CD44/chondroitin sulfate proteoglycan and α2β1 integrin mediate human melanoma cell migration on type IV collagen and invasion of basement membranes

Molecular Biology of the Cell

Volumn 7, Issue 3, 1996, Pages 383-396

  Knutson, Jennifer R ^a   Iida, Joji ^a   Fields, Gregg B ^a,b   McCarthy, James B ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; HERMES ANTIGEN; INTEGRIN; LAMININ; MONOCLONAL ANTIBODY; PROTEOCHONDROITIN SULFATE;

ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PURIFICATION; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL SURFACE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; MELANOMA CELL; PRIORITY JOURNAL;

EID: 0029921188     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.3.383     Document Type: Article

References (85)

1. Albini, A., Iwamoto, Y., Kleinman, H.K., Martin, G.R., Aaronson, S.A., Kozlowski, J.M., and McEwan, R.N. (1987). A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res. 47, 3239-3245.
2. Altruda, F., Cervella, P., Tarone, G., Botta, C., Balzac, F., Stefanuto, G., and Silengo, L (1990). A human integrin β1 subunit with a unique cytoplasmic domain generated by alternative mRNA processing. Gene 95, 261-266.
3. Birch, M., Mitchell, S., and Hart, I.R. (1991). Isolation and characterization of human melanoma cell variants expressing high and low levels of CD44. Cancer Res. 51, 6660-6667.
4. Bosman, F.T. (1993). Integrins: cell adhesives and modulators of cell function. Histochem. J. 25, 469-477.
5. Bourguignon, L.Y.W., Lokeshwar, V.B., He, J., Chen, X., and Bourguignon, G.J. (1992). A CD44-like endothelial cell transmembrane glycoprotein (GP116) interacts with extracellular matrix and ankyrin. Mol. Cell Biol. 12, 4464-4471.
6. Bumol, T.F., and Reisfeld, R.A. (1982). Unique glycoprotein-proteoglycan complex defined by monoclonal antibody on human melanoma cells. Proc. Natl. Acad. Sci. USA 79, 1245-1249.
7. Cameron, J.D., Skubitz, A.P.N., and Furcht, L.T. (1991). Type IV collagen and corneal epithelial adhesion and migration: effects of type IV collagen fragments and synthetic peptides on rabbit corneal epithelial cell adhesion and migration in vitro. Invest. Ophthalmol. Vis. Sci. 32, 2766-2773.
8. Carter, W.G., and Wayner, E A. (1988). Characterization of the class III collagen receptor, a phosphorylated, transmembrane glycoprotein expressed in nucleated human cells. J. Biol. Chem. 263, 4193-4201.
9. Chan, B M., and Hemler, M.E. (1993). Multiple functional forms of the integrin VLA-2 can be derived from a single α2 cDNA clone: interconversion of forms induced by an anti-β1 antibody. J. Cell Biol. 120, 537-543.
10. Chan, B.M., Kassner, P.D., Schiro, J.A., Byers, H.R., Kupper, T.S., and Hemler, M.E. (1992). Distinct cellular functions mediated by different VLA integrin α subunit cytoplasmic domains. Cell 68, 1051-1060.
11. Chan, B.M., Matsuura, N., Takada, Y., Zetter, B.R., and Hemler, M.E. (1991). In vitro and in vivo consequences of VLA-2 expression on rhabdomyosarcoma cells. Science 251, 1600-1602.
12. Chattopadhyay, P., Starkey, J., Morrow, W.J., and Raychaudhuri, S. (1992) Murine monoclonal anti-idiotope antibody breaks unresponsiveness and induces a specific antibody response to human melanoma-associated proteoglycan antigen in cynomolgus monkeys. Proc. Natl. Acad. Sci. USA 89, 2684-2688.
13. Chattopadhyay, P , Starkey, J., and Raychaudhuri, S. (1991). Analysis of anti-tumor antibodies in mice and rabbits induced by monoclonal anti-idiotope antibodies. J. Immunol. 147, 2055-2062.
14. Chelberg, M K., McCarthy, J.B., Skubitz, A.P.N., Furcht, L.T., and Tsilibary, E.C. (1990). Characterization of a synthetic peptide from type IV collagen that promotes melanoma cell adhesion, spreading, and motility. J. Cell Biol. 111, 262-270.
