Matrix metalloproteinase-9 associated with heparan sulphate chains of GPI-anchored cell surface proteoglycans mediates motility of murine colon adenocarcinoma cells

Journal of Biochemistry

Volumn 143, Issue 5, 2008, Pages 581-592

  Koyama, Yoshie ^a,b   Naruo, Hideaki ^a   Yoshitomi, Yasuo ^a   Munesue, Seiichi ^a   Kiyono, Shinsuke ^a   Kusano, Yuri ^b   Hashimoto, Katsunori ^c   Yokoi, Toyoharu ^c   Nakanishi, Hayao ^d   Shimizu, Satoru ^a   Okayama, Minoru ^a   Oguri, Kayoko ^b  

^a KYOTO SANGYO UNIVERSITY   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

Author keywords

Cell motility; Cell surface heparan sulphate; Glypican; Invasion; Matrix metalloproteinase 9

Indexed keywords

GELATINASE B; GLYPICAN; HEPARIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOMA CELL; CELL LYSATE; CELL MIGRATION; CELL MOTILITY; COLON ADENOCARCINOMA; CONTROLLED STUDY; ENZYME RELEASE; FEMALE; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION;

ADENOCARCINOMA; ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CLONE CELLS; COLONIC NEOPLASMS; FEMALE; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEPARAN SULFATE PROTEOGLYCANS; MATRIX METALLOPROTEINASE 9; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; TISSUE INHIBITOR OF METALLOPROTEINASES;

MURINAE;

EID: 43449136980     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvn006     Document Type: Article

References (57)

