Long-lasting complete inhibition of human solid tumors in SCID mice by targeting endothelial cells of tumor vasculature with antihuman endoglin immunotoxin

Clinical Cancer Research

Volumn 3, Issue 7, 1997, Pages 1031-1044

  Seon, Ben K ^a   Matsuno, Fumihiko ^a   Haruta, Yuro ^a   Kondo, Masao ^a   Barcos, Maurice ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; ENDOGLIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY K 4 2 C 10; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER TRANSPLANTATION; COMBINED IMMUNODEFICIENCY; CYTOTOXICITY; DRUG EFFICACY; DRUG SPECIFICITY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; PRIORITY JOURNAL; TUMOR VASCULARIZATION; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; BREAST NEOPLASMS; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; IMMUNOTOXINS; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CELL SURFACE; SKIN TRANSPLANTATION; TRANSPLANTATION, HETEROLOGOUS; UMBILICAL VEINS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 0030858765     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Wingo, P. A., Tong T., and Bolden, S. Cancer Statistics, 1995. CA Cancer J. Clin., 45: 8-30, 1995.
2. Folkman, J. Anti-angiogenesis: new concept for therapy of solid tumors. Ann. Surg., 175: 409-416, 1972.
3. Auerbach, W., and Auerbach, R. Angiogenesis inhibition: a review. Pharmacol. Ther., 63: 265-311, 1994.
4. Bicknell, R., and Harris, A. L. Anticancer strategies involving the vasculature: vascular targeting and the inhibition of angiogenesis. Semin. Cancer Biol., 3: 399-407, 1992.
5. Denekamp, J. Angiogenesis, neovascular proliferation and vascular pathophysiology as targets for cancer therapy. Br. J. Radiol., 66: 181-196, 1993.
6. Thorpe, P. E., and Burrows, F. J. Antibody-directed targeting of the vasculature of solid tumors. Breast Cancer Res. Treat., 36: 237-251, 1995.
7. Haruta, Y., and Seon, B. K. Distinct human leukemia-associated cell surface glycoprotein GP160 defined by monoclonal antibody SN6. Proc. Natl. Acad. Sci. USA, 83: 7898-7902, 1986.
8. Matsuzaki, H., Haruta, Y., and Seon, B. K. Effect of induced transformation of human leukemia cells on the expression of GP160, a novel human leukemia-associated cell surface glycoprotein. Fed. Proc., 46: 1056, 1987.
9. Gougos, A., and Letarte, M. Identification of a human endothelial cell antigen with monoclonal antibody 44G4 produced against a pre-B leukemic cell line. J. Immunol., 141: 1925-1933, 1988.
10. Gougos, A., and Letarte, M. Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J. Biol. Chem., 265: 8361-8364, 1990.
11. Cheifetz, S., Bellón, T., Calés, C., Vera, S., Bernabéu, C., Massagúe, J., and Letarte, M. Endoglin is a component of the transforming growth factor-β receptor system in human endothelial cells. J. Biol. Chem., 267: 19027-19030, 1992.
12. Bellón, T., Corbí, A., Lastres, P., Calés, C., Cebrián, M., Vera, S., Cheifetz, S., Massagué, J., Letarte, M., and Bernabéu. C. Identification and expression of two forms of the human transforming growth factor-β-binding protein endoglin with distinct cytoplasmic regions. Eur. J. Immunol., 23: 2340-2345, 1993.
13. Kishimoto, T., Goyert, S., Kikutani, H., Mason, D., Miyasaka, M., Moretta, L., Ohno, T., Okumura, K., Shaw, S., Springer, T. A., Sugamura, K., Sugawara, H., Kr. von dem Borne, A. E. G., and Zola, H. (eds.). Leukocyte Typing VI: White Cell Differentiation Antigens, in press. New York: Garland Publishing, Inc., 1997.
14. Burrows, F. J., Derbyshire, E. J., Tazzari, P. L., Amlot, P., Gazdar, A. F., King, S. W., Letarte, M., Vitetta, E. S., and Thorpe, P. E. Up-regulation of endoglin on vascular endothelial cells in human solid tumors: implications for diagnosis and therapy. Clin. Cancer Res., 1: 1623-1634, 1995.
15. Wang, J. M., Kumar, S., Pye, D., van Agthoven, A. J., Krupinski, J., and Hunter, R. D. A monoclonal antibody detects heterogeneity in vascular endothelium of tumours and normal tissues. Int. J. Cancer, 54: 363-370, 1993.
16. Dighiero, G. Autoreactive B-cell repertoire. In: Molecular Immunobiology of Self Reactivity, C. Bona and A. Kaushik (eds.), pp. 39-60. New York: Marcel Dekker, 1992.
