Microvessel organization and structure in experimental brain tumors: Microvessel populations with distinctive structural and functional properties

Microvascular Research

Volumn 58, Issue 3, 1999, Pages 312-328

  Schlageter, Kurt E ^a,b   Molnar, Peter ^a,c   Lapin, Gregory D ^a   Groothuis, Dennis R ^a,d  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF DEBRECEN   (Hungary)

^d EVANSTON HOSPITAL   (United States)

Author keywords

Blood brain barrier; Brain tumor; Glioma; Microvessels; Morphometry; Permeability; Ultrastructure

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL DIAMETER; BRAIN CAPILLARY; BRAIN TUMOR; CAPILLARY DENSITY; ELECTRON MICROSCOPY; MEMBRANE PERMEABILITY; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; TUMOR VASCULARIZATION;

ANIMALIA; MAIZE STREAK VIRUS;

EID: 0032754657     PISSN: 00262862     EISSN: None     Source Type: Journal    
DOI: 10.1006/mvre.1999.2188     Document Type: Article

References (88)

1. Aas, A. T., Brun, A., Blennow, C., Stromblad, S., and Salford, L. G. (1995). The RG2 rat glioma model. J. Neurooncol. 23, 175-183.
2. Assimakopoulou, M., Sotiropoulou-Bonikou, G., Maraziotis, T., Papadakis, N., and Varakis, I. (1997). Microvessel density in brain tumors. Anticancer Res. 17, 4747-4754.
3. Ausprunk, D. H., and Folkman, J. (1977). Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc. Res. 14, 53-64.
4. Axelsson, K., Ljung, B. E., Moore, D. H., Thor, A. D., Chew, K. L., Edgerton, S. M., Smith, H. S., and Mayall, B. H. (1995). Tumor angiogenesis as a prognostic assay for invasive ductal breast carcinoma. J. Natl. Cancer Inst. 87, 997-1008.
5. Barnett, P. A., Roman-Goldstein, S., Ramsey, F., McCormick, C. I., Sexton, G., Szumowski, J., and Neuwelt, E. A. (1995). Differential permeability and quantitative MR imaging of a human lung carcinoma brain xenograft in the nude rat. Am. J. Pathol. 146, 436-449.
6. Barth, R. F. (1998). Rat brain tumor models in experimental neurooncology: The 91, C6, T9, F98, RG-2 (D74), RT-2 and CNS1 gliomas. J. Neurooncol. 36, 91-102.
7. Bearer, E. L., and Orci, L. (1985). Endothelial fenestral diaphragms: A quick-freeze, deep-etch study. J. Cell Biol. 100, 418-428.
8. Behrens, P. F., Warnke, P. C., Bigner, D. D., and Groothuis, D. R. (1994). Monoclonal antibody 81C6 distribution, permeability and cellular proliferation in human glioma brain xenografts: a triple label autoradiographic study. Proc. Am. Assoc. Cancer Res. 35, 422.
9. Bigner, D. D., Bigner, S. H., Ponten, J., Westermark, B., Mahaley, M. S., Ruoslahti, E., Herschman, H., Eng, L. F., and Wikstrand, C. J. (1981). Heterogeneity of genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J. Neuropathol. Exp. Neurol. 40, 201-229.
10. Blasberg, R. G., and Groothuis, D. R. (1986). Chemotherapy of brain tumors: Physiological and pharmacokinetic considerations. Semin. Oncol. 13, 70-83.
11. Blasberg, R. G., Kobayashi, T., Horowitz, M., Rice, J., Groothuis, D. R., Molnar, P., and Fenstermacher, J. D. (1983a). Regional blood flow in ethylnitrosourea (ENU)-induced brain tumors. Ann. Neurol. 14, 189-201.
12. Blasberg, R. G., Kobayashi, T., Horowitz, M., Rice, J., Groothuis, D. R., Molnar, P., and Fenstermacher, J. D. (1983b). Regional blood-to-tissue transport in ethylnitrosourea (ENU)-induced brain tumors. Ann. Neurol. 14, 202-215.
13. Blasberg, R. G., Nakagawa, H., Bourdon, M. A., Groothuis, D. R., Patlak, C. S., and Bigner, D. D. (1987). Regional localization of a glioma associated antigen defined by monoclonal antibody 81C6: Implications for diagnosis and therapy. Cancer Res. 47, 4432-4443.