15. Chelberg, M.K., Tsilibary, E.C., Hauser, A.R., and McCarthy, J.B. (1989). Type IV collagen-mediated melanoma cell adhesion and migration: involvement of multiple, distinct domains of the collagen molecule. Cancer Res. 49, 4796-4802.
16. Danen, E.H., van Muijen, G.N., van de Wiel-van Kemenade, E., Jansen, K.F., Ruiter, D.J., and Figdor, C G. (1993). Regulation of integrin-mediated adhesion to laminin and collagen in human melanocytes and in non-metastatic and highly metastatic human melanoma cells. Int. J. Cancer. 54, 315-321.
17. De Vries, J.E., Keizer, G.D., Te Velde, A.A., Voordouw, A., Ruiter, D., Rumke, P., Spits, H., and Figdor, C.G. (1986). Characterization of melanoma-associated surface antigens involved in the adhesion and motility of human melanoma cells. Int. J. Cancer 38, 465-473.
18. Dedhar, S., Saulnier, R., Nagle, R., and Overall, C.M. (1993). Specific alterations in the expression of α3β1 and α6β4 integrins in highly invasive and metastatic variants of human prostate carcinoma cells selected by in vitro invasion through reconstituted basement membrane. Clin. Exp. Metastasis 11, 391-400.
19. Elices, M.J., and Hemler, M.E. (1989). The human integrin VLA-2 is a collagen receptor on some cells and a collagen/laminin receptor on others. Proc. Natl. Acad. Sci. USA 86, 9906-9910.
20. Etoh, T., Byers, H.R., and Mihm, M.C. (1992). Integrin expression in malignant melanoma and their role in cell attachment and migration on extracellular matrix proteins. J. Dermatol. 19, 841-846.
21. Etoh, T., Thomas, L., Pastel-Levy, C., Colvin, R.B., Mihm, M.C., Jr., and Byers, H.R. (1993). Role of integrin α2β1 (VLA-2) in the migration of human melanoma cells on laminin and type IV collagen. J. Invest. Dermatol 100, 640-647.
22. Faassen, A.E., Drake, S.L., Iida, J., Knutson, J.R., and McCarthy, J.B. (1992a). Mechanisms of normal cell adhesion to the extracellular matrix and alterations associated with tumor invasion and metastasis. Adv. Pathol. Lab. Med. 5, 229-259.
23. Faassen, A E., Mooradian, D.L., Tranquillo, R.T., Dickinson, R B., Letourneau, P.C., Oegema, T.R., and McCarthy, J.B. (1993). Cell surface CD44-related chondroitin sulfate proteoglycan is required for transforming growth factor-β-stimulated mouse melanoma cell motility and invasive behavior on type I collagen. J. Cell Sci. 105, 501-511.
24. Faassen, A.E., Schrager, J.A., Klein, D.J., Oegema, T.R., Couchman, J.R., and McCarthy, J.B. (1992b). A cell surface chondroitin sulfate proteoglycan, immunologically related to CD44, is involved in type I collagen-mediated melanoma cell motility and invasion. J. Cell Biol. 116, 521-531.
25. Fields, C.G., Mickelson, D.J., Drake, S.L., McCarthy, J.B., and Fields, G.B. (1993). Melanoma cell adhesion and spreading activities of a synthetic 124-residue triple-helical "mini-collagen". J. Biol. Chem. 268, 14153-14160.
26. Furcht, L.T., McCarthy, J.B., Palm, S L., Basara, M.L., and Enenstein, J. (1984). Peptide fragments of laminin and fibronectin promote migration (haptotaxis and chemotaxis) of metastatic cells. Ciba Found. Symp. 108, 130-145.
27. Gallagher, J.T. (1989). The extended family of proteoglycans: social residents of the pericellular zone. Curr. Opin. Cell Biol 1, 1201-1218.
28. Gallatin, W.M., Wayner, E.A., Hoffman, P.A., St. John, T., Butcher, E.G., and Carter, W.G. (1989). Structural homology between lymphocyte receptors for high endothelium and class III extracellular matrix receptor. Proc. Natl. Acad. Sci. USA 86, 4654-4658.
29. Gehlsen, K.R., Davis, G.E., and Sriramarao, P. (1992a). Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin. Exp. Metastasis 10, 111-120.
30. Gehlsen, K.R., Sriramarao, P., Furcht, L.T., and Skubitz, A.P N. (1992b). A synthetic peptide derived from the carboxy terminus of the laminin A chain represents a binding site for the α3β1 integrin. J. Cell Biol. 117, 449-459
31. Geppert, T.D., and Lipsky, P.E. (1991). Association of various T cell-surface molecules with the cytoskeleton: effect of cross-linking and activation. J. Immunol. 146, 3298-3305.