17. O'Connell K. A., and Edidin, M. A mouse lymphoid endothelial cell line immortalized by simian virus 40 binds lymphocytes and retains functional characteristics of normal endothelial cells. J. Immunol., 144: 521-525, 1990.
18. Soule, H. D., Vazquez, J., Long, A., Albert, S., and Brennan, M. A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst., 51: 1409-1416, 1973.
19. Hara, H., and Seon, B. K. Complete suppression of in vivo growth of human leukemia cells by specific immunotoxins: nude mouse models. Proc. Natl. Acad. Sci. USA, 84: 3390-3394, 1987.
20. Kawata, A., Yoshida, M., Okazaki, M., Yokota, S., Barcos, M., and Seon, B. K. Establishment of new SCID and nude mouse models of human B leukemia/lymphoma and effective therapy of the tumors with immunotoxin and monoclonal antibody: marked difference between the SCID and nude mouse models in the antitumor efficacy of monoclonal antibody. Cancer Res., 54: 2688-2694, 1994.
21. Matsuzaki, H., Fukukawa, T., and Seon, B. K. Simple solid-phase radioimmunoassay for human leukemia-associated cell membrane antigens. J. Immunol. Methods, 81: 55-63, 1985.
22. Seon, B. K., Negoro, S., Minowada, J., and Yoshizaki, K. Human T cell leukemia antigens on the cell membranes: purification, molecular characterization, and preparation of specific antisera. J. Immunol, 127: 2580-2588, 1981.
23. Merril, C. R., Goldman, D., Sedman, S. A., and Ebert, M. H. Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science (Washington DC), 211: 1437-1438, 1981.
24. Seon, B. K., Negoro, S., and Barcos, M. P. Monoclonal antibody that defines a unique human T cell leukemia antigen. Proc. Natl. Acad. Sci. USA, 80: 845-849, 1983.
25. Matsuzaki, H., and Seon, B. K. Molecular nature of a cell membrane antigen specific for human T-cell acute lymphoblastic leukemia. Cancer Res., 47: 4283-4286, 1987.
26. Goding, J. W. Conjugation of antibodies with fluorochromes: modifications to the standard methods. J. Immunol. Methods. 13: 215-226, 1976.
27. Kawata, A., Han, T., Dadey, B., Weier, H-U. G., Okazaki, M., Yokota, S., Fukiage, T., Xiao, H., Block, A. M., Barcos, M., Henderson, E., Yoshida, M., and Seon, B. K. Establishment and characterization of the tumors of chronic lymphocytic leukemia cell line in nude and SCID mice. Leukemia Res., 17: 883-894, 1993.
28. Thorpe, P. E., Wallace, P. M., Knowles, P. P., Relf, M. G., Brown, A. N. F., Watson, G. J., Knyba, R. E., Wawrzynczak, E. J., and Blakey, D. C. New coupling agents for the synthesis of immunotoxins containing a hindered disulfide bond with improved stability in vivo. Cancer Res., 47: 5924-5931, 1987.
29. May, R. D., Finkelman, F. D., Wheeler, H. T., Uhr, J. W., and Vitetta, E. S. Evaluation of ricin A chain-containing immunotoxins directed against different epitopes on the 8-chain of cell surface-associated IgD on murine B cells. J. Immunol., 144: 3637-3642, 1990.
30. Rimm, A. A., Hartz, A. J., Kalbfleisch, J. H., Anderson, A. J., and Hoffmann, R. G. Basic Biostatistics in Medicine and Epidemiology, pp. 267-272. New York: Appleton-Century-Crofts, 1980.
31. 121. Cancer Res., 55: 5296-5301, 1995.
32. Ono, M., Kawahara, N., Goto, D., Wakabayashi, Y., Ushiro, S., Yoshida, S., Izumi, H., Kuwano, M., and Sato, Y. Inhibition of tumor growth and neovascularization by an anti-gastric ulcer agent, irsogladine. Cancer Res., 56: 1512-1516, 1996.
33. Rokhlin, O. W., Cohen, M. B., Kubagawa, H., Letarte, M., and Cooper, M. D. Differential expression of endoglin on fetal and adult hematopoietic cells in human bone marrow. J. Immunol., 154: 4456-4465, 1995.
34. Vickers, P. J., Dickson, R. B., Shoemaker, R., and Cowan, K. H. A multidrug-resistant MCF-7 human breast cancer cell line which exhibits cross-resistance to antiestrogens and hormone-independent tumor growth in vivo. Mol. Endocrinol., 2, 886-892, 1988.
35. Seon, B. K. Specific killing of human T leukemia cells by immunotoxins prepared with ricin A chain and monoclonal anti-human T-cell leukemia antibodies. Cancer Res., 44: 259-264, 1984.