14. Blasberg, R. G., Patlak, C. S., and Fenstermacher, J. D. (1983c). The transport of alpha-aminoisobutyric acid across brain capillary and cellular membranes. J. Cereb. Blood Flow Metab. 3, 8-32.
15. Coomber, B. L., Stewart, P. A., Hayakawa, E. M., Farrell, C. L., and Del Maestro, R. F. (1988). A quantitative assessment of microvessel ultrastructure in C6 astrocytoma spheroids transplanted to brain and to muscle. J. Neuropathol. Exp. Neurol. 47, 29-40.
16. Crone, C. (1963). The permeability of capillaries in various organs as determined by the use of the "indicator diffusion" method. Acta Physiol. Scand. 59, 292-305.
17. Deane, B. R., and Lantos, P. L. (1981). The vasculature of experimental brain tumours. Part 2. A quantitative assessment of morphological abnormalities. J. Neuropathol. Exp. Neurol. 49, 67-77.
18. Dellian, M., Witwer, B. P., Salehi, H. A., Yuan, F., and Jain, R. K. (1996). Quantitation and physiological characterization of angiogenic vessels in mice: Effect of basic fibroblast growth factor, vascular endothelial growth factor/vascular permeability factor, and host microenvironment. Am. J. Pathol. 149, 59-71.
19. Donelli, M. G., Zucchetti, M., and D'Incalci, M. D. (1992). Do anti-cancer agents reach the tumor target in the human brain? Canc. Chemother. Pharmacol. 30, 251-260.
20. Fenstermacher, J. D., Blasberg, R. G., and Patlak, C. S. (1981). Methods for quantifying the transport of drugs across brain barrier systems. Pharmacol. Therapeut. 14, 217-248.
21. Fenstermacher, J. D., Nakata, H., Tajima, A., Yen, M.-H., Acuff, V., and Gruber, K. (1992). Structural, ultrastructural, and functional correlations among local capillary systems with the brain. In "Barriers and Fluids of the Eye and Brain" (M. Segal, Ed.), pp. 59-71, MacMillan, London.
22. Glauert, A. (1974). "Practical Methods in Electron Microscopy." North Holland, Amsterdam.
23. Groothuis, D. R., and Blasberg, R. G. (1985). Rational brain tumor chemotherapy: the interaction of drug and tumor. In "Neurological Clinics, Neuro-Oncology" (N. A. Vick and D. D. Bigner, Eds.), pp. 801-816.
24. Groothuis, D. R., Fischer, J. M., Lapin, G. D., Bigner, D. D., and Vick, N. A. (1982). Permeability of different brain tumor models to horseradish peroxidase. J. Neuropathol. Exp. Neurol. 41, 164-185.
25. Groothuis, D. R., Fischer, J. M., Pasternak, J. F., Blasberg, R. G., Bigner, D. D., and Vick, N. A. (1983a). Regional measurements of blood-to-tissue transport in transplanted RG-2 rat gliomas. Cancer Res. 43, 3368-3373.
26. Groothuis, D. R., Molnar, P., and Blasberg, R. G. (1984). Regional blood flow and blood-to-tissue transport in five brain tumor models: Implications for chemotherapy. In "Progress in Experimental Brain Tumor Research" (M. Rosenblum and C. Wilson, Eds.), pp. 132-153. Karger, Basel.
27. Groothuis, D. R., Pasternak, J. F., Fischer, J. M., Blasberg, R. G., Bigner, D. D., and Vick, N. A. (1983b). Regional measurements of blood flow in transplanted RG-2 rat gliomas. Cancer Res. 43, 3362-3367.
28. Groothuis, D. R., Vriesendorp, F. J., Kupfer, B., Warnke, P. C., Lapin, G. D., Kuruvilla, A., Vick, N. A., Mikhael, M. A., and Patlak, C. S. (1991). Quantitative measurements of capillary transport in human brain tumors by computed tomography. Ann. Neurol. 30, 581-588.
29. Gross, P. M., Sposito, N. M., Pettersen, S. E., Panton, D. G., and Fenstermacher, J. D. (1987). Topography of capillary density, glucose metabolism, and microvascular function within the rat inferior colliculus. J. Cereb. Blood Flow Metab. 7, 154-160.
