Endostatin: an endogenous inhibitor of angiogenesis and tumor growth
Open accessAbstract
We previously identified the angiogenesis inhibitor angiostatin. Using a similar strategy, we have identified endostatin, an angiogenesis inhibitor produced by hemangioendothelioma. Endostatin is a 20 kDa C-terminal fragment of collagen XVIII. Endostatin specifically inhibits endothelial proliferation and potently inhibits angiogenesis and tumor growth. By a novel method of sustained release, E. coli-derived endostatin was administered as a nonrefolded suspension. Primary tumors were regressed to dormant microscopic lesions. Immunohistochemistry revealed blocked angiogenesis accompanied by high proliferation balanced by apoptosis in tumor cells. There was no toxicity. Together with angiostatin data, these findings validate a strategy for identifying endogenous angiogenesis inhibitors, suggest a theme of fragments of proteins as angiogenesis inhibitors, and demonstrate dormancy therapy.
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The C-terminal non-collagenous (NC1) domain of collagen has been reported as an inhibitor of angiogenesis.
“The C-terminal non-collagenous (NC1) domain of the collagen has been reported as an inhibitor of angiogenesis (29–31).”
From Common variants near FRK/COL10A1 and VEGFA are associated with advanced age-related macular degeneration (2011) · cites this paper as [29]
Cites
Tumor angiogenesis: therapeutic implications
Sherwood, L. M., Parris, E. E., & Folkman, J. (1971) · New England Journal of Medicine · doi:10.1056/nejm197111182852108 · Cited by 10,187 · see citing works
Self-citationIdentification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444 · see citing works
Angiogenesis in cancer, vascular, rheumatoid and other disease
Folkman, J. (1995) · Nature Medicine · doi:10.1038/nm0195-27 · Cited by 7,627 · see citing works
Self-citation[6] Use of T7 RNA polymerase to direct expression of cloned genes
Studier, F. W., Rosenberg, A. H., Dunn, J. J., & Dubendorff, J. W. (1990) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(90)85008-c · Cited by 6,562 · see citing works
What Is the Evidence That Tumors Are Angiogenesis Dependent?
Folkman, J. (1990) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/82.1.4 · Cited by 4,509 · see citing works
Self-citationKim, K. J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H. S., & Ferrara, N. (1993) · Nature · doi:10.1038/362841a0 · Cited by 3,605 · see citing works
OʼReilly, M. (1994) · Cell · doi:10.1016/0092-8674(94)90200-3 · Cited by 3,344 · see citing works
Self-citationTransplacental Carcinogenesis by Stilbestrol
Folkman, J. (1971) · New England Journal of Medicine · doi:10.1056/nejm197108122850711 · Cited by 2,640 · see citing works
Self-citationClinical Applications of Research on Angiogenesis
Folkman, J. (1995) · New England Journal of Medicine · doi:10.1056/nejm199512283332608 · Cited by 2,242 · see citing works
Self-citationPlasminogen: Purification from Human Plasma by Affinity Chromatography
Deutsch, D. G., & Mertz, E. T. (1970) · Science · doi:10.1126/science.170.3962.1095 · Cited by 2,145 · see citing works
Holmgren, L., O’Reilly, M. S., & Folkman, J. (1995) · Nature Medicine · doi:10.1038/nm0295-149 · Cited by 1,870 · see citing works
Self-citationControl of Angiogenesis in Fibroblasts by p53 Regulation of Thrombospondin-1
Dameron, K. M., Volpert, O. V., Tainsky, M. A., & Bouck, N. (1994) · Science · doi:10.1126/science.7521539 · Cited by 1,437 · see citing works
Cell death and control of cell survival in the oligodendrocyte lineage
Barres, B. A., Hart, I. K., Coles, H. S. R., Burne, J. F., Voyvodic, J. T., Richardson, W. D., & Raff, M. C. (1992) · Cell · doi:10.1016/0092-8674(92)90531-g · Cited by 1,345 · see citing works
Model Predicting Survival in Stage I Melanoma Based on Tumor Progression
Clark, W. H., Elder, D. E., Guerry, D., Braitman, L. E., Trock, B. J., Schultz, D., Synnestvedt, M. B., & Halpern, A. C. (1989) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/81.24.1893 · Cited by 1,247 · see citing works
Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant
Millauer, B., Shawver, L. K., Plate, K. H., Risaui, W., & Ullrich, A. (1994) · Nature · doi:10.1038/367576a0 · Cited by 1,219 · see citing works
Angiostatin induces and sustains dormancy of human primary tumors in mice
O’Reilly, M. S., Holmgren, L., Chen, C., & Folkman, J. (1996) · Nature Medicine · doi:10.1038/nm0696-689 · Cited by 1,170 · see citing works
Self-citationThe implications of angiogenesis for the biology and therapy of cancer metastasis
Fidler, I. J. (1994) · Cell · doi:10.1016/0092-8674(94)90187-2 · Cited by 1,099 · see citing works
Good, D. J., Polverini, P. J., Rastinejad, F., Beau, M. M. L., Lemons, R. S., Frazier, W. A., & Bouck, N. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.17.6624 · Cited by 1,051 · see citing works
Important Advances in Oncology: 1986
Merrill, J. M. (1986) · JAMA · doi:10.1001/jama.1986.03380040106043 · Cited by 909 · see citing works
Long-term culture of capillary endothelial cells.
