Quantitative angiogenesis assays: Progress and problems

Nature Medicine

Volumn 3, Issue 11, 1997, Pages 1203-1208

  Jain, Rakesh K ^a   Schlenger, Karlheinz ^b   Höckel, Michael ^b   Yuan, Fan ^c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CANCER GROWTH; CARCINOGENESIS; CONTROLLED STUDY; METASTASIS; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; TUMOR VASCULARIZATION;

ANIMALIA;

EID: 0030669894     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1197-1203     Document Type: Review

References (82)

1. Folkman, J. Tumor angiogenesis. in The Molecular Basis of Cancer (eds. Mendelsohn, J., Howley, P.M., Israel, M.A. & Liotta, L.A.) 206-232 (W.B. Saunders, Philadelphia, 1995).
2. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med. 1, 27-31 (1995).
3. Hanahan, D. Signaling vascular morphogenesis and maintenance. Science 277, 48-50 (1997).
4. Risau, W. Mechanisms of angiogenesis. Nature 386, 671-674 (1997).
5. Höckel, M., Schlenger, K., Doctrow, S., Kissel, T. & Vaupel, P. Therapeutic angiogenesis. Arch. Surg. 128, 423-429 (1993).
6. Ware, J.A. & Simons, M. Angiogenesis in ischemic heart disease. Nature Med. 3, 158-164 (1997).
7. Auerbach, R., Auerbach, W. & Polakowski, I. Assays for angiogenesis: A review. Pharmacol. Ther. 51, 1-11 (1991).
8. Fan, T.-P.D. & Polverini, P.J. In vivo models of Angiogenesis. in Tumor angiogenesis (eds. Bicknell, R., Lewis, C.E. & Ferrara, N.) 5-18 (Oxford University Press, Oxford, 1997).
9. Patan, S., Munn, L.L. & Jain, R.K. Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft: A novel mechanism of tumor angiogenesis. Microvasc. Res. 51, 260-272 (1996).
10. Ausprunk, D.H. & Folkman, J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc. Res. 14, 53-65 (1977).
11. Sholley, M.M., Ferguson, G.P., Seibel, H.R., Montour, J.L. & Wilson, J.D. Mechanisms of neovascularization: Vascular sprouting can occur without proliferation of endothelial cells. Lab. Invest. 51, 624-634 (1984).
12. Jain, R.K. 1996 Landis Award Lecture: Delivery of molecular and cellular medicine to solid tumors. Microcirculation 4, 1-23 (1997).
13. Sandison, J.C. A new method for the microscopic study of living growing tissues by the introduction of a transparent chamber in the rabbit's ear. Anat. Rec. 28, 281-287 (1924).
14. Ide, A.G., Baker, N.H. & Warren, S.L. Vascularization of the Brown-Pearce rabbit epithelioma transplant as seen in the transparent ear chamber. Am. J. Roentgenol. 42, 891-899 (1939).
15. Zawicki, D.F., Jain, R.K., Schmid-Schoenbein, G.W. & Chien, S. Dynamics of neovascularization in normal tissue. Microvasc. Res. 21, 27-47 (1981).
16. Dudar, T.E. & Jain, R.K. Microcirculatory flow changes during tissue growth. Microvasc. Res. 25, 1-21 (1983).
17. Gerlowski, L. & Jain, R.K. Microvascular permeability of normal and neoplastic tissues. Microvasc. Res. 31, 288-305 (1986).
18. Algire, G.H. An adaptation of the transparent chamber technique to the mouse. J. Natl. Cancer Inst. USA 4, 1-11 (1943).
19. Algire, G.H. & Chalkley, H.W. Vascular reactions of normal and malignant tissues in vivo. I. Vascular reactions of mice to wounds and to normal and neoplastic transplants. J. Natl. Cancer Inst. USA 6, 73-85 (1945).
20. Leunig, M. et al. Angiogenesis, microvascular architecture, microhemodynamics, and interstitial fluid pressure during early growth of human adenocarcinoma LS174T in SCID mice. Cancer Res. 52, 6553-6560 (1992).
