Aberrant, persistent inclusion into lipid rafts limits the tumorigenic function of membrane type-1 matrix metalloproteinase in malignant cells

Experimental Cell Research

Volumn 293, Issue 1, 2004, Pages 81-95

  Rozanov, Dmitri V ^a   Deryugina, Elena I ^a   Monosov, Edward Z ^a   Marchenko, Natalia D ^a   Strongin, Alex Y ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Breast carcinoma; Caveolin; Extracellular matrix; Glioblastoma; Invasion; Lipid rafts; Migration; Xenografts

Indexed keywords

CADHERIN; CHLOROQUINE; COLLAGEN; CYCLOHEXIMIDE; ENZYME PRECURSOR; ILOMASTAT; LIPID; MATRIX METALLOPROTEINASE 14; MEMBRANE-TYPE 1 MATRIX METALLOPROTEINASE; METALLOPROTEINASE; MUTANT PROTEIN; PROTEINASE; UVOMORULIN;

AMINO ACID SUBSTITUTION; ANIMAL; ANIMAL CELL; ARTICLE; BREAST CARCINOMA; BREAST TUMOR; CANCER CELL; CARCINOGENESIS; CARCINOMA; CARCINOMA CELL; CAVEOLA; CELL ADHESION; CELL AGGREGATION; CELL GROWTH; CELL MEMBRANE; CELL MIGRATION; CELL MOTION; CELL SURFACE; CELL TRANSPLANTATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; HUMAN; HUMAN CELL; METABOLISM; MOUSE; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; TUMOR CELL LINE; WILD TYPE; XENOGRAFT;

EID: 0347951043     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.10.006     Document Type: Article

References (65)

1. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev., Cancer. 2:2002;161-174.
2. Nagase H., Woessner J.F. Matrix metalloproteinases. J. Biol. Chem. 274:1999;21491-21494.
3. Massova I., Kotra L.P., Fridman R., Mobashery S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J. 12:1998;1075-1095.
4. McCawley L.J., Matrisian L.M. Matrix metalloproteinases: they're not just for matrix anymore! Curr. Opin. Cell Biol. 13:2001;534-540.
5. Hotary K., Allen E., Punturieri A., Yana I., Weiss S.J. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149:2000;1309-1323.
6. Hotary K.B., Yana I., Sabeh F., Li X.Y., Holmbeck K., Birkedal-Hansen H., Allen E.D., Hiraoka N., Weiss S.J. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J. Exp. Med. 195:1999;295-308.
7. Deryugina E.I., Ratnikov B.I., Strongin A.Y. Prinomastat, a hydroxamate inhibitor of matrix metalloproteinases, has a complex effect on migration of breast carcinoma cells. Int. J. Cancer. 104:2003;533-541.
8. Sato H., Takino T., Okada Y., Cao J., Shinagawa A., Yamamoto E., Seiki M. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature. 370:1994;61-65.
9. Hernandez-Barrantes S., Bernardo M., Toth M., Fridman R. Regulation of membrane type-matrix metalloproteinases. Semin. Cancer Biol. 12:2002;131-138.
10. Seiki M., Koshikawa N., Yana I. Role of pericellular proteolysis by membrane-type 1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Metastasis Rev. 22:2003;129-143.
11. Seiki M. Membrane-type 1 matrix metalloproteinase: a key enzyme for tumor invasion. Cancer Lett. 194:2003;1-11.
12. Knauper V., Bailey L., Worley J.R., Soloway P., Patterson M.L., Murphy G. Cellular activation of proMMP-13 by MT1-MMP depends on the C-terminal domain of MMP-13. FEBS Lett. 532:2002;127-130.
13. Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., Goldberg G.I. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270:1995;5331-5338.
14. Kajita M., Itoh Y., Chiba T., Mori H., Okada A., Kinoh H., Seiki M. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153:2001;893-904.
15. Belkin A.M., Akimov S.S., Zaritskaya L.S., Ratnikov B.I., Deryugina E.I., Strongin A.Y. Matrix-dependent proteolysis of surface transglutaminase by membrane-type metalloproteinase regulates cancer cell adhesion and locomotion. J. Biol. Chem. 276:2001;18415-18422.
16. Ito K., Okamoto I., Araki N., Kawano Y., Nakao M., Fujiyama S., Tomita K., Mimori T., Saya H. Calcium influx triggers the sequential proteolysis of extracellular and cytoplasmic domains of E-cadherin, leading to loss of beta-catenin from cell-cell contacts. Oncogene. 18:1999;7080-7090.
17. Steinhusen U., Weiske J., Badock V., Tauber R., Bommert K., Huber O. Cleavage and shedding of E-cadherin after induction of apoptosis. J. Biol. Chem. 276:2001;4972-4980.
18. Ratnikov B.I., Rozanov D.V., Postnova T.I., Baciu P.C., Zhang H., DiScipio R.G., Chestukhina G.G., Smith J.W., Deryugina E.I., Strongin A.Y. An alternative processing of integrin alpha(v) subunit in tumor cells by membrane type-1 matrix metalloproteinase. J. Biol. Chem. 277:2002;7377-7385.
19. Deryugina E.I., Ratnikov B.I., Postnova T.I., Rozanov D.V., Strongin A.Y. Processing of integrin alpha(v) subunit by membrane type 1 matrix metalloproteinase stimulates migration of breast carcinoma cells on vitronectin and enhances tyrosine phosphorylation of focal adhesion kinase. J. Biol. Chem. 277:2002;9749-9756.
20. Overall C.M., Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev., Cancer. 2:2002;657-672.
21. Pei D., Weiss S.J. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature. 375:1995;244-247.
22. Bassi D.E., Lopez De Cicco R., Mahloogi H., Zucker S., Thomas G., Klein-Szanto A.J. Furin inhibition results in absent or decreased invasiveness and tumorigenicity of human cancer cells. Proc. Natl. Acad. Sci. U. S. A. 98:2001;10326-10331.
23. Rozanov D.V., Deryugina E.I., Ratnikov B.I., Monosov E.Z., Marchenko G.N., Quigley J.P., Strongin A.Y. 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. 276:2001;25705-25714.
24. Rozanov D.V., Strongin A.Y. Membrane type-1 matrix metalloproteinase functions as a proprotein self-convertase. Expression of the latent zymogen in Pichia pastoris, autolytic activation, and the peptide sequence of the cleavage forms. J. Biol. Chem. 278:2003;8257-8260.
25. Sato T., Kondo T., Fujisawa T., Seiki M., Ito A. Furin-independent pathway of membrane type 1-matrix metalloproteinase activation in rabbit dermal fibroblasts. J. Biol. Chem. 274:1999;37280-37284.
26. Yana I., Weiss S.J. Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol. Biol. Cell. 11:2000;2387-2401.
27. Zucker S., Drews M., Conner C., Foda H.D., DeClerck Y.A., Langley K.E., Bahou W.F., Docherty A.J., Cao J. Tissue inhibitor of metalloproteinase-2 (TIMP-2) binds to the catalytic domain of the cell surface receptor, membrane type 1-matrix metalloproteinase 1 (MT1-MMP). J. Biol. Chem. 273:1998;1216-1222.
28. Toth M., Hernandez-Barrantes S., Osenkowski P., Bernardo M.M., Gervasi D.C., Shimura Y., Meroueh O., Kotra L.P., Galvez B.G., Arroyo A.G., Mobashery S., Fridman R. Complex pattern of membrane type 1 matrix metalloproteinase shedding. Regulation by autocatalytic cells surface inactivation of active enzyme. J. Biol. Chem. 277:2002;26340-26350.
29. Jiang A., Lehti K., Wang X., Weiss S.J., Keski-Oja J., Pei D. Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proc. Natl. Acad. Sci. U. S. A. 98:2001;13693-13698.
30. Maquoi E., Peyrollier K., Noel A., Foidart J.M., Frankenne F. Regulation of membrane-type 1 matrix metalloproteinase activity by vacuolar H+-ATPases. Biochem. J. 373:1999;19-24.
31. Zucker S., Hymowitz M., Conner C.E., DiYanni E.A., Cao J. Rapid trafficking of membrane type 1-matrix metalloproteinase to the cell surface regulates progelatinase A activation. Lab. Invest. 82:2002;1673-1684.