Folkman, J., Haudenschild, C. C., & Zetter, B. R. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.10.5217 · Cited by 766 · see citing works
Self-citationGrant, D. S., Tashiro, K., Seguí‐Real, B., Yamada, Y., Martin, G. R., & Kleinman, H. K. (1989) · Cell · doi:10.1016/0092-8674(89)90945-8 · Cited by 740 · see citing works
Inhibition of Angiogenesis In Vivo by Interleukin 12
Voest, E. E., Kenyon, B. M., OʼReilly, M., Truitt, G. A., D’Amato, R. J., & Folkman, J. (1995) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/87.8.581 · Cited by 722 · see citing works
Self-citationHuman interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo.
Angiolillo, A. L., Sgadari, C., Taub, D. D., Liao, F., Farber, J. M., Maheshwari, S., Kleinman, H. K., Reaman, G. H., & Tosato, G. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.182.1.155 · Cited by 704 · see citing works
Inhibition of Angiogenesis by Recombinant Human Platelet Factor-4 and Related Peptides
Maione, T. E., Gray, G. S., Petro, J., Hunt, A. J., Donner, A. L., Bauer, S., Carson, H. F., & Sharpe, R. J. (1990) · Science · doi:10.1126/science.1688470 · Cited by 698 · see citing works
Brown, L. F., Berse, B., Jackman, R. W., Tognazzi, K., Manseau, E. J., Senger, D. R., & Dvorak, H. F. (1993) · PubMed · Cited by 635 · see citing works
Tolsma, S. S., Volpert, O. V., Good, D., Frazier, W., Polverini, P., & Bouck, N. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.2.497 · Cited by 572 · see citing works
Kandel, J. J., Bossy‐Wetzel, E., Radvanyi, F., Klagsbrun, M., Folkman, J., & Hanahan, D. (1991) · Cell · doi:10.1016/0092-8674(91)90033-u · Cited by 507 · see citing works
Self-citationRegulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene
Rastinejad, F., Polverini, P. J., & Bouck, N. (1989) · Cell · doi:10.1016/0092-8674(89)90238-9 · Cited by 460 · see citing works
Bursch, W., Paffe, S., Putz, B., Barthel, G., & Schulte‐Hermann, R. (1990) · Carcinogenesis · doi:10.1093/carcin/11.5.847 · Cited by 444 · see citing works
Fisher, B., Gündüz, N., & Saffer, E. (1983) · PubMed · Cited by 421 · see citing works
Effect of surgical removal on the growth and kinetics of residual tumor.
Gündüz, N., Fisher, B., & Saffer, E. (1979) · PubMed · Cited by 412 · see citing works
A model of angiogenesis in the mouse cornea.
Kenyon, B. M., Voest, E. E., Chen, C. C., Flynn, E. A., Folkman, J., & D’Amato, R. J. (1996) · PubMed · Cited by 403 · see citing works
Self-citationKringle Domains of Human Angiostatin
Cao, Y., Ji, R. W., Davidson, D. J., Schaller, J., Marti, D. N., Söhndel, S., McCance, S. G., O’Reilly, M. S., Llinás, M., & Folkman, J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.46.29461 · Cited by 368 · see citing works
Self-citationPresence of a growth-stimulating factor in serum following primary tumor removal in mice.