21. Dellian, M., Witwer, B.P., Salehi, H.A., Yuan, F. & Jain, R.K. 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, 59-72 (1996).
22. Greenblatt, M. & Shubik, P. Tumor angiogenesis: Transfilter diffusion studies in the hamster by the transparent chamber technique. J. Natl. Cancer Inst. USA 41, 111-124 (1968).
23. Brooks, P.C. et al. Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J. Clin. Invest. 96, 1815-1822 (1995).
24. Briscoe, D.M. et al. The problem of chronic rejection: influence of leukocyte-endothelial interactions. Kidney Int. (suppl.) 58, S22-S27 (1997).
25. Levasseur, J.E., Wei, E.P., Raper, A.J., Kontos, H.A. & Patterson, J.J.L. Detailed description of a cranial window technique for acute and chronic experiments. Stroke 6, 308-317 (1975).
26. Yuan, F. et al. Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 54, 4564-4568 (1994).
27. Yuan, F. et al. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc. Nat. Acad. Sci. USA 93, 14765-14770 (1996).
28. Sckell, A., Safabakhsh, N. & Jain, R.K. Tumor size dependence of growth factor induced angiogenesis: Response in in vivo gel assays (abstract). Microcirculation 4, 145 (1997).
29. Zietman, A.L., Suit, H.D., Ramsay, J.R., Silobrcic, V. & Sedlacek, R.S. Quantitative studies on the transplantability of murine and human tumors into the brain and subcutaneous tissues of NCr/Sed nude mice. Cancer Res. 48, 6510-6516 (1988).
30. Joyner, W.L. & Gilmore, J.P. Tissues grafted into the cheek pouch of the hamster. in Microcirculatory Technology (eds. Baker, C.H. & Nastuk, W.L.) 3-17 (Academic Press, New York, 1986).
31. Heuser, L.S. & Miller, F.N. Differential macromolecular leakage from the vasculature of tumors. Cancer 57, 461-464 (1986).
32. Zeidman, I. The fate of circulating tumor cells: I. Passage of cells through capillaries. Cancer Res. 21, 38-39 (1961).
33. Fukumura, D., Yuan, F., Monsky, W.L., Chen, Y. & Jain, R.K. Effect of host microenvironment on the microcirculation of human colon adenocarcinoma LS174T. Am. J. Pathol. 151, 679-688 (1997).
34. Runkel, S., Hunter, N. & Milas, L. An intradermal assay for quantification and kinetics studies of tumor angiogenesis in mice. Radiat. Res. 126, 237-243 (1991).
35. Leighton, J. The Spread of Cancer: Pathogenesis, Experimental Methods, Interpretations (Academic Press, New York, 1967).
36. Auerbach, R., Arensman, R., Kubai, L. & Folkman, J. Tumor-induced angiogenesis: Lack of inhibition by irradiation. Int. J. Cancer 15, 241-245 (1975).
37. Nguyen, M., Shing, Y. & Folkman, J. Quantitation of angiogenesis and antiangiogenesis in the chick embryo chorioallantoic membrane. Microvasc. Res. 47, 31-40 (1994).
38. v integrins. Science 270, 1500-1502 (1995).
39. Taylor, C.M. & Weiss, J.B. The chick vitelline membrane as a test system for angiogenesis and antiangiogenesis (abstract). Int. J. Microcirc. Clin. Exp. 3, 337 (1984).
40. Gimbrone, M.A., Leapman, S.B., Cotran, R.S. & Folkman, J. Tumor dormancy in vivo by prevention of neovascularization. J. Exp. Med. 136, 261-276 (1972).
41. Gimbrone, M.A. & Gullino, P.M. Angiogenic capacity of preneoplastic lesions of the murine mammary gland as a marker of neoplastic transformation. Cancer Res. 36, 2611-2620 (1976).
