Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo

Journal of Clinical Investigation

Volumn 102, Issue 8, 1998, Pages 1599-1608

  Sharma, Bela ^a   Handler, Melissa ^a   Eichstetter, Inge ^a   Whitelock, John M ^b   Nugent, Matthew A ^c   Iozzo, Renate V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b CSIRO   (Australia)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FGF 2; FGF 7; Fibroblast growth factor; Heparan sulfate; Proteoglycans

Indexed keywords

KERATINOCYTE GROWTH FACTOR; PERLECAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION;

EID: 3643129096     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI3793     Document Type: Article

References (41)

1. Hanahan, D., and J. Folkman. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353-364.
2. Holmgren, L., M. O'Reilly, and J. Folkman. 1995. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1:149-153.
3. O'Reilly, M.S., L. Holmgren, C. Chen, and J. Folkman. 1996. Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat. Med. 2: 689-692.
4. Folkman, J., and P.A. D'Amore. 1996. Blood vessel formation: what is its molecular basis? Cell. 87:1153-1155.
5. Iozzo, R.V. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67:609-652.
6. Noonan, D.M., A. Fulle, P. Valente, S. Cai, E. Horigan, M. Sasaki, Y. Yamada, and J.R. Hassell. 1991. The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J. Biol. Chem. 266:22939-22947.
7. Iozzo, R.V., I.R. Cohen, S. Grässel, and A.D. Murdoch. 1994. The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem. J. 302:625-639.
8. Handler, M., P.D. Yurchenco, and R.V. lozzo. 1997. Developmental expression of perlecan during murine embryogenesis. Dev. Dyn. 210:130-145.
9. Cohen, I.R., A.D. Murdoch, M.F. Naso, D. Marchetti, D. Berd, and R.V. Iozzo. 1994. Abnormal expression of perlecan proteoglycan in metastatic melanomas. Cancer Res. 54:5771-5774.
10. Timar, J., A. Ladanyi, K. Lapis, and M. Moczar. 1992. Differential expression of proteoglycans on the surface of human melanoma cells characterized by altered experimental metastatic potential. Am. J. Pathol 141:467-474.
11. Vigny, M., M.P. Ollier-Hartmann, M. Lavigne, N. Fayein, J.C. Jeanny, M. Laurent, and Y. Courtois. 1988. Specific binding of basic fibroblast growth factor to basement membrane-like structures and to purified heparan sulfate proteoglycan of the EHS tumor. J. Cell. Physiol. 137:321-328.
12. Aviezer, D., D. Hecht, M. Safran, M. Eisinger, G. David, and A. Yayon. 1994. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 79:1005-1013.
13. Yayon, A., M. Klagsbrun, J.D. Esko, P. Leder, and D.M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64:841-848.
14. Ornitz, D.M., A. Yayon, J.G. Flanagan, C.M. Svahn, E. Levi, and P. Leder. 1992. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol. Cell. Biol. 12:240-247.
15. Whitelock, J.M., A.D. Murdoch, R.V. Iozzo, and P.A. Underwood. 1996. The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin and heparanases. J. Biol. Chem. 271:10079-10086.
16. Aviezer, D., R.V. Iozzo, D.M. Noonan, and A. Yayon. 1997. Suppression of autocrine and paracrine functions of basic fibroblast growth factor by stable expression of perlecan antisense cDNA. Mol. Cell. Biol. 17:1938-1946.
17. Adatia, R., A. Albini, S. Carlone, D. Giunciuglio, R. Benelli, L. Santi, and D.M. Noonan. 1998. Suppression of invasive behavior of melanoma cells by stable expression of anti-sense perlecan cDNA. Ann. Oncol. 8:1257-1261.
18. Mathiak, M., C. Yenisey, D.S. Grant, B. Sharma, and R.V. Iozzo. 1997. A role for perlecan in the suppression of growth and invasion in fibrosarcoma cells. Cancer Res. 57:2130-2136.
19. Murdoch, A.D., G.R. Dodge, I. Cohen, R.S. Tuan, and R.V. Iozzo. 1992. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 267:8544-8557.
20. Santra, M., T. Skorski, B. Calabretta, E.C. Lattime, and R.V. Iozzo. 1995. De novo decorin gene expression suppresses the malignant phenotype in human colon cancer cells. Proc. Natl. Acad. Sci. USA. 92:7016-7020.