Fisher, B., Gündüz, N., Coyle, J., Rudock, C., & Saffer, E. (1989) · PubMed · Cited by 361 · see citing works
Multifactorial analysis of p53 alteration in human cancer: A review
Soussi, T., Legros, Y., Lubin, R., Ory, K., & Schlichtholz, B. (1994) · International Journal of Cancer · doi:10.1002/ijc.2910570102 · Cited by 351 · see citing works
Antiangiogenic therapy of transgenic mice impairs de novo tumor growth.
Parangi, S., OʼReilly, M., Christofori, G., Holmgren, L., Grosfeld, J. A., Folkman, J., & Hanahan, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.5.2002 · Cited by 343 · see citing works
Self-citationThe 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis
Clapp, C., MARTIAL, J. A., Guzman, R. C., Rentier-Delure, F., & Weiner, R. I. (1993) · Endocrinology · doi:10.1210/endo.133.3.7689950 · Cited by 338 · see citing works
Tumor angiogenesis and tissue factor
Folkman, J. (1996) · Nature Medicine · doi:10.1038/nm0296-167 · Cited by 295 · see citing works
Self-citationStrieter, R. M., Kunkel, S. L., Arenberg, D. A., et al. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.1626 · Cited by 289 · see citing works
Hori, A., Sasada, R., Matsutani, E., et al. (1991) · PubMed · Cited by 263 · see citing works
Increased capillary endothelial cell protease activity in response to angiogenic stimuli in vitro.
Gross, J. L., Moscatelli, D., & Rifkin, D. B. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.9.2623 · Cited by 261 · see citing works
Quantitation of Angiogenesis and Antiangiogenesis in the Chick Embryo Chorioallantoic Membrane
Nguyen, M. T. N., Shing, Y., & Folkman, J. (1994) · Microvascular Research · doi:10.1006/mvre.1994.1003 · Cited by 245 · see citing works
Self-citationPotentiation of cytotoxic cancer therapies by TNP‐470 alone and with other anti‐angiogenic agents
Teicher, B. A., Holden, S. A., Ara, G., Sotomayor, E. A., Huang, Z. D., Chen, Y., & Brem, H. (1994) · International Journal of Cancer · doi:10.1002/ijc.2910570624 · Cited by 231 · see citing works
LERCH, P. G., Rickli, E. E., Lergier, W., et al. (1980) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1980.tb04617.x · Cited by 223 · see citing works
Ponting, C. P., Marshall, J. M., & Cederholm-Williams, S. A. (1992) · Blood Coagulation & Fibrinolysis · doi:10.1097/00001721-199210000-00012 · Cited by 216 · see citing works
Angiostatin: A Circulating Endothelial Cell Inhibitor That Suppresses Angiogenesis and Tumor GrowthPreprint
OʼReilly, M., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Cao, Y., Moses, M. A., Lane, W. S., Sage, E. H., & Folkman, J. (1994) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1994.059.01.052 · Cited by 216 · see citing works
Self-citationGately, S. T., Twardowski, P., Stack, M. S., Patrick, M., Boggio, L. N., Cundiff, D. L., Schnaper, H. W., Madison, L. D., Volpert, O. V., Bouck, N., et al. (1996) · PubMed · Cited by 197 · see citing works
Muragaki, Y., Timmons, S., Griffith, M., Oh, S. P., Fadel, B. M., Quertermous, T., & Olsen, B. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.19.8763 · Cited by 194 · see citing works
Self-citationOh, S. P., KAMAGATA, Y., Muragaki, Y., et al. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.10.4229 · Cited by 189 · see citing works
Rehn, M., & Pihlajaniemi, T. A. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.10.4234 · Cited by 180 · see citing works
Inhibition of angiogenesis and tumor growth by a synthetic laminin peptide, CDPGYIGSR-NH2.