42. Brem, S.S., Gullino, P.M. & Medina, D. Angiogenesis: A marker for neoplastic transformation of mammary papillary hyperplasia. Science 195, 880-882 (1977).
43. Maiorana, A. & Gullino, P.M. Acquisition of angiogenic capacity and neoplastic transformation in the rat mammary gland. Cancer Res. 38, 4409-4414 (1978).
44. Klintworth, G.K. Corneal Angiogenesis: A Comprehensive Critical Review (Springer, New York, 1991).
45. Gimbrone, M.A.J., Cotran, R.S., Leapman, S.B. & Folkman, J. Tumor growth and neovascularization: An experimental model using the rabbit cornea. J. Natl. Cancer Inst. 52, 413-427 (1974).
46. Muthukkaruppan, V.R. & Auerbach, R. Angiogenesis in the mouse cornea. Science 205, 1416-1418 (1979).
47. Schlenger, K., Höckel, M., Schwab, R., Frischmann-Berger, R. & Vaupel, P. How to improve the uterotomy healing: I. Effects of fibrin and tumor necrosis factor-α in the rat uterotomy model. J. Surg. Res. 56, 235-241 (1994).
48. Dvorak, H.F. et al. Fibrin containing gels induce angiogenesis: Implications for tumor stroma generation and wound healing. Lab. Invest. 57, 673-686 (1987).
49. Mahadevan, V., Hart, I.R. & Lewis, G.P. Factors influencing blood supply in wound granuloma quantitated by a new in vivo technique. Cancer Res. 49, 415-419 (1989).
50. Plunkett, M.L. & Hailey, J.A. An in vivo quantitative angiogenesis model using tumor cells entrapped in alginate. Lab. Invest. 62, 510-517 (1990).
51. Passaniti, A. et al. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab. Invest. 67, 519-528 (1992).
52. Kowalski, J., Kwan, H.H., Prionas, S.D., Allison, A.C. & Fajardo, L.F. Characterization and applications of the disc angiogenesis system. Exp. Mol. Pathol. 56, 1-19 (1992).
53. Jain, R.K. Determinants of tumor blood flow: A review. Cancer Res. 48, 2641-2658 (1988).
54. Gasparini, G. Prognostic and predictive value of intra-tumoral microvessel density in human solid tumors. in Tumor Angiogenesis (eds. Bicknell, R., Lewis, C.E. & Ferrara, N.) 29-44, (Oxford University Press, Oxford, 1997).
55. Gullino, P.M. & Grantham, F.H. Studies on the exchange of fluids between host and tumor: III. Regulation of blood flow in hepatomas and other rat tumors. J. Natl. Cancer Inst. 28, 211-227 (1962).
56. Less, J.R., Posner, M.C., Skalak, T., Wolmark, N. & Jain, R.K. Geometric resistance to blood flow and vascular network architecture in human colorectal carcinoma. Microcirculation 4, 25-33 (1997).
57. Brem, S., Cotran, R. & Folkman, J. Tumor angiogenesis: A quantitative method for histologic grading. J. Natl. Cancer Inst. 48, 347-356 (1972).
58. Srivastava, A., Laidler, P., Hughes, L.E., Woodcock, J. & Shedden, E.J. Neovascularization in human cutaneous melanoma: A quantitative morphological and Doppler ultrasound study. Eur. J. Cancer Clin. Oncol. 22, 1205-1209 (1986).
59. Weidner, N., Semple, J.P., Welch, W.R. & Folkman, J. Tumor angiogenesis and metastasis - Correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8 (1991).
60. Perez-Atayde, A.R. et al. Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia. Am. J. Pathol. 150, 815-821 (1997).
61. Montesano, R. Regulation of angiogenesis in vitro. Eur. J. Clin. Invest. 22, 504-515 (1992).
62. Montesano, R., Vassalli, J.D., Baird, A., Guillemin, R. & Orci, L. Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. USA 83, 7297-7301 (1986).
