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. 1993 May;84(5):549–557. doi: 10.1111/j.1349-7006.1993.tb00175.x

Augmented Expression of a Type IV Collagen‐binding Protein in a Highly Metastatic Murine Fibrosarcoma Clone

Katsuhisa Kogawa 1, Yoshihiro Mogi 1, Tetsuji Takayama 1, Kazuhiko Koike 1, Naohito Yoshizaki 1, Hiroshi Muramatsu 1, Yoshiro Niitsu 1,✉
PMCID: PMC5919167  PMID: 8391525

Abstract

The adhesive properties of highly and weakly metastatic murine sarcoma (Meth A) clones were investigated. A highly metastatic clone, MH‐02, preferentially adhered to type IV collagen‐coated plastic dishes and to bovine pulmonary arterial endothelial cell‐coated plastic dishes as compared to a weakly metastatic clone, ML‐01. Pretreatment of MH‐02 and ML‐01 cells with antisera against MH‐02 cells resulted in almost equivalent adhesiveness to type IV collagen. Preincubation of 125I‐radiolabeled tumor cells with the antisera against MH‐02 significantly reduced the arrest of MH‐02 cells in the lung, but ML‐01 cells were not affected. The number of pulmonary metastatic nodules of MH‐02 cells was reduced to the same level as that of ML‐01 cells by preincubation of the tumor cells with the antisera in an experimental metastasis experiment. These results indicated that the high metastatic ability of MH‐02 can be attributed to its preferential adhesiveness to type IV collagen. The type IV collagen‐binding proteins of MH‐02 and ML‐01 were analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS‐PAGE) and autoradiography. Among several proteins which bound to type IV collagen, expression of a protein with a molecular weight of 29 kD was significantly greater in MH‐02 than in ML‐01. These results suggest that the greater adhesion of highly metastatic MH‐02 cells to type IV collagen is due to enhanced expression of the type IV collagen‐binding 29 kD protein.

Keywords: Meth A sarcoma, Highly metastatic clone, Type IV collagen‐binding protein