1. Chambers, A.F. and Matrisian, L.M. (1997) Changing views of the role of matrixmetalloproteinases in metastasis. J. Natl Cancer Inst. 89, 1260-1270
2. Borden, P. and Heller, R.A. (1997) Transcriptional control of matrix metalloproteinases and the tissue inhibitors of matrix metalloproteinases. Crit. Rev. Eukaryot. Gene Expr. 7, 159-178
3. Nagase, H. and Woessner, Jr., J.F. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494
4. Gomez, D.E., Alonso, D.F., Yoshiji, H., and Thorgeirsson, U.P. (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur. J. Cell Biol. 74, 111-122
5. Liotta, L.A., Tryggvason, K., Garbisa, S., Hart, I., Foltz, C.M., and Shafie, S. (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284, 67-68
6. Stetler-Stevenson, W.G., Aznavoorian, S., and Liotta, L.A. (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis. Ann. Rev. Cell Biol. 9, 541-573
7. Klein, G., Vellenga, E., Fraaije, M.W., Kamps, W.A., and de Bont, E.S. (2004) The possible roles of matrix metalloproteinase (MMP)-2 and MMP-9 in cancer, e.g. acute leukemia. Crit. Rev. Oncol. Hematol. 50, 87-100
8. 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
9. Seiki, M. (2002) The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr. Opin. Cell Biol. 14, 624-632
10. Sehgal, G., Hua, J., Bernhard, E.J., Sehgal, I., Thompson, T.C., and Muschel, R.J. (1998) Requirement for matrix metalloproteinase-9 (gelatinase B) expression in metastasis by murine prostate carcinoma. Am. J. Pathol. 152, 591-596
11. van Kempen, L.C. and Coussens, L.M. (2002) MMP9 potentiates pulmonary metastasis formation. Cancer Cell 2, 251-252
12. Fridman, R. (2003) Surface association of secreted matrix metalloproteinases. Curr. Top. Dev. Biol. 54, 75-100
13. Yamagata, S., Ito, Y., Tanaka, R., and Shimizu, S. (1988) Gelatinases of metastatic cell lines of murine colonic carcinoma as detected by substrate-gel electrophoresis. Biochem. Biophys. Res. Commun. 151, 158-162
14. Sakata, K., Kozaki, K., Iida, K., Tanaka, R., Yamagata, S., Utsumi, K.R., Saga, S., Shimizu, S., and Matsuyama, M. (1996) Establishment and characterization of high- and low-lung-metastatic cell lines derived from murine colon adenocarcinoma 26 tumor line. Jpn. J. Cancer Res. 87, 78-85
15. Reich, R., Thompson, E., Iwamoto, Y., Martin, G.R., Deason, J.R., Fuller, G.C., and Miskin, R. (1988) Effects of plasminogen activator, serine protease, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res. 48, 3307-3312
16. Okada, Y., Gonoji, Y., Naka, K., Tomita, K., Nakanishi, I., Iwata, K., Yamashita, K., and Hayakawa, T. (1992) Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells: purification and activation of the precursor and enzymic properties. J. Biol. Chem. 267, 21712-21719
17. Kusano, Y., Yoshitomi, Y., Munesue, S., Okayama, M., and Oguri, K. (2004) Cooperation of syndecan-2 and syndecan-4 among cell surface heparan sulfate proteoglycans in the actin cytoskeletal organization of Lewis lung carcinoma cells. J. Biochem. 135, 129-137
18. Itano, N., Oguri, K., Nakanishi, H., and Okayama, M. (1993) Membrane-intercalated proteoglycan of a stroma-inducing clone from Lewis lung carcinoma binds to fibronectin via its heparan sulfate chains. J. Biochem. 114, 862-873
19. Ferry, G., Lonchampt, M., Pennel, L., de Nanteuil, G., Canet, E., and Tucker, G. C. (1997) Activation of MMP-9 by neutrophil elastase in an in vivo model of acute lung injury. FEBS Lett. 402, 111-115
20. Yoshitomi, Y., Nakanishi, H., Kusano, Y., Munesue, S., Oguri, K., Tatematsu, M., Yamashina, I., and Okayama, M. (2004) Inhibition of experimental lung metastases of Lewis lung carcinoma cells by chemically modified heparin with reduced anticoagulant activity. Cancer Lett. 207, 165-174
21. Kenagy, R.D., Nikkari, S.T., Weigus, H.G., and Clowes, A.W. (1994) Heparin inhibits the induction of three matrix metalloproteinases(stromelysin, 92kD gelatinase, and collagenase) in primate arterial smooth muscle. J. Clin. Invest. 93, 1987-1993
22. Yu, Q. and Stamenkovic, I. (1999) Localization of mtrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13, 35-48
23. van Hinsbergh, V.W.M., Engelse, M.A., and Quax, H.A. (2006) Pericellular proteases in angiogenesis and vasculogenesis. Arteriocler. Thromb. Vasc. Biol. 26, 716-728
24. Hardingham, T.M. and Fosang, A.J. (1992) Proteoglycans: many forms and many functions. FASEB J. 6, 861-870
25. Abecassis, I., Olofsson, B., Schmid, M., Zalcman, G., and Karniguian, A. (2003) RhoA induces MMP-9 expression at CD44 lamellipodial focal complexes and promotes HMEC-1 cell invasion. Exp. Cell Res. 291, 363-376
26. Jadhav, U., Chigurupati, S., Lakka, S.S., and Mohanam, S. (2004) Inhibition of matrix metalloproteinase-9 reduces in vitro invasion and angiogenesis in human microvascular endothelial cells. Int. J. Oncol. 25, 1407-1414
27. Bandow, K., Ohnishi, T., Tamura, M., Semba, I., and Daikuhara, Y. (2004) Hepatocyte growth factor/scatter factor stimulates migration of muscle precursors in developing mouse tongue. J. Cell Physiol. 201, 236-243
28. Scott, K.A., Arnott, C.H., Robinson, S.C., Moore, R.J., Thompson, R.G., Marshall, I.F., and Balkwill, F.R. (2004) TNG-alpha regulates epithelial expression of MMP-9 and integrin alphaVbeta6 during tumour promotion. A role for TNF-alpha in keratinocyte migration? Oncogene 23, 6954-6966
29. Momota, Y., Suzuki, N., Kasuya, Y., Kobayashi, T., Mizoguchi, M., Yokoyma, F., Nomizu, M., Shinkai, H., Iwasaki, T., and Utani, A. (2005) Laminin alpha3 LG4 module induces keratinocyte migration: involvement of matrix metalloproteinase-9. J. Recept. Signal Transduct. Res. 25, 1-17
