Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: Insights from a mathematical model

Cancer Research

Volumn 67, Issue 6, 2007, Pages 2729-2735

  Jain, Rakesh K ^a   Tong, Ricky T ^a,b   Munn, Lance L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; GROWTH FACTOR; MONOCLONAL ANTIBODY DC101; VASCULOTROPIN A; VASCULOTROPIN C;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER CELL; DRUG EFFECT; EDEMA; HYDRAULIC CONDUCTIVITY; HYDRAULIC PERMEABILITY; HYPERTENSION; INTERSTITIUM; LYMPH NODE METASTASIS; MATHEMATICAL MODEL; PRIORITY JOURNAL; SENTINEL LYMPH NODE; TISSUE PRESSURE; TUMOR GROWTH; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; CAPILLARY PERMEABILITY; EDEMA; EXTRACELLULAR FLUID; HUMANS; LYMPHATIC METASTASIS; MATHEMATICAL COMPUTING; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 34047260282     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-4102     Document Type: Article

References (52)

1. Jain RK. Barriers to drug delivery in solid tumors. Sci Am 1994;271:58-65.
2. Jain RK. Transport of molecules in the tumor interstitium: a review. Cancer Res 1987;47:3038-50.
3. Jain RK. Transport of molecules across tumor vasculature. Cancer Metastasis Rev 1987;6:559-94.
4. Boucher Y, Jain RK. Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res 1992;52:5110-4.
5. Boucher Y, Leunig M, Jain RK. Tumor angiogenesis and interstitial hypertension. Cancer Res 1996;56:4264-6.
6. Netti PA, Baxter LT, Boucher Y, Skalak R, Jain RK. Time-dependent behavior of interstitial fluid pressure in solid tumors: implications for drug delivery. Cancer Res 1995;55:5451-8.
7. Netti PA, Hamberg LM, Babich JW, et al. Enhancement of fluid filtration across tumor vessels: implication for delivery of macromolecules. Proc Natl Acad Sci U S A 1999;96:3137-42.
8. Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK. Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res 2000;60:4324-7.
9. Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002;296:1883-6.
10. Jain RK, Fenton BT. Intra-tumor lymphatic vessels: a case of mistaken identity or malfunction? J Natl Cancer Inst 2002;94:417-21.
11. Padera TP, Stoll BR, Tooredman JB, et al. Pathology: cancer cells compress intratumour vessels. Nature 2004; 427:695.
12. Isaka N, Padera TP, Hagendoorn J, Fukumura D, Jain RK. Peritumor lymphatics induced by vascular endothelial growth factor-C exhibit abnormal function. Cancer Res 2004;64:4400-4.
13. Nathanson S. Insights into the mechanisms of lymph node metastasis. Cancer 2003;98:413-23.
14. Jain RK, Baxter LT. Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure. Cancer Res 1988;48:7022-32.
15. Baxter LT, Jain RK, Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. Microvasc Res 1989;37:77-104.
16. Baxter LT, Jain RK. Transport of fluid and macromolecules in tumors. II. Role of heterogeneous perfusion and lymphatics. Microvasc Res 1990;40:246-63.
17. Baxter LT, Jain RK. Transport of fluid and macromolecules in tumors. III. Role of binding and metabolism. Microvasc Res 1991;41:5-23.
18. Boucher Y, Baxter LT, Jain RK. Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy. Cancer Res 1990;50:4478-84.
19. Butler TP, Grantham FH, Gullino PM. Bulk transfer of fluid in the interstitial compartment of mammary tumors. Cancer Res 1975;35:3084-8.
20. Sevick EM, Jain RK. Blood flow and venous pH of tissue-isolated Walker 256 carcinoma during hyperglycemia. Cancer Res 1988;48:1201-7.
21. Sevick EM, Jain RK. Measurement of capillary filtration coefficient in a solid tumor. Cancer Res 1991; 51:1352-5.
22. Less JR, Posner MC, Skalak T, Wolmark N, Jain RK. Geometric resistance to blood flow and vascular network architecture in human colorectal carcinoma. Microcirculation 1997;4:25-33.
23. Jain RK. Normalizing tumor vasculature with antiangiogenic therapy: a new paradigm for combination therapy. Nat Med 2001;7:987-9.
24. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
25. Lee CG, Heijn M, di Tomaso E, et al. Anti-vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res 2000;60:5565-70.
