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From the Cardiovascular Research Institute and Department of
Anatomy,*
University of California, San Francisco,
California; and the Edwin L. Steele
Laboratory,
Department of Radiation Oncology,
Massachusetts General Hospital and Harvard Medical School,
Boston, Massachusetts
Leakiness of blood vessels in tumors may contribute to disease progression and is key to certain forms of cancer therapy, but the structural basis of the leakiness is unclear. We sought to determine whether endothelial gaps or transcellular holes, similar to those found in leaky vessels in inflammation, could explain the leakiness of tumor vessels. Blood vessels in MCa-IV mouse mammary carcinomas, which are known to be unusually leaky (functional pore size 1.2–2 µm), were compared to vessels in three less leaky tumors and normal mammary glands. Vessels were identified by their binding of intravascularly injected fluorescent cationic liposomes and Lycopersicon esculentum lectin and by CD31 (PECAM) immunoreactivity. The luminal surface of vessels in all four tumors had a defective endothelial monolayer as revealed by scanning electron microscopy. In MCa-IV tumors, 14% of the vessel surface was lined by poorly connected, overlapping cells. The most superficial lining cells, like endothelial cells, had CD31 immunoreactivity and fenestrae with diaphragms, but they had a branched phenotype with cytoplasmic projections as long as 50 µm. Some branched cells were separated by intercellular openings (mean diameter 1.7 µm; range, 0.3–4.7 µm). Transcellular holes (mean diameter 0.6 µm) were also present but were only 8% as numerous as intercellular openings. Some CD31-positive cells protruded into the vessel lumen; others sprouted into perivascular tumor tissue. Tumors in RIP-Tag2 mice had, in addition, tumor cell-lined lakes of extravasated erythrocytes. We conclude that some tumor vessels have a defective cellular lining composed of disorganized, loosely connected, branched, overlapping or sprouting endothelial cells. Openings between these cells contribute to tumor vessel leakiness and may permit access of macromolecular therapeutic agents to tumor cells.
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S. M. Rybak, E. Sanovich, M. G. Hollingshead, S. D. Borgel, D. L. Newton, G. Melillo, D. Kong, G. Kaur, and E. A. Sausville "Vasocrine" Formation of Tumor Cell-lined Vascular Spaces: Implications for Rational Design of Antiangiogenic Therapies Cancer Res., June 1, 2003; 63(11): 2812 - 2819. [Abstract] [Full Text] [PDF]
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R. Giavazzi, B. Sennino, D. Coltrini, A. Garofalo, R. Dossi, R. Ronca, M. P. M. Tosatti, and M. Presta Distinct Role of Fibroblast Growth Factor-2 and Vascular Endothelial Growth Factor on Tumor Growth and Angiogenesis Am. J. Pathol., June 1, 2003; 162(6): 1913 - 1926. [Abstract] [Full Text] [PDF]
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Y. Izumi, E. di Tomaso, A. Hooper, P. Huang, J. Huber, D. J. Hicklin, D. Fukumura, R. K. Jain, and H. D. Suit Responses to Antiangiogenesis Treatment of Spontaneous Autochthonous Tumors and Their Isografts Cancer Res., February 15, 2003; 63(4): 747 - 751. [Abstract] [Full Text] [PDF]
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H. Kubo and K. Alitalo The bloody fate of endothelial stem cells Genes & Dev., February 1, 2003; 17(3): 322 - 329. [Full Text] [PDF]
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M. S. Gee, W. N. Procopio, S. Makonnen, M. D. Feldman, N. M. Yeilding, and W. M. F. Lee Tumor Vessel Development and Maturation Impose Limits on the Effectiveness of Anti-Vascular Therapy Am. J. Pathol., January 1, 2003; 162(1): 183 - 193. [Abstract] [Full Text] [PDF]
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Y.-J. Lee, N. Nagai, C.-H. Siar, K. Nakano, H. Nagatsuka, H. Tsujigiwa, C.-H. Roan, and M. Gunduz Angioarchitecture of Primary Oral Malignant Melanomas J. Histochem. Cytochem., November 1, 2002; 50(11): 1555 - 1562. [Abstract] [Full Text] [PDF]
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J. A. Tuxhorn, S. J. McAlhany, F. Yang, T. D. Dang, and D. R. Rowley Inhibition of Transforming Growth Factor-{beta} Activity Decreases Angiogenesis in a Human Prostate Cancer-reactive Stroma Xenograft Model Cancer Res., November 1, 2002; 62(21): 6021 - 6025. [Abstract] [Full Text] [PDF]
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D. M. McDonald and P. Baluk Significance of Blood Vessel Leakiness in Cancer Cancer Res., September 15, 2002; 62(18): 5381 - 5385. [Abstract] [Full Text] [PDF]