30. Hobbs, S. K., Monsky, W. L., Yuan, F., Roberts, W. G., Griffith, L., Torchilin, V. P., and Jain, R. K. (1998). Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl. Acad. Sci. USA 95, 4607-4612.
31. Jain, R. K. (1987). Transport of molecules across tumor vasculature. Canc. Metas. Rev. 6, 559-593.
32. Jain, R. K. (1990). Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Canc. Metas. Rev. 9, 253-266.
33. Jain, R. K. (1994). Barriers to drug delivery in solid tumors. Sci. Am. 271, 58-65.
34. Jain, R. K. (1996). Delivery of molecular medicine to solid tumors. Science 271, 1079-1080.
35. Jain, R. K. (1998). The next frontier of molecular medicine: Delivery of therapeutics. Nat. Med. 4, 655-657.
36. 82Rb: The effect of dexameth-asone and whole-brain radiation therapy. Ann. Neurol. 18, 636-646.
37. Karlsson, U., and Schultz, R. L. (1965). Fixation of the central nervous system for electron microscopy by aldehyde perfusion. J. Ultrastruct. Res. 12, 160-206.
38. Kayar, S. R., Archer, P. G., Lechner, A. J., and Banchero, N. (1982). The closest-individual method in the analysis of the distribution of capillaries. Microvasc. Res. 24, 326-341.
39. Kaye, A. H., and Laws, E. R. (1995). "Brain Tumors: An Encyclopedic Approach," Churchill Livingstone, Edinburgh.
40. Kenney, J., Schmiedl, U., Maravilla, K., Starr, F., Graham, M., Spence, A., and Nelson, J. (1992). Measurement of blood brain barrier permeability in a tumor model using magnetic resonance imaging with gadolinium DTPA. Magn. Reson. Med. 27, 68-75.
41. Knierim, M., Paweletz, N., and Finze, E.-M. (1986). Tumor-related reconstitutive vascularization. An ultrastructural study. Anticancer Res. 6, 1305-1316.
42. Koestner, A., Swenberg, J. A., and Wechsler, W. (1971). Transplacental production with ethylnitrosourea of neoplasms in the nervous system of Sprague-Dawley rats. Am. J. Pathol. 63, 37-50.
43. Konerding, M. A., Miodonski, A. J., and Lametschwandtner, A. (1995). Microvascular corrosion casting in the study of tumor vascularity: A review. Scanning Microsc. 9, 1233-1244.
44. Kroll, R. A., Pagel, M. A., Langone, J. J., Sexton, G. J., and Neuwelt, E. A. (1994). Differential permeability of the blood tumour barrier in intracerebral tumour bearing rats: Antidrug antibody to achieve systemic drug rescue. Ther. Immunol. 1, 333-341.
45. Lapin, G. D. (1994). Modeling drug delivery to brain tissue. In "Polymeric Site-Specific Pharmacotherapy" (A. J. Domb, Ed.), pp. 70-93, Wiley, Chichester.
46. Lee, Y. S., Bigner, S. H., Eng, L. F., Molnar, P., Kuruvilla, A., Groothuis, D. R., and Bigner, D. D. (1986). A glial fibrillary acidic protein-expressing and tumorigenic cell line derived from an avian sarcoma virus-induced rat glioma. J. Neuropathol. Exp. Neurol. 45, 704-720.
47. Levin, V. A., Patlak, C. S., and Landahl, H. D. (1980). Heuristic modeling of drug delivery to malignant brain tumors. J. Pharmacokinet. Biopharm. 8, 257-296.
48. Lin, S.-Z., Sposito, N., Pettersen, S., Rybacki, L., McKenna, E., Pettigrew, K., and Fenstermacher, J. (1990). Cerebral capillary bed structure of normotensive and chronically hypertensive rats. Microvasc. Res. 40, 341-357.
49. Miyagawa, T., Oku, T., Uehara, H., Desai, R., Beattie, B., Tjuvajev, J., and Blasberg, R. (1998). "Facilitated" amino acid transport is upregulated in brain tumors. J. Cereb. Blood Flow Metab. 18, 500-509.
50. 125I-albumin distribution in experimental RG-2 gliomas and adjacent brain. J. Cereb. Blood Flow Metab. 7, 687-701.