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REFERENCES

  • 1. ) Fidler , I. J.Tumor heterogeneity and the biology of cancer invasion and metastasis . Cancer Res. , 38 , 2651 – 2660 ( 1978. ). [PubMed] [Google Scholar]
  • 2. ) Sugerbaker , E. , Weingard , D. N. and Roseman , J. M.Observation on cancer metastasis in man . In “ Tumor Invasion and Metastasis ,” ed. Liotta L. A. and Hart I. R. , pp. 427 – 466 ( 1982. ). Nijhoff; , Boston . [Google Scholar]
  • 3. ) Nicolson , G. L.Cancer metastasis: organ colonization and the cell surface properties of malignant cells . Biochim. Biophys. Acta , 695 , 113 – 176 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 4. ) Liotta , L. A.Tumor invasion and metastasis: role of the basement membrane . Am. J. Pathol. , 117 , 339 – 348 ( 1984. ). [PMC free article] [PubMed] [Google Scholar]
  • 5. ) Fidler , I. J.Biological behavior of malignant melanoma cells correlated to their survival in vivo . Cancer Res. , 35 , 218 – 224 ( 1975. ). [PubMed] [Google Scholar]
  • 6. ) Starkey , L. , Jr. , Jones , W. and Hosick , H. L.Influence of migratory blood cells on the attachment of tumor cells to vascular endothelium . Int. J. Cancer , 34 , 535 – 543 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 7. ) Gasic , G. J. , Gasic , T. B. and Jimenes , S. A.Platelet aggregating material in mouse tumor cells. Removal and regeneration . Lab. Invest. , 36 , 413 – 419 ( 1977. ). [PubMed] [Google Scholar]
  • 8. ) Tohgo , A. , Tanaka , N. G. and Ogawa , H.Platelet aggregating activities of metastasizing tumor cells . Invasion Metastasis , 6 , 58 – 68 ( 1986. ). [PubMed] [Google Scholar]
  • 9. ) Tanaka , K. , Kohga , S. , Kinjo , M. and Kodama , Y.Tumor metastasis and thrombosis, with special reference to thromboplastic and fibrinolytic activities of tumor cells . Gann Monogr. Cancer Res. , 20 , 97 – 119 ( 1977. ). [Google Scholar]
  • 10. ) Kinjo , M. , Oka , K. , Naito , S. , Kohga , S. , Tanaka , K. , Oboshi , S. , Hayata , Y. and Yasumoto , K.Thromboplastic and fibrinolytic activities of cultured human cancer cell lines . Br. J. Cancer , 39 , 15 – 23 ( 1979. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. ) Sindeler , W. , Tralka , T. S. and Ketcham , A. S.Electron microscopic observation on formation of pulmonary metastases . J. Surg. Res. , 18 , 137 – 167 ( 1975. ). [DOI] [PubMed] [Google Scholar]
  • 12. ) Kramer , R. and Nicolson , G. L.Interaction of tumor cells with vascular endothelial cell monolayers: A model for metastatic invasion . Proc. Natl. Acad. Sci. USA , 76 , 5704 – 5708 ( 1979. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13. ) Vlodavsky , I. , Schirrmacher , V. , Ariav , Y. and Fuks , Z.Lymphoma cell interaction with cultured endothelial cells and with the subendothelial basal lamina: attachment, invasion and morphological appearance . Invasion Metastasis , 3 , 81 – 97 ( 1983. ). [PubMed] [Google Scholar]
  • 14. ) Zamora , P. , Danielson , K. G. and Hosick , H. L.Invasion of endothelial cell monolayers on collagen gels by cells from mammary tumor spheroids . Cancer Res. , 40 , 4631 – 4639 ( 1980. ). [PubMed] [Google Scholar]
  • 15. ) Heberern , C. and Zupehik , H. Z.Diversity of adhesion to basement membrane components for human pancreatic adenocarcinoma . Cancer Res. , 45 , 5246 – 5251 ( 1985. ). [PubMed] [Google Scholar]
  • 16. ) Terranova , V. , Liotta , L. A. , Russo , R. G. and Martin , G. R.Role of laminin in the attachment and metastasis of murine tumor cells . Cancer Res. , 42 , 2265 – 2269 ( 1982. ). [PubMed] [Google Scholar]
  • 17. ) Nicolson , G. L.Metastatic tumor cell attachment assay utilizing vascular endothelial cell monolayers . J. Histochem. Cytochem. , 30 , 214 – 220 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 18. ) Tao , T. and Johnson , L. K.Altered adhesiveness of tumor cell surface variants with reduced metastasizing capacity and reduced adhesiveness to vascular wall components in culture . Int. J. Cancer , 30 , 763 – 766 ( 1982. ). [DOI] [PubMed] [Google Scholar]