21. Sharma, B., and R.V. lozzo. 1998. Transcriptional silencing of perlecan gene expression by interferon-γ. J. Biol. Chem. 273:4642-4646.
22. Murdoch, A.D., B. Liu, R. Schwarting, R.S. Tuan, and R.V. Iozzo. 1994. Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. J. Histochem. Cytochem. 42:239-249.
23. Fannon, M., and M.A. Nugent. 1996. Basic fibroblast growth factor binds its receptors, is internalized, and stimulates DNA synthesis in Balb/c3T3 cells in the absence of heparan sulfate. J. Biol. Chem. 271:17949-17956.
24. Basilico, C., and D. Moscatello. 1992. The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59:115-165.
25. Aaronson, S.A., D.P. Bottaro, T. Miki, D. Ron, P.W. Finch, T.P. Fleming, J. Ahn, W.G. Taylor, and J.S. Rubin. 1991. Keratinocyte growth factor. A fibroblast growth factor family member with unusual target cell specificity. Ann. NY Acad. Sci. 638:62-77.
26. Wang, Y., and D. Becker. 1997. Antisense targeting of basic fibroblast growth factor and fibroblast growth factor receptor-1 in human melanomas blocks intratumoral angiogenesis and tumor growth. Nat. Med. 3:887-893.
27. Weidner, N., J.P. Semple, W.R. Welch, and J. Folkman. 1991. Tumor angiogenesis and metastasis: correlation in invasive breast carcinoma. N. Engl. J. Med. 324:1-8.
28. Talmadge, J.E., and I.J. Fidler. 1982. Enhanced metaslatic potential of tumor cells harvested from spontaneous metastases of heterogenous murine tumors. J. Natl. Cancer Inst. 69:975-980.
29. Becker, D., C.B. Meier, and M. Herlyn. 1989. Proliferation of human malignant melanomas is inhibited by antisense oligodeoxynucleotides targeted against basic fibroblast growth factor. EMBO (Eur. Mol. Biol. Organ.) J. 8: 3685-3691.
30. Kistner, A., M. Gossen, F. Zimmermann, J. Jerecic, C. Ullmer, H. Lübbert, and H. Bujard. 1996. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice. Proc. Natl. Acad. Sci. USA. 93:10933-10938.
31. Skobe, M., P. Rockwell, N. Goldstein, S. Vosseler, and N.E. Fusenig. 1997. Halting angiogenesis suppresses carcinoma cell invasion. Nat. Med. 3: 1222-1227.
32. Parangi, S., M. O'Reilly, G. Christofori, L. Holmgren, J. Grosfeld, J. Folkman, and D. Hanahan. 1996. Antiangiogenic therapy of transgenic mice impairs de novo tumor growth. Proc. Natl. Acad. Sci. USA. 93:2002-2007.
33. Iozzo, R.V., and A.D. Murdoch. 1996. Proteoglycans of the extracellular environment: clues from the gene and protein side offer novel perspectives in molecular diversity and function. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:598-614.
34. Benitz, W.E., R.T. Kelley, C.M. Anderson, D.E. Lorant, and M. Bernfield. 1990. Endothelial heparan sulfate proteoglycan. I. Inhibitory effects on smooth muscle cell proliferation. Am. J. Respir. Cell Mol. Biol. 2:13-24.
35. Forsten, K.E., N.A. Courant, and M.A. Nugent. 1997. Endothelial proteoglycans inhibit bFGF binding and mitogenesis. J. Cell. Physiol 172:209-220.
36. O'Reilly, M.S., L. Holmgren, Y. Shing, C. Chen, R.A. Rosenthal, M. Moses, W.S. Lane, Y. Cao, E.H. Sage, and J. Folkman. 1994. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell. 79:315-328.
37. O'Reilly, M.S., T. Boehm, Y. Shing, N. Fukai, G. Vasios, W.S. Lane, E. Flynn, J.R. Birkhead, B.R. Olsen, and J. Folkman. 1997. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell. 88:277-285.
38. Sage, E.H. 1997. Pieces of eight-bioactive fragments of extracellular proteins as regulators of angiogenesis. Trends Cell Biol. 7:182-186.
39. Hohenester, E., T. Sasaki, B.R. Olsen, and R. Timpl. 1998. Crystal structure of the angiogenesis inhibitor endostatin in 1.5Å resolution. EMBO (Eur. Mol. Biol. Organ.) J. 17:1656-1664.
40. Iozzo, R.V., J. Pillarisetti, B. Sharma, A.D. Murdoch, K.G. Danielson, J. Uitto, and A. Mauviel. 1997. Structural and functional characterization of the human perlecan gene promoter. J. Biol. Chem. 272:5219-5228.
41. Hassell, J.R., W.C. Leyshon, S.R. Ledbetter, B. Tyree, S. Suzuki, M. Kato, K. Kimata, and H.K. Kleinman. 1985. Isolation of two forms of basement membrane proteoglycans. J. Biol. Chem. 260:8098-8105.