32. Urena J.M., Merlos-Suarez A., Baselga J., Arribas J. The cytoplasmic carboxy-terminal amino acid determines the subcellular localization of proTGF-(alpha) and membrane type matrix metalloprotease (MT1-MMP). J. Cell Sci. 112:1999;773-784.
33. Rozanov D.V., Ghebrehiwet B., Ratnikov B.I., Monosov E.Z., Deryugina E.I., Strongin A.Y. 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. 527:2002;51-57.
34. Seiki M., Yana I. Roles of pericellular proteolysis by membrane type-1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Sci. 94:2003;569-574.
35. Rozanov D.V., Ghebrehiwet B., Postnova T.I., Eichinger A., Deryugina E.I., Strongin A.Y. The hemopexin-like C-terminal domain of membrane type 1 matrix metalloproteinase regulates proteolysis of a multifunctional protein, gC1qR. J. Biol. Chem. 277:2002;9318-9325.
36. Deryugina E.I., Soroceanu L., Strongin A.Y. Up-regulation of vascular endothelial growth factor by membrane-type 1 matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis. Cancer Res. 62:2002;580-588.
37. Deryugina E.I., Ratnikov B.I., Monosov E., Postnova T.I., DiScipio R., Smith J.W., Strongin A.Y. MT1-MMP initiates activation of pro-MMP-2 and integrin alphavbeta3 promotes maturation of MMP-2 in breast carcinoma cells. Exp. Cell Res. 263:2001;209-223.
38. Deryugina E.I., Bourdon M.A., Luo G.X., Reisfeld R.A., Strongin A.Y. Matrix metalloproteinase-2 activation modulates glioma cell migration. J. Cell Sci. 110:1997;2473-2482.
39. Deryugina E.I., Bourdon M.A., Reisfeld R.A., Strongin A.Y. Remodeling of collagen matrix by human tumor cells requires activation and cell surface association of matrix metalloproteinase-2. Cancer Res. 58:1998;3743-3750.
40. Sounni N.E., Devy L., Hajitou A., Frankenne F., Munaut C., Gilles C., Deroanne C., Thompson E.W., Foidart J.M., Noel A. MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J. 16:2002;555-564.
41. Galbiati F., Volonte D., Brown A.M., Weinstein D.E., Ben-Ze'ev A., Pestell R.G., Lisanti M.P. Caveolin-1 expression inhibits Wnt/beta-catenin/ Lef-1 signaling by recruiting beta-catenin to caveolae membrane domains. J. Biol. Chem. 275:2000;23368-23377.
42. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1981;1604-1607.
43. Bricker T.M., Sherman L.A. Triton X-114 phase fractionation of membrane proteins of the cyanobacterium Anacystis nidulans R2. Arch. Biochem. Biophys. 235:1984;204-211.
44. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:2003;267-277.
45. Marella M., Lehmann S., Grassi J., Chabry J. Filipin prevents pathological prion protein accumulation by reducing endocytosis and inducing cellular PrP release. J. Biol. Chem. 277:2002;25457-25464.
46. Annabi B., Lachambre M., Bousquet-Gagnon N., Page M., Gingras D., Beliveau R. Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem. J. 353:2001;547-553.
47. Puyraimond A., Fridman R., Lemesle M., Arbeille B., Menashi S. MMP-2 colocalizes with caveolae on the surface of endothelial cells. Exp. Cell Res. 262:2001;28-36.
48. Marchenko G.N., Marchenko N.D., Strongin A.Y. The human and mouse matrix metalloproteinase MMP-21: the structure and the regulation of the gene and the protein. Biochem. J. 372:2003;503-515.
49. Lehti K., Lohi J., Juntunen M.M., Pei D., Keski-Oja J. Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J. Biol. Chem. 277:2002;8440-8448.
50. 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., Birkedal-Hansen H. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell. 99:1999;81-92.
51. Will H., Atkinson S.J., Butler G.S., Smith B., Murphy G. The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. J. Biol. Chem. 271:1996;17119-17123.
52. Mori H., Tomari T., Koshikawa N., Kajita M., Itoh Y., Sato H., Tojo H., Yana I., Seiki M. CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J. 21:2002;3949-3959.
53. Nakahara H., Howard L., Thompson E.W., Sato H., Seiki M., Yeh Y., Chen W.T. Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc. Natl. Acad. Sci. U. S. A. 94:1997;7959-7964.
54. Takahashi M., Tsunoda T., Seiki M., Nakamura Y., Furukawa Y. Identification of membrane-type matrix metalloproteinase-1 as a target of the beta-catenin/Tcf4 complex in human colorectal cancers. Oncogene. 21:2002;5861-5867.
55. Kang T., Nagase H., Pei D. Activation of membrane-type matrix metalloproteinase 3 zymogen by the proprotein convertase furin in the trans-Golgi network. Cancer Res. 62:2002;675-681.
56. Pei D., Weiss S.J. Transmembrane-deletion mutants of the membrane-type matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity. J. Biol. Chem. 271:1996;9135-9140.
57. Uekita T., Itoh Y., Yana I., Ohno H., Seiki M. Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J. Cell Biol. 155:2001;1345-1356.
58. Galbiati F., Razani B., Lisanti M.P. Emerging themes in lipid rafts and caveolae. Cell. 106:2001;403-411.
59. Kurzchalia T.V., Parton R.G. Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11:1999;424-431.
60. Razani B., Lisanti M.P. Caveolins and caveolae: molecular and functional relationships. Exp. Cell Res. 271:2001;36-44.
61. Shiao Y.J., Vance J.E. Sphingomyelin transport to the cell surface occurs independently of protein secretion in rat hepatocytes. J. Biol. Chem. 268:1993;26085-26092.
62. Morrow I.C., Rea S., Martin S., Prior I.A., Prohaska R., Hancock J.F., James D.E., Parton R.G. Flotillin-1/reggie-2 traffics to surface raft domains via a novel golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. J. Biol. Chem. 277:2002;48834-48841.
63. Smart E.J., Graf G.A., McNiven M.A., Sessa W.C., Engelman J.A., Scherer P.E., Okamoto T., Lisanti M.P. Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19:1999;7289-7304.
64. Anderson R.G. The caveolae membrane system. Annu. Rev. Biochem. 67:1998;199-225.
65. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev., Cancer. 3:2003;362-374.