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 L. Jussila and K. Alitalo Vascular Growth Factors and Lymphangiogenesis Physiol Rev, July 1, 2002; 82(3): 673 - 700. [Abstract] [Full Text] [PDF]
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J. A. Tuxhorn, S. J. McAlhany, T. D. Dang, G. E. Ayala, and D. R. Rowley Stromal Cells Promote Angiogenesis and Growth of Human Prostate Tumors in a Differential Reactive Stroma (DRS) Xenograft Model Cancer Res., June 1, 2002; 62(11): 3298 - 3307. [Abstract] [Full Text] [PDF]
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 R. Clarijs, I. Otte-Holler, D. J. Ruiter, and R. M. W. de Waal Presence of a Fluid-Conducting Meshwork in Xenografted Cutaneous and Primary Human Uveal Melanoma Invest. Ophthalmol. Vis. Sci., April 1, 2002; 43(4): 912 - 918. [Abstract] [Full Text] [PDF]
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J. L. Yu, J. W. Rak, G. Klement, and R. S. Kerbel Vascular Endothelial Growth Factor Isoform Expression as a Determinant of Blood Vessel Patterning in Human Melanoma Xenografts Cancer Res., March 1, 2002; 62(6): 1838 - 1846. [Abstract] [Full Text] [PDF]
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S. Morikawa, P. Baluk, T. Kaidoh, A. Haskell, R. K. Jain, and D. M. McDonald Abnormalities in Pericytes on Blood Vessels and Endothelial Sprouts in Tumors Am. J. Pathol., March 1, 2002; 160(3): 985 - 1000. [Abstract] [Full Text] [PDF]
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 A. K. Sood, M. S. Fletcher, and M. J. C. Hendrix The Embryonic-Like Properties of Aggressive Human Tumor Cells Reproductive Sciences, January 1, 2002; 9(1): 2 - 9. [Abstract] [PDF]
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 M. ANGHELINA, A. SCHMEISSER, P. KRISHNAN, L. MOLDOVAN, R.H. STRASSER, and N.I. MOLDOVAN Migration of Monocytes/Macrophages In Vitro and In Vivo Is Accompanied by MMP12-dependent Tunnel Formation and by Neovascularization Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 209 - 216. [Abstract] [PDF]
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R. PASQUALINI and W. ARAP Profiling the Molecular Diversity of Blood Vessels Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 223 - 226. [Abstract] [PDF]
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K. Shirakawa, H. Kobayashi, Y. Heike, S. Kawamoto, M. W. Brechbiel, F. Kasumi, T. Iwanaga, F. Konishi, M. Terada, and H. Wakasugi Hemodynamics in Vasculogenic Mimicry and Angiogenesis of Inflammatory Breast Cancer Xenograft Cancer Res., January 1, 2002; 62(2): 560 - 566. [Abstract] [Full Text] [PDF]
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 A. Abramsson, O. Berlin, H. Papayan, D. Paulin, M. Shani, and C. Betsholtz Analysis of Mural Cell Recruitment to Tumor Vessels Circulation, January 1, 2002; 105(1): 112 - 117. [Abstract] [Full Text] [PDF]
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 D. M. MCDONALD Angiogenesis and Remodeling of Airway Vasculature in Chronic Inflammation Am. J. Respir. Crit. Care Med., November 15, 2001; 164(10): S39 - 45. [Abstract] [Full Text] [PDF]
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D. A. Elson, G. Thurston, L. E. Huang, D. G. Ginzinger, D. M. McDonald, R. S. Johnson, and J. M. Arbeit Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1{alpha} Genes & Dev., October 1, 2001; 15(19): 2520 - 2532. [Abstract] [Full Text] [PDF]
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Z. Hu and A. Garen Targeting tissue factor on tumor vascular endothelial cells and tumor cells for immunotherapy in mouse models of prostatic cancer PNAS, September 26, 2001; (2001) 201420298. [Abstract] [Full Text] [PDF]
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T. Karpanen and K. Alitalo Lymphatic Vessels as Targets of Tumor Therapy? J. Exp. Med., September 17, 2001; 194(6): F37 - F42. [Full Text] [PDF]
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T. Ezaki, P. Baluk, G. Thurston, A. La Barbara, C. Woo, and D. M. McDonald Time Course of Endothelial Cell Proliferation and Microvascular Remodeling in Chronic Inflammation Am. J. Pathol., June 1, 2001; 158(6): 2043 - 2055. [Abstract] [Full Text] [PDF]
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A. K. Sood, E. A. Seftor, M. S. Fletcher, L. M. G. Gardner, P. M. Heidger, R. E. Buller, R. E. B. Seftor, and M. J. C. Hendrix Molecular Determinants of Ovarian Cancer Plasticity Am. J. Pathol., April 1, 2001; 158(4): 1279 - 1288. [Abstract] [Full Text] [PDF]
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