  • 19. ) Kramer , R. , Gonzalez , R. and Nicolson , G. L.Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells . Int. J. Cancer , 26 , 639 – 645 ( 1980. ). [DOI] [PubMed] [Google Scholar]
  • 20. ) Bal de Kier Joffe , E. , Puricelli , L. and De Lustig , E. S.Modified adhesion behavior after in vitro passage of two related murine mammary adenocarcinomas with different metastasizing ability . Invasion Metastasis , 6 , 302 – 312 ( 1986. ). [PubMed] [Google Scholar]
  • 21. ) Netland , P. A. and Zetter , B. R.Melanoma cell adhesion to defined extracellular matrix components . Biophys. Biochem. Res. Commun. , 139 , 515 – 522 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 22. ) Pierschbacher , M. D. and Rouslahti , E.Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule . Nature , 309 , 30 – 33 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 23. ) Iwamoto , Y. , Robey , F. A. , Graf , J. , Sasaki , M. , Kleinman , H. K. , Yamada , Y. and Martin , G. R.YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation . Science , 238 , 1132 – 1134 ( 1987. ). [DOI] [PubMed] [Google Scholar]
  • 24. ) Hamphreys , M. J. , Olden , K. and Yamada , K. M.A synthetic peptide from fibronectin inhibits experimental metastasis of melanoma cells . Science , 233 , 467 – 469 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 25. ) Niitsu , Y. , Watanabe , N. , Yamauchi , N. , Maeda , M. , Kogawa , K. , Kuriyama , H. , Neda , H. and Sone , H.The anti‐metastatic effect of tumor necrosis factor on the artificial metastasis . Cancer J. , 2 , 91 – 94 ( 1988. ). [Google Scholar]
  • 26. ) Mogt , Y. , Kogawa , K. , Takayama , T. , Yoshizaki , N. , Bannai , K. , Muramatsu , H. , Koike , K. , Kohgo , Y. , Watanabe , N. and Niitsu , Y.Platelet aggregation induced by adenosine diphosphate released from cloned murine fibrosarcoma cells is positively correlated with the experimental metastatic potential of the cells . Jpn. J. Cancer Res. , 82 , 192 – 198 ( 1991. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27. ) Fidler , I. J.Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125I‐5‐iodo‐2′‐deoxyuridine . J. Natl. Cancer Inst. , 45 , 773 – 782 ( 1970. ). [PubMed] [Google Scholar]
  • 28. ) Raz , A. and Lotan , R.Endogenous galactoside‐binding lectins: a new class of functional tumor cell surface molecules related to metastasis . Cancer Metastasis Rev. , 6 , 433 – 452 ( 1987. ). [DOI] [PubMed] [Google Scholar]
  • 29. ) McGuire , E. J. , Mascali , J. J. , Gardy , S. R. and Nicolson , G. L.Involvement of cell‐cell adhesion molecules in liver colonization by metastatic murine lymphoma/lymphosarcoma variants . Clin. Exp. Metastasis , 2 , 213 – 222 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 30. ) Mentzer , T. , Burrakoff , S. and Faller , D.Adhesion of T‐lymphocytes to human endothelial cells is regulated by the LFA‐1 membrane molecule . J. Cell Physiol. , 126 , 283 – 290 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 31. ) Shearman , P. J. , Gallatin , W. M. and Longenecker , B. M.Detection of a cell‐surface antigen correlated with organ‐specific metastasis . Nature , 286 , 267 – 269 ( 1980. ). [DOI] [PubMed] [Google Scholar]
  • 32. ) Alby , L. and Auerbach , R.Differential adhesion of tumor cells to capillary endothelial cells in vitro . Proc. Natl Acad. Sci. USA , 81 , 5739 – 5743 ( 1984. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33. ) Auerbach , R. , Lu , W. C. , Pardon , E. , Gumkowski , F. , Kaminska , G. and Kaminska , M.Specificity of adhesion between murine tumor cells and capillary endothelium . Cancer Res. , 47 , 1942 – 1946 ( 1987. ). [PubMed] [Google Scholar]
  • 34. ) Korach , S. , Poupon , M. F. and Du Villard , J. A.Differential adhesiveness of rhabdomyosarcoma‐derived cloned metastatic cell lines to vascular endothelial monolayers . Cancer Res. , 46 , 3624 – 3629 ( 1986. ). [PubMed] [Google Scholar]
  • 35. ) Wang , N. , Yu , S. H. , Liener , I. E. , Hebbel , R. P. , Watson , J. W. and Mckahn , C. F.Characterization of high‐ and low‐metastatic clones derived from a methylcholanthrene‐induced murine fibrosarcoma . Cancer Res. , 42 , 1898 – 1903 ( 1982. ). [PubMed] [Google Scholar]