32. Gunthert, U., Hofmann, M., Rudy, W., Reber, S., Zoller, M., Haubmann, I., Matzku, S., Wenzel, A., Ponta, H., and Herrlich, P. (1991). A new variant of glycoprotein CD44 confers metastatic potential to rat carcinoma cells. Cell 65, 13-24.
33. Harper, J.R., Bumol, T.F., and Reisfeld, R.A. (1984). Characterization of monoclonal antibody 155.8 and partial characterization of its proteoglycan antigen on human melanoma cells. J. Immunol. 132, 2096-2104.
34. Harper, J.R., and Reisfeld, R.A. (1983). Inhibition of anchorage-independent growth of human melanoma cells by a monoclonal antibody to a chondroitin sulfate proteoglycan. J. Natl. Cancer Inst. 71, 259-263.
35. Honn, K.V., and Tang, D.G. (1992). Adhesion molecules and tumor cell interaction with endothelium and subendothelial matrix. Cancer Metastasis Rev. 11, 353-375.
36. Iwamoto, Y., Robey, F.A., Graf, J., Sasai, M., Kleinman, H.K., Yamada, Y., and Martin, G.R. (1987). YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 238, 1132-1134.
37. Jacobson, K., O'Dell, D., Holifield, B., Murphy, T.L., and August, T. (1984). Redistribution of a major cell surface glycoprotein during cell movement. J. Cell Biol. 99, 1613-1623.
38. Jalkanen, S., Bargatze, R.F., de los Toyos, J., and Butcher, E.C. (1987). Lymphocyte recognition of high endothelium: antibodies to distinct epitopes of an 85-95 kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells. J. Cell Biol. 105, 983-990.
39. Kalomiris, E.L., and Bourguignon, L.Y.W. (1988). Mouse T lymphoma cells contain a transmembrane glycoprotein (gp85) that binds ankyrin. J. Cell Biol. 106, 319-327.
40. Kanemoto, T., Martin, G.R., Hamilton, T.C., and Fridman, R. (1991). Effects of synthetic peptides and protease inhibitors on the interaction of a human ovarian cancer cell line (NIH:OVCAR-3) with a reconstituted basement membrane (Matrigel). Invasion Metastasis 11, 84-92.
41. Kapron-Bras, C., Fitz-Gibbon, L., Jeevaratnam, P., Wilkins, J., and Dedhar, S. (1993). Stimulation of tyrosine phosphorylation and accumulation of GTP-bound p21ras upon antibody-mediated α2β1 integrin activation in T-lymphoblastic cells. J. Biol. Chem. 268, 20701-20704.
42. Karecla, P.I., Timpl, R., and Watt, F.M. (1994). Adhesion of human epidermal keratinocytes to laminin. Cell Adh. Commun. 2, 309-318.
43. Kawasaki, K., Murakami, T., Namikawa, M., Mizuta, T., Iwai, Y., Yamashiro, Y., Hama, T., Yamamoto, S., and Mayumi, T. (1994). Amino acids and peptides. XXI. Laminin-related peptide analogs including poly(ethylene glycol) hybrids and their inhibitory effect on experimental metastasis. Chem. Pharmacol. Bull. 42, 917-921.
44. Kramer, R.H., and Marks, N. (1989). Identification of integrin collagen receptors on human melanoma cells. J Biol. Chem. 264, 4684-4688.
45. Lacy, B.E., and Underhill, C.B. (1987) The hyaluronate receptor is associated with actin filaments. J. Cell Biol. 105, 1395-1404.
46. Lallier, T., Deutzmann, R., Perris, R., and Bronner-Fraser, M. (1994). Neural crest cell interactions with laminin: structural requirements and localization of the binding site for α1β1 integrin. Dev. Biol. 162, 451-464.
47. Larjava, H., Lyons, J.G., Salo, T., Makela, M., Koivisto, L., Birkedal-Hansen, H., Akiyama, S.K., Yamada, K.M., and Heino, J. (1993). Anti-integrin antibodies induce type IV collagenase expression in keratinocytes. J. Cell. Physiol. 157, 190-200.
48. Leavesley, D.I., Schwartz, M.A., Rosenfeld, M., and Cheresh, D.A. (1993). Integrin β1- and β3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J. Cell Biol. 121, 163-170.