Sakamoto, N., Iwahana, M., Tanaka, N., et al. (1991) · PubMed · Cited by 159 · see citing works
Lane, W. S., Gałat, A., Harding, M. W., & Schreiber, S. L. (1991) · Journal of Protein Chemistry · doi:10.1007/bf01024778 · Cited by 159 · see citing works
Self-citationMilas, L., Hunter, N. R., Mason, K. A., et al. (1974) · PubMed · Cited by 149 · see citing works
Gupta, S. K., Hassel, T., & Singh, J. P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7799 · Cited by 141 · see citing works
The inhibition of tumor growth by tumor mass.
Prehn, R. T. (1991) · PubMed · Cited by 136 · see citing works
Cao, Y., Chen, C., Weatherbee, J. A., Tsang, M., & Folkman, J. (1995) · The Journal of Experimental Medicine · doi:10.1084/jem.182.6.2069 · Cited by 135 · see citing works
Self-citationConcomitant Tumor Immunity and the Resistance to a Second Tumor Challenge
Gorelik, E. (1983) · Advances in cancer research · doi:10.1016/s0065-230x(08)61033-7 · Cited by 134 · see citing works
Obeso, J. L., Weber, J. B., & Auerbach, R. (1990) · PubMed · Cited by 132 · see citing works
Rehn, M., & Pihlajaniemi, T. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.9.4705 · Cited by 128 · see citing works
Factors in the Production and Growth of tumor Metastases.
Tyzzer, E. E. (1913) · PubMed · Cited by 124 · see citing works
On Concomitant Immunity in Tumour-bearing Hamsters
Gershon, R. K., Carter, R. L., & KONDO, K. (1967) · Nature · doi:10.1038/213674a0 · Cited by 119 · see citing works
Heparin-binding fragments of fibronectin are potent inhibitors of endothelial cell growth.
Homandberg, G. A., Williams, J. E., Grant, D., et al. (1985) · PubMed · Cited by 116 · see citing works
Schatten, W. E. (1958) · Cancer · doi:10.1002/1097-0142(195805/06)11:3 · Cited by 111 · see citing works
Hamada, J., Cavanaugh, P. G., Lotan, O., & Nicolson, G. (1992) · British Journal of Cancer · doi:10.1038/bjc.1992.269 · Cited by 107 · see citing works
A strategy to discover circulating angiogenesis inhibitors generated by human tumors.
Chen, C., Parangi, S., Tolentino, M. J., & Folkman, J. (1995) · PubMed · Cited by 99 · see citing works
Self-citationGROWTH OF A LOCAL TUMOR EXERTS A SPECIFIC INHIBITORY EFFECT ON PROGRESSION OF LUNG METASTASES
Gorelik, E., Segal, S., & Feldman, M. M. (1978) · International Journal of Cancer · doi:10.1002/ijc.2910210512 · Cited by 94 · see citing works
Two competing influences that may explain concomitant tumor resistance.
Prehn, R. T. (1993) · PubMed · Cited by 89 · see citing works
Bok, R., & Mangel, W. F. (1985) · Biochemistry · doi:10.1021/bi00334a031 · Cited by 83 · see citing works
Angiogenesis and its inhibitors.
Folkman, J. (1985) · PubMed · Cited by 80 · see citing works
Self-citationAn elastase-dependent pathway of plasminogen activation
Machovich, R., & Owen, W. G. (1989) · Biochemistry · doi:10.1021/bi00436a059 · Cited by 72 · see citing works
Interactions between newly formed endothelial channels and carcinoma cells in plasma clot culture
Nicosia, R. F., Tchao, R., & Leighton, J. (1986) · Clinical & Experimental Metastasis · doi:10.1007/bf00119076 · Cited by 71 · see citing works
“Concomitant immunity” in murine tumours of non-detectable immunogenicity
Ruggiero, R. A., Bustuoabad, O. D., Bonfil, R. D., Meiss, R. P., & Pasqualini, C. D. (1985) · British Journal of Cancer · doi:10.1038/bjc.1985.6 · Cited by 69 · see citing works
Rehen, M. (1994) · Medical Entomology and Zoology · Cited by 66 · see citing works
Sage, E. H., Bassuk, J. A., Yost, J. C., Folkman, M. J., & Lane, T. F. (1995) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240570113 · Cited by 65 · see citing works
5, E. G., Segal, S., & Feldman, M. (1980) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/65.6.1257 · Cited by 62 · see citing works
The inhibitory influence of a transplanted hamster lymphoma on metastasis.