  • 36. ) Nicolson , G. L. and Custead , S. E.Effects of chemotherapeutic drugs on platelet and metastatic tumor cell‐endothelial cell interactions such as a model for assessing vascular endothelial integrity . Cancer Res. , 45 , 331 – 336 ( 1985. ). [PubMed] [Google Scholar]
  • 37. ) Nicolson , G. L.Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites . Cancer Metastasis Rev. , 7 , 143 – 188 ( 1988. ). [DOI] [PubMed] [Google Scholar]
  • 38. ) Terranova , V. P. , Rao , C. N. , Kalebic , T. , Margulies , I. M. and Liotta , L. A.Laminin receptor on human breast carcinoma cells . Proc. Natl. Acad. Sci. USA , 80 , 444 – 448 ( 1981. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. ) Nicolson , G. L. , Irimura , T. , Gonzalez , R. and Rouslahti , E.The role of fibronectin in adhesion of metastatic melanoma cells to endothelial cells and their basal lamina . Exp. Cell Res. , 135 , 161 – 170 ( 1981. ). [DOI] [PubMed] [Google Scholar]
  • 40. ) Murray , C. J. , Liotta , L. A. , Rennard , S. I. and Martin , G. R.Adhesion characteristics of murine metastatic and non‐metastatic tumor cells in vitro . Cancer Res. , 40 , 347 – 351 ( 1980. ). [PubMed] [Google Scholar]
  • 41. ) Turley , E. A.Proteoglycans and cell adhesion. Their putative role during tumorigenesis . Cancer Metastasis Rev. , 3 , 325 – 339 ( 1984. ). [DOI] [PubMed] [Google Scholar]
  • 42. ) Rieber , M. , Gross , A. and Rieber , M. S.Relationship of a Mr 140 fibronectin receptor and other adhesion‐related glycoproteins to tumor cell‐cell interaction . Cancer Res. , 47 , 5127 – 5131 ( 1987. ). [PubMed] [Google Scholar]
  • 43. ) Kramer , R. H. , McDonald , K. A. , Crowly , E. , Ramos , D. M. and Damsky , C. H.Melanoma cell adhesion to basement membrane mediated by integrin‐related complexes . Cancer Res. , 49 , 393 – 402 ( 1989. ). [PubMed] [Google Scholar]
  • 44. ) Kramer , R. H. and Marks , M.Identification of integrin collagen receptors on human melanoma cells . J. Biol. Chem. , 264 , 4684 – 4688 ( 1989. ). [PubMed] [Google Scholar]
  • 45. ) Staatz , W. D. , Rajpara , S. M. , Wayner , E. A. , Carter , W. G. and Santoro , S. A.The membrane glycoprotein Ia‐IIa (VLA‐2) complex mediates the MgΨΨ‐dependent adhesion of platelets to collagen . J. Cell Biol. , 108 , 1917 – 1924 ( 1989. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. ) Semba , K. , Nishizawa , M. , Miyajima , N. , Yoshida , M. C. , Sukegawa , J. , Yamanashi , Y. , Sasaki , M. , Yamamoto , T. and Toyoshima , K.yes‐related protooncogene, syn, belongs to the protein‐tyrosine kinase family . Proc. Natl. Acad. Sci. USA , 83 , 5459 – 5463 ( 1986. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. ) Kawakami , T. , Pennington , C. Y. and Robbins , K. C.Isolation and oncogenic potential of a novel human src‐like gene . Mol. Cell Biol. , 6 , 4159 – 4201 ( 1986. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48. ) Kurkinen , M. , Taylor , A. , Garrels , J. I. and Hogan , B. L. M.Cell surface‐associated proteins which bind native type IV collagen or gelatin . J. Biol. Chem. , 259 , 5915 – 5922 ( 1984. ). [PubMed] [Google Scholar]
  • 49. ) Senior , R. M. , Hinek , A. , Griffin , G. L. , Pipoly , D. J. , Crouch , E. C. and Mechem , R. P.Neutrophils show chemotaxis to type IV collagen and its 7S domain and contain a 67kD type IV collagen binding protein with lectin properties . Am. J. Respir. Cell Mol. Biol. , 1 , 479 – 487 ( 1989. ). [DOI] [PubMed] [Google Scholar]
  • 50. ) Lu , M. L. , Beacham , D. A. and Jacobson , B. S.The identification and characterization of collagen receptors involved in Hela cell‐substratum adhesion . J. Biol. Chem. , 264 , 13546 – 13558 ( 1989. ). [PubMed] [Google Scholar]
  • 51. ) Mollenhauer , J. , Bee , J. A. , Lizarbe , M. A. and Von der Mark , K.Role of anchorin CII, a 31,000‐mol‐wt membrane protein, in the interaction of chondrocytes with type II collagen . J. Cell Biol. , 98 , 1572 – 1578 ( 1984. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

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