49. Lesley, J., Hyman, R., and Kincade, P.W. (1993). CD44 and its interactions with extracellular matrix. Adv. Immunol. 54, 271-335.
50. Lynch, S.A., Bouchard, B.N., Vijayasaradhi, S., Yuasa, H., and Houghton, A.N. (1991). Antigens of melanocytes and melanoma. Cancer Metastasis Rev. 10, 141-150.
51. Matsumura, Y., and Tarin, D. (1992). Significance of CD44 gene products for cancer diagnosis and disease evaluation. Lancet 340, 1053-1058.
52. Matter, M.L., and Laurie, G.W. (1994). A novel laminin E8 cell adhesion site required for lung alveolar formation in vitro. J. Cell Biol. 124, 1083-1090.
53. Melchiori, A., Mortarini, R., Carlone, S., Marchisio, P.C., Anichini, A., Noonan, D.M., and Albini, A. (1995). The α3β1 integrin is involved in melanoma cell migration and invasion. Exp. Cell Res. 219, 233-242.
54. Merzak, A., Koocheckpour, S., and Pilkington, G.J. (1994). CD44 mediates human glioma cell adhesion and invasion in vitro. Cancer Res. 54, 3988-3992.
55. Miyamoto, S., Akiyama, S.K., and Yamada, K.M. (1995). Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267, 883-885.
56. Moczar, M., Caux, F., Bailly, M., Berthier, O., and Dore, J.F. (1993). Accumulation of heparan sulfate in the culture of human melanoma cells with different metastatic ability. Clin. Exp. Metastasis 11, 462-471.
57. Mortarini, R., Anichini, A., and Parmiani, G. (1991). Heterogeneity for integrin expression and cytokine-mediated VLA modulation can influence the adhesion of human melanoma cells to extracellular matrix proteins. Int. J. Cancer 47, 551-559.
58. Nakai, M., Mundy, G.R., Williams, P.J., Boyce, B., and Yoneda, T. (1992). A synthetic antagonist to laminin inhibits the formation of osteolytic metastases by human melanoma cells in nude mice. Cancer Res. 52, 5395-5399.
59. Nishiyama, A., and Stallcup, W.B. (1993). Expression of NG2 proreoglycan causes retention of type VI collagen on the cell surface. Mol. Biol. Cell 4, 1097-1108.
60. Nomizu, M., Yamamura, K., Kleinman, H.K., and Yamada, Y. (1993). Multimeric forms of Tyr-Ile-Gly-Ser-Arg (YIGSR) peptide enhance the inhibition of tumor growth and metastasis. Cancer Res. 53, 3459-3461.
61. Oegema, T.R., Hascall, V.C., and Eisenstein, R. (1979). Characterization of bovine aorta proteoglycan extracted with guanidine hydrochloride in the presence of protease inhibitors. J. Biol. Chem. 254, 1312-1318.
62. Paulsson, M. (1992). Basement membrane proteins: structure, assembly, and cellular interactions. Crit. Rev. Biochem. Mol. Biol. 27, 93-127.
63. Paulus, W., and Tonn, J.C. (1994). Basement membrane invasion of glioma cells mediated by integrin receptors. J. Neurosurg. 80, 515-519.
64. Perris, R., Syfrig, J., Paulsson, M., and Bronner-Fraser, M. (1993). Molecular mechanisms of neural crest cell attachment and migration on types I and IV collagen. J. Cell Sci. 106, 1357-1368.
65. Perschl, A., Lesley, J., English, N., Trowbridge, I., and Hyman, R. (1995). Role of CD44 cytoplasmic domain in hyaluronan binding. Eur. J. Immunol. 25, 495-501.
66. Riikonen, T., Westermarck, J., Koivisto, L., Broberg, A., Kahari, V.M., and Heino, J. (1995). Integrin α2β1 is a positive regulator of collagenase (MMP-1) and collagen α1(I) gene expression. J. Biol. Chem. 270, 13548-13552.
67. Rudy, W., Hofmann, M., Schwart-Albieez, R., Zoller, M., Heider, K.H., Ponta, H., and Herrlich, P. (1993). The two major CD44 proteins expressed on a metastatic rat tumor cell line are derived from different splice variants: each one individually suffices to confer metastatic behavior. Cancer Res. 53, 1262-1268.