36. Blakey, D. C., Watson, G. J., Knowles, P. P., and Thorpe, P. E. Effect of chemical deglycosylation of ricin A chain on the in vivo fate and cytotoxic activity of an immunotoxin composed of ricin A chain and anti-Thy 1.1 antibody. Cancer Res., 47: 947-952, 1987.
37. 1 tumor: effect of immunotoxin valency and deglycosylation of the ricin A chain. Cancer Res., 48: 2626-2631, 1988.
38. Folkman, J., and Shing, Y. Angiogenesis. J. Biol. Chem., 267: 10931-10934, 1992.
39. Sipos, E. P., Tamargo, R. J., Weingart, J. D., and Brem, H. Inhibition of tumor angiogenesis. Ann. NY Acad. Sci., 732: 263-272, 1994.
40. Kerbel, R. S. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents. Bioassays, 13: 31-36, 1991.
41. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med., 1: 27-31, 1995.
42. Jain, R. K. Barriers to drug delivery in solid tumors. Sci. Am., 271: 58-65, 1994.
43. Dvorak, H. F., Nagy, J. A., and Dvorak, A. M. Structure of solid tumors and their vasculature: implications for therapy with monoclonal antibodies. Cancer Cells, 3: 77-85, 1991.
44. Burrows, F. J., and Thorpe, P. E. Eradication of large solid tumors in mice with an immunotoxin directed against tumor vasculature. Proc. Natl. Acad. Sci. USA. 90: 8996-9000, 1993.
45. 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell, 79: 1157-1164, 1994.
46. Ramakrishnan, S., Olson, T. A., Bautch, V. L., and Mohanraj, D. Vascular endothelial growth factor-toxin conjugate specifically inhibits KDR/flk-1-positive endothelial cell proliferation in vitro and angiogenesis in vivo. Cancer Res., 56: 1324-1330, 1996.
47. Hawkins, M. J. Clinical trials of antiangiogenic agents. Curr. Opin. Oncol., 7: 90-93, 1995.
48. Kim, K. J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H. S., and Ferrara, N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature (Lond.) 562: 841-844, 1993.
49. O'Reilly, M. S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Moses, M., Lane, W. S., Cao, Y., Sage, E. H., and Folkman, J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell, 79: 315-328, 1994.
50. Voest, E. E., Kenyon, B. M., O'Reilly, M. S., Truitt, G., D'Amato, R. J., and Folkman, J. Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst., 87: 581-586, 1995.
51. Engerman, R. L., Pfaffenbach, D., and Davis, M. D. Cell turnover of capillaries. Lab. Invest., 17: 738-743, 1967.
52. Risau, W. Differentiation of endothelium. FASEB J., 9: 926-933, 1995.
53. Lastres, P., Bellón, T., Cabañas, C., Sanchez-Madrid, F., Acevedo, A., Gougos, A., Letarte, M., and Bernabéu, C. Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur. J. Immunol., 22: 393-397, 1992.
54. Kreitman, R. J., Chang, C. N., Hudson, D. V., Queen, C., Bailon, P., and Pastan, I. Anti-Tac(Fab)-PE40, a recombinant double-chain immunotoxin which kills interleukin-2-receptor-bearing cells and induces complete remission in an in vivo tumor model. Int. J. Cancer, 57: 856-864, 1994.
55. Benhar, I., Reiter, Y., Pai, L. H., and Pastan, I. Administration of disulfide-stabilized Fv-immunotoxins B1 (dsFv)-PE38 and B3 (dsFv)-PE38 by continuous infusion increases their efficacy in curing large tumor xenografts in nude mice. Int. J. Cancer, 62: 351-355, 1995.
56. Siegall, C. B., Chace, D., Mixan, B., Garrigues, U., Wan, H., Paul, L., Wolff, E., Hellström, I., and Hellström, K. E. In vitro and in vivo characterization of BR96 sFv-PE40: a single-chain immunotoxin fusion protein that cures human breast carcinoma xenografts in athymic mice and rats. J. Immunol., 152: 2377-2384, 1994.
57. Folkman, J. Clinical applications of research on angiogenesis. N. Engl. J. Med. 333: 1757-1763, 1995.
58. Huang, X., Molema, G., King, S., Watkins, L., Edgington, T. S., and Thorpe, P. E. Tumor infarction in mice by antibody-directed targeting of tissue factor to tumor vasculature. Science (Washington DC), 275: 547-550, 1997.
59. O'Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., Flynn, E., Birkhead, J. R., Olsen, B. R., and Folkman, J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell, 88: 277-285, 1997.