51. Nishio, S., Ohta, M., Abe, M., and Kitamura, K. (1983). Microvascular abnormalities in ethylnitrosourea(ENU)-induced rat brain tumors: Structural basis for altered blood-brain barrier function. Acta Neuropathol. 59, 1-10.
52. 30 for microvessel characterization in an intracranial glioma model. J. Magn. Reson. Imag. 8, 799-806.
53. Paku, S., and Paweletz, N. (1991). First steps of tumor-related angiogenesis. Lab. Invest. 65, 334-346.
54. Plate, K. H. (1999). Mechanisms of angiogenesis in the brain. J. Neuropath. Exp. Neurol. 58, 313-320.
55. Renkin, E. M. (1959). Transport of potassium-42 from blood to tissue in isolated mammalian skeletal muscle. Am. J. Physiol. 197, 1205-1210.
56. Rhodin, J. A. G. (1962). The diaphragm of capillary endothelial fenestrations. J. Ultrastruct. Res. 6, 171-185.
57. Roberts, W. G., and Palade, G. E. (1997). Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 57, 765-772.
58. Robinson, P. J., and Rapoport, S. I. (1990). Model for drug uptake by brain tumors: Effect of osmotic treatment and of diffusion in brain. J. Cereb. Blood Flow Metab. 10, 153-161.
59. Sakurada, O., Kennedy, C., Jehle, J., Brown, J. D., Carbin, G., and Sokoloff, L. (1978). Measurement of local cerebral blood flow with iodo[14C]antipyrine. Am. J. Physiol. 234, H59-H66.
60. Schold, S. C., Jr., Zalutsky, M. R., Coleman, R. E., Glantz, M. J., Friedman, A. H., Jaszczak, R. J., Bigner, S. H., and Bigner, D. D. (1993). Distribution and dosimetry of 1-123 labeled monoclonal antibody 81C6 in patients with anaplastic glioma. Invest. Radiol. 28, 488-496.
61. Schor, A. M., Pendleton, N., Pazouki, S., Smither, R. L., Morris, J., Lessan, K., Heerkens, E., Chandrachud, L. M., Carmichael, G., Adi, M., Chisholm, D. M., and Stevenson, H. (1998). Assessment of vascularity in histological sections: effects of methodology and value as an index of angiogenesis in breast tumours. Histochem. J. 30, 849-856.
62. Schuster, J. M., and Bigner, D. D. (1992). Immunotherapy and monoclonal antibody therapies. Curr. Opin. Oncol. 4, 547-552.
63. Seitz, R. J., and Weschler, W. (1986). Vascularization of human cerebral gliomas: A lectin-cytochemical and morphometric study. In "Biology of Brain Tumour" (M. D. Walker and D. G. T. Thomas, Eds.), pp. 131-137. Martinus Nijhoff, Boston.
64. Sipos, E. P., and Brem, H. (1995). New delivery systems for brain tumor therapy. Neurol. Clin. 13, 813-825.
65. Stewart, D. J. (1989). The role of chemotherapy in the treatment of gliomas in adults. Cancer Treat. Rev. 16, 129-160.
66. Stewart, P. A., Farrell, C. L., and Del Maestro, R. F. (1991). The effect of cellular microenvironment on vessels in the brain. Part 1: Vessel structure in tumor, peritumour and brain from humans with malignant glioma. Int. J. Radiat. Biol. 60, 125-130.
67. Stewart, P. A., Hayakawa, K., Farrell, C. L., and Del Maestro, R. (1985). A quantitative study of blood-brain barrier permeability ultrastructure in a new rat glioma model. Acta Neuropathol. 67, 96-102.
68. Uehara, H., Miyagawa, T., Tjuvajev, J., Joshi, R., Beattie, B., Oku, T., Finn, R., and Blasberg, R. (1997). Imaging experimental brain tumors with 1-aminocyclopentante carboxylic acid and alpha-aminoisobutyric acid: Comparison to fluorodeoxyglucose and diethelenetriaminepentaacetic acid in morphologically defined tumor regions. J. Cereb. Blood Flow Metab. 17, 1239-1253.
69. Vartanian, R. K., and Weidner, N. (1994). Correlation of intratumoral endothelial cell proliferation with microvessel density (tumor angiogenesis) and tumor cell proliferation in breast carcinoma. Am. J. Pathol. 144, 1188-1194.