Greene, H. S. N., & Harvey, E. K. (1960) · PubMed · Cited by 55 · see citing works
On the mechanism of tumor ‘concomitant immunity’
Gorelik, E., Segal, S., & Feldman, M. M. (1981) · International Journal of Cancer · doi:10.1002/ijc.2910270618 · Cited by 50 · see citing works
The natural and induced resistance of mice to the growth of cancer
Bashford, E. F., Murray, J. A., & Cramer, W. (1907) · Proceedings of the Royal Society of London Series B Containing Papers of a Biological Character · doi:10.1098/rspb.1907.0014 · Cited by 50 · see citing works
Important Advances in Oncology 1986
Hellmän, S., DeVita, V. T., & Rosenberg, S. A. (1986) · Cited by 49 · see citing works
Inhibition of subcutaneously growing line 1 carcinomas due to metastatic spread.
Yuhas, J. M., & Pazmiño, N. H. (1974) · PubMed · Cited by 49 · see citing works
Resistance of tumor-bearing mice to a second tumor challenge.
Gorelik, E. (1983) · PubMed · Cited by 36 · see citing works
NELSON, J., Allen, W. E., Scott, W. N., et al. (1995) · PubMed · Cited by 35 · see citing works
Role of concomitant resistance in the development of murine lung metastases
Bonfil, R. D., Ruggiero, R. A., Bustuoabad, O. D., et al. (1988) · International Journal of Cancer · doi:10.1002/ijc.2910410317 · Cited by 30 · see citing works
Band, P. R., Feldstein, M., Saccomanno, G., Watson, L., & King, G. (1980) · Cancer · doi:10.1002/1097-0142(19800315)45:6 · Cited by 25 · see citing works
Neutrophil proteases in plasminogen activation
Machovich, R., Himer, Á., & Owen, W. G. (1990) · Blood Coagulation & Fibrinolysis · doi:10.1097/00001721-199008000-00004 · Cited by 22 · see citing works
Concomitant immunity in hamsters bearing dmba‐induced tumor transplants
Lausch, R. N., & Rapp, F. (1969) · International Journal of Cancer · doi:10.1002/ijc.2910040213 · Cited by 21 · see citing works
Himmele, J. C., Rabenhorst, B., & Werner, D. (1986) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/bf00400757 · Cited by 13 · see citing works
Flagged first, then by citations
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Sorted by citations
Angiogenesis in cancer and other diseases
Carmeliet, P., & Jain, R. K. (2000) · Nature · doi:10.1038/35025220 · Cited by 9,070 · see citing works
New functions for the matrix metalloproteinases in cancer progression
Egeblad, M., & Werb, Z. (2002) · Nature Reviews Cancer · doi:10.1038/nrc745 · Cited by 6,108 · see citing works
Vascular-specific growth factors and blood vessel formation
Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J., & Holash, J. (2000) · Nature · doi:10.1038/35025215 · Cited by 3,699 · see citing works
Tumorigenesis and the angiogenic switch
Bergers, G., & Benjamin, L. E. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1093 · Cited by 3,559 · see citing works
Functional Polarization of Tumour-Associated Macrophages by Tumour-Derived Lactic Acid
Colegio, O. R., Chu, N.-Q., Szabo, A. L., Chu, T., Rhebergen, A. M., Jairam, V., Cyrus, N., Brokowski, C. E., Eisenbarth, S. C., Phillips, G. M., et al. (2014) · Nature · doi:10.1038/nature13490 · Cited by 3,046 · see citing works
Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.-H., Ito, S., Yang, C., Wang, P., Xiao, M.-T., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2010.12.014 · Cited by 2,875 · see citing works
Angiogenesis as a therapeutic target
Ferrara, N., & Kerbel, R. S. (2005) · Nature · doi:10.1038/nature04483 · Cited by 2,653 · see citing works
Concepts of extracellular matrix remodelling in tumour progression and metastasis
Winkler, J., Abisoye-Ogunniyan, A., Metcalf, K. J., & Werb, Z. (2020) · Nature Communications · doi:10.1038/s41467-020-18794-x · Cited by 2,296 · see citing works
Openings Between Defective Endothelial Cells Explain Tumor Vessel Leakiness
Hashizume, H., Baluk, P., Morikawa, S., McLean, J. W., Thurston, G., Roberge, S., Jain, R. K., & McDonald, D. M. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)65006-7 · Cited by 1,689 · see citing works
Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance
Boehm, T., Folkman, J., Browder, T., & O'Reilly, M. S. (1997) · Nature · doi:10.1038/37126 · Cited by 1,683 · see citing works
Self-citationFolkman, J. (2006) · Annual Review of Medicine · doi:10.1146/annurev.med.57.121304.131306 · Cited by 1,209 · see citing works
Self-citationFibroblasts in fibrosis: novel roles and mediators
Kendall, R. T., & Feghali-Bostwick, C. A. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00123 · Cited by 1,082 · see citing works
Regulation of matrix biology by matrix metalloproteinases
Mott, J. D., & Werb, Z. (2004) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2004.07.010 · Cited by 1,104 · see citing works
Molecular mechanisms of blood vessel growth
Conway, E. (2001) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00281-9 · Cited by 1,030 · see citing works
Materials as stem cell regulators
Murphy, W. L., McDevitt, T. C., & Engler, A. J. (2014) · Nature Materials · doi:10.1038/nmat3937 · Cited by 947 · see citing works
Adipose tissue mass can be regulated through the vasculature
Rupnick, M. A., Panigrahy, D., Zhang, C.-Y., Dallabrida, S. M., Lowell, B. B., Langer, R., & Folkman, M. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162349799 · Cited by 845 · see citing works
Mechanisms of normal and tumor-derived angiogenesis
Papetti, M., & Herman, I. M. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00389.2001 · Cited by 809 · see citing works
Angiogenesis: regulators and clinical applications
Liekens, S., De Clercq, E., & Neyts, J. (2001) · Biochemical Pharmacology · doi:10.1016/s0006-2952(00)00529-3 · Cited by 748 · see citing works
Angiogenesis modulates adipogenesis and obesity
Cao, Y. (2007) · Journal of Clinical Investigation · doi:10.1172/jci32239 · Cited by 736 · see citing works
Moulton, K. S., Heller, E., Konerding, M. A., Flynn, E., Palinski, W., & Folkman, J. (1999) · Circulation · doi:10.1161/01.cir.99.13.1726 · Cited by 688 · see citing works
Self-citationBasement membrane proteoglycans: from cellar to ceiling
Iozzo, R. V. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1702 · Cited by 521 · see citing works
The good and the bad collagens of fibrosis – Their role in signaling and organ function
Karsdal, M. A., Nielsen, S. H., Leeming, D. J., Langholm, L. L., Nielsen, M. J., Manon-Jensen, T., Siebuhr, A., Gudmann, N. S., Rønnow, S., Sand, J. M., et al. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.07.014 · Cited by 509 · see citing works
Exploiting the critical perioperative period to improve long-term cancer outcomes
Horowitz, M., Neeman, E., Sharon, E., & Ben-Eliyahu, S. (2015) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2014.224 · Cited by 487 · see citing works
A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype
Naumov, G. N., Bender, E., Zurakowski, D., Kang, S.-Y., Sampson, D., Flynn, E., Watnick, R. S., Straume, O., Akslen, L. A., Folkman, J., et al. (2006) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djj068 · Cited by 423 · see citing works
Self-citationAnti-angiogenic therapy: current challenges and future perspectives
Lopes-Coelho, F., Martins, F., Pereira, S. A., & Serpa, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073765 · Cited by 416 · see citing works
RETRACTED: Engineered whole organs and complex tissues
Badylak, S. F., Weiss, D. J., Caplan, A., & Macchiarini, P. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60073-7 · Cited by 417 · see citing works
RetractedStress and cancer: mechanisms, significance and future directions
Eckerling, A., Ricon-Becker, I., Sorski, L., Sandbank, E., & Ben-Eliyahu, S. (2021) · Nature Reviews Cancer · doi:10.1038/s41568-021-00395-5 · Cited by 348 · see citing works
Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials.