63. Sankar, S. et al. Modulation of transforming growth factor beta receptor levels on microvascular endothelial cells during in vitro angiogenesis. J. Clin. Invest. 97, 1436-1446 (1996).
64. Jain, R.K. & Helmlinger, G. Tumor microenvironment and microcirculation: A dynamic interplay. in An International Workshop - The tumor microenvironment (Martha's Vineyard, MA, 1997).
65. Alessandri, G., Rayu, K. & Gullino, P.M. Mobilization of capillary endothelium in vitro induced by effectors of angiogeneses in vivo. Cancer Res. 43, 1790-1797 (1983).
66. Alessandri, G., Cornaglia-Ferraris, P. & Gullino, P.M. Angiogenic and angiostatic microenvironment in tumors - Role of gangliosides. Acta. Oncol. 36, 383-387 (1997).
67. Holmgren, L., O'Reilly, M.S. & Folkman, J. Dormancy of micrometastases: Balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Med. 1, 149-153 (1995).
68. Denekamp, J. Review article: Angiogenesis, neovascular proliferation and vascular pathophysiology as targets for cancer therapy. Br. J. Radiol. 66, 181-196 (1993).
69. Jain, R.K. et al. Leukocyte-endothelial adhesion and angiogenesis in tumors. Cancer Metastasis Rev. 15, 195-204 (1996).
70. Clark, E.R., Kirby-Smith, H.T., Rex, R.O. & Williams, R.G. Recent modifications in the method of studying living cells and tissues in transparent chambers inserted in the rabbit's ear. Anat. Rec. 47, 187-211 (1930).
71. Leunig, M., Yuan, F., Berk, D.A., Gerweck, L. & Jain, R.K. Angiogenesis and regeneration of grafted bone in dorsal skin chamber of nude mice. Lab. Invest. 71, 300-307 (1994).
72. Yamada, S. et al. Rolling in P-selectin-deficient mice is reduced but not eliminated in the dorsal skin. Blood 86, 3487-3492 (1995).
73. Endrich, B., Intaglietta, M., Reinhold, H.S. & Gross, J.F. Hemodynamic characteristics in microcirculatory blood channels during early tumor growth. Cancer Res. 39, 17-23 (1979).
74. Dewhirst, M.W. et al. Morphologic and hemodynamic comparison of tumor and healing normal tissue microvasculature. Int. J. Radiat. Oncol. Biol. Phys. 17, 91-99 (1989).
75. Eddy, H.A. & Casarett, G.W. Development of the vascular system in the hamster malignant neurilemmoma. Microvasc. Res. 6, 63-82 (1973).
76. Lutz, B.R., Fulton, G.P., Patt, D.I. & Handler, A.H. The growth rate of tumor transplants in the cheek pouch of the hamster (Mesocricetus auratus). Cancer Res. 10, 231-232 (1950).
77. Sidky, Y.A. & Auerbach, R. Lymphocyte-induced angiogenesis: A quantitative and sensitive assay of the graft-vs.-host reaction. J. Exp. Med. 141, 1084-1100 (1975).
78. Auerbach, R., Kubai, L., Knighton, D. & Folkman, J. A simple procedure for the long-term cultivation of chicken embryos. Dev. Biol. 41, 391-394 (1974).
79. Norrby, K., Jakobsson, A. & Sörbo, J. Quantitative angiogenesis in spreads of intact rat mesenteric windows. Microvasc. Res. 39, 341-348 (1990).
80. Luckè, B. & Schlumberger, H.G. The effect of X-rays on frog carcinoma studied by direct microscopic examination of living intra-ocular transplants. Cancer Res. 10, 231 (1950).
81. Less, J.R., Skalak, T.C., Sevick, E.M. & Jain, R.K. Microvascular architecture in a mammary carcinoma: Branching patterns and vessel dimensions. Cancer Res. 51, 265-273 (1991).
82. Gullino, P.M. & Grantham, F.H. Studies on the exchange of fluids between host and tumor. I. A method for growing "Tissue-isolated" tumors in laboratory animals. J. Natl. Cancer. Inst. 27, 679-693 (1961).