleavage of ECM and inhibits cell migration. We utilized the cytoplasmic tail domain deletion (${\Delta}CT$) or the E240A mutant of MT1-MMP. Co-expression of caveolin-1 with the wild-type or the ${\Delta}CT$ MT1-MMP decreased the proMMP-2 activation and inhibited collagen degradation and cell migration. Caveolin-1 had no effect on the catalytically inert E240A MT1-MMP. Our findings suggest that caveolin-1 is essential in the down-regulation of MT1-MMP activity by promoting internalization from the cell surface.

Keywords

References

  1. Nagase, H. and Woessner, J.F., Jr. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494. https://doi.org/10.1074/jbc.274.31.21491
  2. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65. https://doi.org/10.1038/370061a0
  3. Egeblad, M. and Werb, Z. (2002) New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174. https://doi.org/10.1038/nrc745
  4. Yana, I. and Weiss, S.J. (2000) Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol. Biol. Cell 11, 2387-2401. https://doi.org/10.1091/mbc.11.7.2387
  5. Rozanov, D.V., Ghebrehiwet, B., Ratnikov, B., Monosov, E.Z., Deryugina, E.I. and Strongin, A.Y. (2002) The cytoplasmic tail peptide sequence of membrane type-1 matrix metalloproteinase (MT1-MMP) directly binds to gC1qR, a compartment-specific chaperone-like regulatory protein. FEBS. Lett. 527, 51-57. https://doi.org/10.1016/S0014-5793(02)03153-8
  6. Cao, J., Kozarekar, P., Pavlaki, M., Chiarelli, C., Bahou, W.F. and Zucker, S. (2004) Distinct roles for the catalytic and hemopexin domains of membrane type 1-matrix metalloproteinase in substrate degradation and cell migration. J. Biol. Chem. 279, 14129-14139. https://doi.org/10.1074/jbc.M312120200
  7. Butler, G.S., Butler, M.J., Atkinson, S.J., Will, H., Tamura, T., Schade van Westrum, S., Crabbe, T., Clements, J., d'Ortho, M.P. and Murphy, G. (1998) The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A. A kinetic study. J. Biol. Chem. 273, 871-880. https://doi.org/10.1074/jbc.273.2.871
  8. 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 (Pt 18), 2789-2798.
  9. 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. https://doi.org/10.1042/0264-6021:3530547
  10. Patel, H.H., Murray, F. and Insel, P.A. (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu. Rev. Pharmacol. Toxicol. 48, 359-391. https://doi.org/10.1146/annurev.pharmtox.48.121506.124841
  11. Krajewska, W.M. and Maslowska, I. (2004) Caveolins: structure and function in signal transduction. Cell Mol. Biol. Lett. 9, 195-220.
  12. Razani, B., Schlegel, A. and Lisanti, M.P. (2000) Caveolin proteins in signaling, oncogenic transformation and muscular dystrophy. J. Cell Sci. 113 (Pt 12), 2103-2109.
  13. Liu, P., Rudick, M. and Anderson, R.G. (2002) Multiple functions of caveolin-1. J. Biol. Chem. 277, 41295-41298. https://doi.org/10.1074/jbc.R200020200
  14. Labrecque, L., Nyalendo, C., Langlois, S., Durocher, Y., Roghi, C., Murphy, G., Gingras, D. and Beliveau, R. (2004) Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J. Biol. Chem. 279, 52132-52140. https://doi.org/10.1074/jbc.M409617200
  15. Atkinson, S.J., English, J.L., Holway, N. and Murphy, G. (2004) Cellular cholesterol regulates MT1 MMP dependent activation of MMP 2 via MEK-1 in HT1080 fibrosarcoma cells. FEBS. Lett. 566, 65-70. https://doi.org/10.1016/j.febslet.2004.04.040
  16. 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. https://doi.org/10.1016/j.yexcr.2003.10.006
  17. Strongin, A.Y., Collier, I., Bannikov, G., Marmer, B.L., Grant, G.A. and Goldberg, G.I. (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331-5338. https://doi.org/10.1074/jbc.270.10.5331
  18. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S.A., Mankani, M., Robey, P.G., Poole, A.R., Pidoux, I., Ward, J.M. and Birkedal-Hansen, H. (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92. https://doi.org/10.1016/S0092-8674(00)80064-1
  19. Itoh, Y., Takamura, A., Ito, N., Maru, Y., Sato, H., Suenaga, N., Aoki, T. and Seiki, M. (2001) Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J. 20, 4782-4793. https://doi.org/10.1093/emboj/20.17.4782
  20. Strongin, A.Y., Marmer, B.L., Grant, G.A. and Goldberg, G.I. (1993) Plasma membrane-dependent activation of the 72-kDa type IV collagenase is prevented by complex formation with TIMP-2. J. Biol. Chem. 268, 14033-14039.

Cited by

  1. Role of caveolin-1 in fibrotic diseases vol.32, pp.6, 2013, https://doi.org/10.1016/j.matbio.2013.03.005
  2. Microdomain-forming proteins of different families in common signal pathways vol.7, pp.1, 2013, https://doi.org/10.1134/S1990747812060037
  3. Effects of autophagy and endocytosis on the activity of matrix metalloproteinase-2 in human renal proximal tubular cells under hypoxia vol.15, pp.5, 2017, https://doi.org/10.3892/mmr.2017.6358
  4. MMP-2 and 9 in Chronic Kidney Disease vol.18, pp.4, 2017, https://doi.org/10.3390/ijms18040776
  5. Rat forming incisor requires a rigorous ECM remodeling modulated by MMP/RECK balance vol.40, pp.3, 2009, https://doi.org/10.1007/s10735-009-9231-4
  6. Caveolin-1 regulates the expression of tight junction proteins during hyperoxia-induced pulmonary epithelial barrier breakdown vol.17, pp.1, 2016, https://doi.org/10.1186/s12931-016-0364-1
  7. Mechanotransduction pulls the strings of matrix degradation at invadosome vol.57-58, 2017, https://doi.org/10.1016/j.matbio.2016.06.007
  8. Restoration of caveolin-1 expression suppresses growth, membrane-type-4 metalloproteinase expression and metastasis-associated activities in colon cancer cells vol.52, pp.11, 2013, https://doi.org/10.1002/mc.21927
  9. Caveolin-1 is a negative regulator of tumor growth in glioblastoma and modulates chemosensitivity to temozolomide vol.12, pp.10, 2013, https://doi.org/10.4161/cc.24497
  10. Down-Regulation of Stromal Caveolin-1 Expression in Esophageal Squamous Cell Carcinoma: A Potent Predictor of Lymph Node Metastases, Early Tumor Recurrence, and Poor Prognosis vol.21, pp.1, 2014, https://doi.org/10.1245/s10434-013-3225-x
  11. Caveolin-1 as a promoter of tumour spreading: when, how, where and why vol.17, pp.3, 2013, https://doi.org/10.1111/jcmm.12030
  12. caveolae-associated ERK and Akt signaling vol.25, pp.11, 2011, https://doi.org/10.1096/fj.11-188607
  13. Hypoxia Activates Src and Promotes Endocytosis Which Decreases MMP-2 Activity and Aggravates Renal Interstitial Fibrosis vol.19, pp.2, 2018, https://doi.org/10.3390/ijms19020581