Liu, J., Wang, Y., Akamatsu, Y., Lee, C. C., Stetler, R. A., Lawton, M. T., & Yang, G.-Y. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.11.004 · Cited by 335 · see citing works
Priming, Replication, and the Hardest Science
Cesario, J. (2014) · Perspectives on Psychological Science · doi:10.1177/1745691613513470 · Cited by 320 · see citing works
Adhesion events in angiogenesis
Eliceiri, B. P., & Cheresh, D. A. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00252-0 · Cited by 287 · see citing works
A comprehensive review of retinal gene therapy
Boye, S. E., Boye, S. L., Lewin, A. S., & Hauswirth, W. W. (2013) · Molecular Therapy · doi:10.1038/mt.2012.280 · Cited by 262 · see citing works
Arenberg, D. A., Keane, M. P., DiGiovine, B., Kunkel, S. L., Morris, S. B., Xue, Y. Y., Burdick, M. D., Glass, M. C., Iannettoni, M. D., & Strieter, R. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci3145 · Cited by 259 · see citing works
Yu, Y., Bhangale, T. R., Fagerness, J., Ripke, S., Thorleifsson, G., Tan, P. L., Souied, E. H., Richardson, A. J., Merriam, J. E., Buitendijk, G. H. S., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr270 · Cited by 254 · see citing works
Proinflammatory functions of vascular endothelial growth factor in alloimmunity
Reinders, M. E. J., Sho, M., Izawa, A., Wang, P., Mukhopadhyay, D., Koss, K. E., Geehan, C. S., Luster, A. D., Sayegh, M. H., & Briscoe, D. M. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17712 · Cited by 251 · see citing works
Matricryptins and matrikines: biologically active fragments of the extracellular matrix
Ricard‐Blum, S., & Salza, R. (2014) · Experimental Dermatology · doi:10.1111/exd.12435 · Cited by 224 · see citing works
Khanna, C., Prehn, J., Yeung, C., Caylor, J., Tsokos, M., & Helman, L. (2000) · Clinical & Experimental Metastasis · doi:10.1023/a:1006767007547 · Cited by 207 · see citing works
Extracellular matrix scaffolding in angiogenesis and capillary homeostasis
Marchand, M., Monnot, C., Muller, L., & Germain, S. (2019) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2018.08.007 · Cited by 205 · see citing works
Endogenous inhibitors of angiogenesis
Ribatti, D. (2009) · Leukemia Research · doi:10.1016/j.leukres.2008.11.019 · Cited by 191 · see citing works
Lentiviral Vector Gene Transfer of Endostatin/Angiostatin for Macular Degeneration (GEM) Study
Campochiaro, P. A., Lauer, A. K., Sohn, E. H., Mir, T. A., Naylor, S., Anderton, M. C., Kelleher, M., Harrop, R., Ellis, S., & Mitrophanous, K. A. (2017) · Human Gene Therapy · doi:10.1089/hum.2016.117 · Cited by 186 · see citing works
Agrawal, V., Tottey, S., Johnson, S. A., Freund, J. M., Siu, B. F., & Badylak, S. F. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0036 · Cited by 180 · see citing works
Bacteria as vectors for gene therapy of cancer
Baban, C. K., Cronin, M., O’Hanlon, D., O’Sullivan, G. C., & Tangney, M. (2010) · Bioengineered Bugs · doi:10.4161/bbug.1.6.13146 · Cited by 175 · see citing works
Angiongenesis: a new theory for endometriosis
Healy, D. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.736 · Cited by 173 · see citing works
Targeting Vascular Pericytes in Hypoxic Tumors Increases Lung Metastasis via Angiopoietin-2
Keskin, D., Kim, J., Cooke, V. G., Wu, C.-C., Sugimoto, H., Gu, C., De Palma, M., Kalluri, R., & LeBleu, V. S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.035 · Cited by 165 · see citing works
Sudhakar, A. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24813 · Cited by 162 · see citing works
RetractedThe Extracellular Matrix in Wound Healing: A Closer Look at Therapeutics for Chronic Wounds
Agren, M. S., & Werthen, M. (2007) · The International Journal of Lower Extremity Wounds · doi:10.1177/1534734607301394 · Cited by 136 · see citing works
Endostatin gene therapy delivered by <i>Salmonella choleraesuis</i> in murine tumor models
Lee, C., Wu, C., & Shiau, A. (2004) · The Journal of Gene Medicine · doi:10.1002/jgm.626 · Cited by 93 · see citing works