68. Ruoslahti, E. (1988). Structure and biology of proteoglycans. Annu. Rev. Cell Biol. 4, 229-255.
69. Sanchez-Mateos, P., Arroyo, A.G., Balboa, M.A., and Sanchez-Madrid, F. (1993). Post-receptor occupancy events in leukocytes during β1 integrin-ligand interactions. Eur. J. Immunol. 23, 2642-2648.
70. Seftor, R.E., Seftor, E.A., Stetler-Stevenson, W.G., and Hendrix, M.J. (1993). The 72 kDa type IV collagenase is modulated via differential expression of αvβ3 and α5β1 integrins during human melanoma cell invasion. Cancer Res. 53, 3411-3415.
71. Seltzer, J.L., Lee, A.Y., Akers, K.T., Sudbeck, B., Southon, E.A., Wayner, E.A., and Eisen, A.Z. (1994). Activation of 72-kDa type IV collagenase/gelatinase by normal fibroblasts in collagen lattices is mediated by integrin receptors but is not related to lattice contraction. Exp. Cell Res. 213, 365-374.
72. Simon-Assmann, P., Leberquier, C., Molto, N., Uezato, T., Bouziges, F., and Kedinger, M. (1994). Adhesive properties and integrin expression profiles of two colonic cancer populations differing by their spreading on laminin. J. Cell Sci. 107, 577-587.
73. Spiro, R.C., Freeze, H.H., Sampath, D., and Garcia, J.A. (1991). Uncoupling of chondroitin sulfate glycosaminoglycan synthesis by Brefeldin A. J. Cell Biol. 115, 1463-1473.
74. Stallcup, W.B., Dahlin, K., and Healy, P. (1990). Interaction of the NG2 chondroitin sulfate proteoglycan with tvpe VI collagen. J. Cell Biol. 111, 3177-3188.
75. Stetler-Stevenson, W.G., Aznavoorian, S., and Liotta, L.A. (1993). Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu. Rev. Cell Biol. 9, 541-573.
76. Tamura, R.N., Cooper, H.M., Collo, G., and Quaranta, V. (1991). Cell-type specific integrin variants with alternative α chain cytoplasmic domains. Proc. Natl. Acad. Sci. USA 88, 10183-10187.
77. Tarone, G., Ferracini, R., Galetto, G., and Comoglio, P. (1984). A cell surface integral membrane glycoprotein of 85,000 mol. wt. (gp85) associated with Triton X-100-insoluble cell skeleton. J. Cell Biol. 99, 512-519.
78. Thomas, L., Etoh, T., Stamenkovic, I., Mihm, M.C., Jr., and Byers, H.R. (1993). Migration of human melanoma cells on hyaluronate is related to CD44 expression. J. Invest. Dermatol. 100, 115-120.
79. Wayner, E.A., and Carter, W.G. (1987). Identification of multiple cell adhesion receptors for collagen and fibronecrin in human fibrosarcoma cells possessing unique α and common β subunits. J. Cell Biol. 105, 1873-1884.
80. Wayner, E.A., Carter, W.G., Piotrowicz, R.S., and Kunicki, T.J. (1988). The function of multiple extracellular matrix receptors in mediating cell adhesion to extracellular matrix: preparation of monoclonal antibodies to the fibronecrin receptor that specifically inhibit cell adhesion to fibronectin and react with platelet glycoproteins Ic-IIa. J. Cell Biol. 107, 1881-1891.
81. Wilke, M.S., and Skubitz, A.P.N. (1991). Human keratinocytes adhere to multiple distinct peptide sequences of laminin. J. Invest. Dermatol. 97, 141-146.
82. Yamada, K.M., Kennedy, D.W., Yamada, S.S., Gralnick, H., Chen, W T, and Akiyama, S.K. (1990). Monoclonal antibody and synthetic peptide inhibitors of human tumor cell migration. Cancer Res 50, 4485-4496.
83. Yamamura, K., Kibbey, M.C., and Kleinman, H.K. (1993). Melanoma cells selected for adhesion to laminin peptides have different malignant properties. Cancer Res. 53, 423-428.
84. Yoshinaga, I.G., Vink, J., Dekker, S.K., Mihm, M.C., and Byers, H.R. (1993). Role of α3β1 and α2β1 integrins in melanoma cell migration. Melanoma Res. 3, 435-441.
85. Zhao, M., Kleinman, H.K., and Mokotoff, M. (1994). Synthetic laminin-like peptides and pseudopeptides as potential antimetastatic agents. J. Med. Chem. 37, 3383-3388.