30. Legrand, C., Gilles, C., Zahm, J.M., Polette, M., Buisson, A.C., Kaplan, H., Birembaut, P., and Tournier, J.M. (1999) Airway epitrhelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J. Cell. Biol. 146, 517-529
31. Mira, E., Manes, S., Lacalle, R.A., Marquez, G., and Martinez-A, C. (1999) Insulin-like growth factor I-triggered cell migration and invasion are mediated by matrix metalloproteinase-9. Endocrinology 140, 1657-1664
32. O-charoenrat, P., Modjtahedi, H., Rhys-Evans, P., Court, W.J., Box, G.M., and Eccles, S.A. (2000) Epidermal growth factor-like ligands differentially up-regulate matrix metalloproteinase 9 in head and neck squamous carcinaoma cells. Cancer Res. 60, 1121-1128
33. Rolli, M., Fransvea, E., Pilch, J., Saven, A., and Felding-Habermann, B. (2003) Activated integrin alphaVbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 9482-9487
34. Kamiguti, A.S., Lee, E.S., Till, K.J., Harris, R.J., Glenn, M.A., Lin, K., Chen, H.J., Zuzel, M., and Cawley, J.C. (2004) The role of matrix metalloproteinase 9 in the pathogenesis of chronic lymphocytic leukaemia. Br. J. Haematolo. 125, 128-140
35. Bjorklund, M., Heikkila, P., and Koivunen, E. (2004) Peptide inhibition of catalytic and noncatalytic activities of matrix metalloproteinase-9 blocks tumor cell migration and invasion. J. Biol. Chem. 279, 29589-29597
36. Murray, D., Morrin, M., and McDonnell, S. (2004) Increased invasion and expression of MMP-9 in human colorectalcell lines by CD44-dependent mechanism. Anticancer Res. 24, 489-494
37. Lauffenburger, D.A. and Horwitz, A.F. (1996) Cell migration: a physically integrated molecular process. Cell 84, 359-369
38. Mitchison, T.J. and Cramer, L.P. (1996) Actin-based cell motility and cell locomotion. Cell 84, 371-379
39. Kramer, R.H., Vogel, K.G., and Nicolson, G.L. (1982) Solubilization and degradation of subendothelial matrix glycoproteins and proteoglycans by metastatic tumor cells. J. Biol. Chem. 257, 2678-2686
40. Irimura, T., Nakajima, M., and Nicolson, G.L. (1986) Chemically modified heparins as inhibitors of heparan sulfate specific endo-beta-glucuronidase (heparanase) of metastatic melanoma cells. Biochemistry 25, 5322-5328
41. Nakajima, M., Irimura, T., and Nicolson, G.L. (1988) Heparanases and tumor metastasis. J. Cell Biochem. 36, 157-167
42. Lapierre, F., Holme, K., Lam, L., Tressler, R.J., Storm, N., Wee, J., Stack, R.J., Castellot, J., and Tyrell, D.J. (1996) Chemical modifications of heparin that diminish its anticoagulant but preserve its heparanase-inhibitory, angiostatic, anti-tumor and anti-metastatic properties. Glycobiology 6, 355-366
43. Engelberg, H. (1999) Actions of heparin that may affect the malignant process. Cancer 85, 257-272
44. Edovitsky, E., Elkin, M., Zcharia, E., Peretz, T., and Vlodavsky, I. (2004) Heparanase gene silencing, tumor invasiveness, angiogenesis, and metastasis. J. Natl Cancer Inst. 96, 1219-1230
45. Yayon, A., Klagsbrum, M., Esko, J.D., Leder, P., and Ornitz, D.M. (2001) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848
46. Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J., and Zako, M. (1999) Function of cell surface heparan sulfate proteoglycans. Ann. Rev. Biochem. 68, 729-777
47. Munesue, S., Kusano, Y., Oguri, K., Itano, N., Yoshitomi, Y., Nakanishi, H., Yamashina, I., and Okayama, M. (2002) The role of syndecan-2 in regulation of actin-cytoskeletal organization of Lewis lung carcinoma-derived metastatic clones. Biochem. J. 363, 201-209
48. Couchman, J.R. (2003) Syndecans: proteoglycan regulators of cell surface microdomains?. Nature Rev. 4, 926-937
49. Yu, W.H. and Woessner, J.F., Jr. (2000) Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J. Biol. Chem. 275, 4183-4191
50. Guo, H., Li, R., Zucker, S., and Toole, B.P. (2000) EMMPRIN (CD147), an inducer of matrix metalloproteinase synthesis, also binds interstitial collagenase to the tumor cell surface. Cancer Res. 60, 888-891
51. Omura, T.H., Noguchi, A., Johanns, C.A., Jeffrey, J.J., and Partridge, N.C. (1994) Identification of a specific receptor for interstitial collagenase on osteoblastic cells. J.Biol. Chem. 269, 24994-24998
52. Fridman, R., Toth, M., Chvyrkova, I., Meroueh, S.O., and Mobashery, S. (2003) Cell surface association of matrix metalloproteinase-9 (gelatinase B). Cancer Metastasis Rev. 22, 153-166
53. Olsen, M.W., Toth, M., Gervasi, D.C., Sado, Y., Ninomiya, Y., and Fridman, R. (1998) High affinity binding of latent matrix metalloproteinase-9 to the alpha2(IV) chain of collagen IV. J. Biol. Chem. 273, 10672-10681
54. Stefanidakis, M., Bjorklund, M., Ihanus, E., Gahmberg, C.G., and Koivunen, E. (2003) Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins. J. Biol. Chem. 278, 34674-34684
55. Bourguignon, L.Y., Gunja-Smith, Z., Iida, N., Zhu, H.B., Young, L.J., Muller, W.J., and Cardiff, R.D. (1998) CD44v (3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J. Cell Physiol. 176, 206-215
56. Karadag, A., Fedarko, N.S., and Fisher, L.W. (2005) Dentin matrix protein 1 enhances invasion potential of colon cancer cells by bridging matrix metalloproteinase-9 to integrins and CD44. Cancer Res. 65, 11545-11552
57. Bennett, K.L., Jackson, D.G., Simon, J.C., Tanczos, E., Peach, R., Modrell, B., Stamenkovic, I., Plowman, G., and Aruffo, A. (1995) CD44 isoforms containing exon V3 are responsible for the presentation of heparin-binding growth factor. J. Cell Biol. 128, 687-698