Microvascular complications and diabetic retinopathy: recent advances and future implications
Barot, M., Gokulgandhi, M. R., Patel, S., & Mitra, A. K. (2013) · Future Medicinal Chemistry · doi:10.4155/fmc.12.206 · Cited by 92 · see citing works
Addressing tumor blood vessels
Folkman, J. (1997) · Nature Biotechnology · doi:10.1038/nbt0697-510 · Cited by 89 · see citing works
Self-citationGene Therapy Intervention in Neovascular Eye Disease: A Recent Update
Lin, F.-L., Wang, P.-Y., Chuang, Y.-F., Wang, J.-H., Wong, V. H. Y., Bui, B. V., & Liu, G.-S. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.06.029 · Cited by 74 · see citing works
Matrikines for therapeutic and biomedical applications
Sivaraman, K., & Shanthi, C. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.10.056 · Cited by 50 · see citing works
Involvement of RB gene family in tumor angiogenesis
Gabellini, C., Del Bufalo, D., & Zupi, G. (2006) · Oncogene · doi:10.1038/sj.onc.1209631 · Cited by 47 · see citing works
Toward improved <i>in vitro</i> models of human cancer
Ayuso, J. M., Park, K.-Y., Virumbrales-Muñoz, M., & Beebe, D. J. (2021) · APL Bioengineering · doi:10.1063/5.0026857 · Cited by 40 · see citing works
Bruch’s Membrane and the Choroid in Age-Related Macular Degeneration
Edwards, M., & Lutty, G. A. (2021) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-66014-7_4 · Cited by 32 · see citing works
A personal voyage through the proteoglycan field
Lindahl, U. (2014) · Matrix Biology · doi:10.1016/j.matbio.2014.01.001 · Cited by 28 · see citing works
Caire, R., Roche, B., Picot, T., Aanei, C.-M., He, Z., Campos, L., Thomas, M., Malaval, L., Vico, L., & Lafage-Proust, M.-H. (2019) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3728 · Cited by 27 · see citing works
The history of angiogenesis inhibitors
Ribatti, D. (2007) · Leukemia · doi:10.1038/sj.leu.2404756 · Cited by 15 · see citing works
Blood Vessel-Targeted Therapy in Colorectal Cancer: Current Strategies and Future Perspectives
Jacobsen, A., Siebler, J., Grützmann, R., Stürzl, M., & Naschberger, E. (2024) · Cancers · doi:10.3390/cancers16050890 · Cited by 11 · see citing works
- Authors
- O'Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., Flynn, E., Birkhead, J. R., Olsen, B. R., & Folkman, J.
- Affiliations
- Boston Children's Hospital (US)
- Harvard University (US)
- Corresponding author
- Folkman, Judah
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 1997-01
- Volume
- 88
- Issue
- 2
- Pages
- 277-285
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2131798870
- Cited by
- 4,486
- References
- 87
- Citations by year
- 2026: 28 · 2025: 28 · 2024: 54 · 2023: 63 · 2022: 68 · 2021: 89 · 2020: 87 · 2019: 79 · 2018: 95 · 2017: 99 · 2016: 100 · 2015: 110 · 2014: 152 · 2013: 131 · 2012: 152
- FWCI
- 74.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01hl040711-03, 5p01hl033014-10)
- National Heart, Lung, and Blood Institute (HL 33014, HL-40711)
- National Cancer Institute (P01CA045548, P0-1 CA-45548)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Vascular Tumors and Angiosarcomas
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- endostatin, angiogenesis inhibitors, angiostatin, collagen XVIII, hemangioendothelioma, tumor growth inhibition, endothelial cell proliferation, tumor dormancy, apoptosis, protein fragments, sustained drug release, tumor regression
- MeSH terms
- Amino Acid Sequence, Animals, Antineoplastic Agents, Capillaries, Cell Division, Collagen, Endothelium, Vascular, Hemangioendothelioma, Male, Mice, Inbred C57BL, Mice, Inbred Strains, Molecular Sequence Data, Neoplasm Metastasis, Neoplasms, Experimental, Neovascularization, Pathologic, Peptide Fragments, Recombinant Proteins, Tumor Cells, Cultured, Culture Media, Conditioned, Neovascularization, Physiologic, Endostatins, Collagen Type XVIII, Mice
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