70. Vick, N. A. (1980). Brain Tumor Microvasculature. In "Brain Metastasis" (L. Weiss, H. A. Gilbert, and J. B. Posner, Eds.), pp. 100-114. G. K. Hall, Boston.
71. Vick, N. A., and Bigner, D. D. (1972). Microvascular abnormalities in virally-induced canine brain tumors: Structural bases for altered blood-brain barrier function. J. Neurol. Sci. 17, 29-39.
72. Villars, F. M. H., and Benedek, G. B. (1974). "Physics with Illustrative Examples from Medicine and Biology: Statistical Physics," Addison-Wesley, Reading, MA.
73. Vriesendorp, F. J., Groothuis, D. R., and Vick, N. A. (1984). Murine sarcoma virus-induced brain tumors: Concurrent measurements of blood flow and transcapillary transport. J. Neurooncol. 2, 301-314.
74. Vriesendorp, F. J., Peagram, C., Bigner, D. D., and Groothuis, D. R. (1987). Concurrent measurements of blood flow and transcapillary transport in xenotransplanted human gliomas in immunosuppressed rats. J. Natl. Cancer Inst. 79, 123-130.
75. Waggener, J. D., and Beggs, J. L. (1976). Vasculature of neural neoplasms. In "Neoplasia in the Central Nervous System" (R. A. Thompson and J. R. Green, Eds.), pp. 27-50. Raven Press, NY.
76. Walter, K. A., Tamargo, R. J., Olivi, A., Burger, P. C., and Brem, H. (1995). Intratumoral chemotherapy. Neurosurgery 37, 1129-1145.
77. Warnke, P. C., Blasberg, R. G., and Groothuis, D. R. (1987). The effect of hyperosmotic blood-brain barrier disruption on blood-to-tissue transport in ENU-induced gliomas. Ann. Neurol. 22, 300-305.
78. Weibel, E. R. (1979). "Stereological Methods. Volume 1: Practical Methods for Biological Morphometry," Academic Press, New York.
79. Weibel, E. R. (1980). "Stereological Methods. Volume 2: Theoretical Foundations," Academic Press, New York.
80. Weinbaum, S., Tsay, R., and Curry, F. E. (1992). A three-dimensional junction-pore-matrix model for capillary permeability. Microvasc. Res. 44, 85-111.
81. Wesseling, P., van der Laak, J. A., de Leeuw, H., Ruiter, D. J., and Burger, P. C. (1994). Quantitative immunohistological analysis of the microvasculature in untreated human glioblastoma multiforme. Computer assisted image analysis of whole tumor sections. J. Neurosurg. 81, 902-909.
82. Wesseling, P., van der Laak, J. A., Link, M., Teepen, H. L., and Ruiter, D. J. (1998). Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum. Pathol. 29, 352-358.
83. Wiederhold, K.-H., Bielser, W., Schulz, U., Veteau, M.-J., and Hunziker, O. (1976). Three-dimensional reconstruction of brain capillaries from frozen serial sections. Microvasc. Res. 11, 175-180.
84. Yoshida, J., Wakabayashi, T., Mizuno, M., Sugita, K., Seo, H., Oshima, M., Tadokoro, M., and Sakuma, S. (1992). Tumor specific binding of radiolabeled G 22 monoclonal antibody in glioma patients. Neurol. Medico-Chirurg. 32, 125-129.
85. Yoshii, Y., and Sugiyama, K. (1988). Intercapillary distance in the proliferating area of human glioma. Cancer Res. 48, 2938-2941.
86. Yuan, F., Dellian, M., Fukumura, D., Leunig, M., Berk, D. A., Torchilin, V. P., and Jain, R. K. (1995). Vascular permeability in a human tumor xenograft: Molecular size dependence and cutoff size. Cancer Res. 55, 3752-3756.
87. Yuan, F., Salehi, H. A., Boucher, Y., Vasthare, U. S., Tuma, R. F., and Jain, R. K. (1994). Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 54, 4564-4568.
88. Yung, W. K., Blank, N. K., and Vick, N. A. (1976). 'Glioblastoma': Induction of a reproducible autochthonous tumor in rats with murine sarcoma virus. Neurology 26, 76-83.