26. Tong RT, Boucher Y, Kozin SV, et al. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res 2004;64:3731-6.
27. Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004;10:145-7.
28. Huber PE, Bischof M, Jenne J, et al. Trimodal cancer treatment: beneficial effects of combined antiangiogenesis, radiation, and chemotherapy. Cancer Res 2005; 65:3643-55.
29. Willett CG, Boucher Y, Duda DG, et al. Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J Clin Oncol 2005;23:8136-9.
30. Ansiaux R, Baudelet C, Jordan BF, et al. Thalidomide radiosensitizes tumors through early changes in the tumor microenvironment. Clin Cancer Res 2005;11: 743-50.
31. Wildiers H, Guetens G, De Boeck G, et al. Effect of antivascular endothelial growth factor treatment on the intratumoral uptake of CPT-11. Br J Cancer 2003;88: 1979-86.
32. Hoshida T, Isaka N, Hagendoorn J, et al. Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 2006;66:8065-75.
33. Hirakawa S, Kodama S, Kunstfeld R, et al. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005;201:1089-99.
34. Qian CN, Berghuis B, Tsarfaty G, et al. Preparing the "soil": the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res 2006;66:10365-76.
35. Xu L, Yoneda J, Herrera C, et al. Inhibition of malignant ascites and growth of human ovarian carcinoma by oral administration of a potent inhibitor of the vascular endothelial growth factor receptor tyrosine kinases. Int J Oncol 2000;16:445-54.
36. Batchelor T, Sorensen G, di Tomaso E, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007;11:83-95.
37. Hobbs SK, Monsky WL, Yuan F, et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci U S A 1998; 95:4607-12.
38. Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363-80.
39. Rippe B, Haraldsson B. Capillary permeability in rat hindquarters as determined by estimations of capillary reflection coefficients. Acta Physiol Scand 1986;127: 289-303.
40. Tyrrell JA, Mahadevan V, Tong RT, et al. A 2-D/3-D model-based method to quantify the complexity of microvasculature imaged by in vivo multiphoton microscopy. Microvasc Res 2005;70:165-78.
41. Chang YS, Munn LL, Hillsley MV, et al. Effect of vascular endothelial growth factor on cultured endothelial cell monolayer transport properties. Microvasc Res 2000;59:265-77.
42. Pocock TM, Foster RR, Bates DO. Evidence of a role for TRPC channels in VEGF-mediated increased vascular permeability in vivo. Am J Physiol Heart Circ Physiol 2003;286:H1015-26.
43. Bates DO, Curry FE. Vascular endothelial growth factor increases hydraulic conductivity of isolated perfused microvessels. Am J Physiol 1996;271:H2520-8.
44. Boucher Y, Brekken C, Netti PA, Baxter LT, Jain RK. Intratumoral infusion of fluid: estimation of hydraulic conductivity and implications for the delivery of therapeutic agents. Br J Cancer 1998;78:1442-8.
45. Yuan F, Chen Y, Dellian M, 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 Natl Acad Sci U S A 1996;93:14765-70.
46. Anderson JL, Malone DM. Mechanism of osmotic flow in porous membranes. Biophys J 1974;14:957-82.
47. Deen W. Hindered transport of large molecules in liquid-filed pores. AIChE Journal 1987;33:1409-25.
48. Jain RK, Safabakhsh N, Sckell A, et al. Endothelial cell death, angiogenesis, and microvascular function after castration in an androgen-dependent tumor: role of vascular endothelial growth factor. Proc Natl Acad Sci U S A 1998;95:10820-5.
49. Rofstad EK, Tunheim SH, Mathiesen B, et al. Pulmonary and lymph node metastasis is associated with primary tumor interstitial fluid pressure in human melanoma xenografts. Cancer Res 2002;62: 661-4.
50. Nathanson S, Nelson L. Interstitial fluid pressure in breast cancer, benign breast conditions and breast parenchyma. Ann Surg Oncol 1994;1:333-8.
51. Izumi Y, Xu L, di Tomaso E, Fukumura D, Jain RK. Tumour biology: Herceptin acts as an anti-angiogenic cocktail. Nature 2002;416:279-80.
52. Tong R. Dynamics of vascular normalization during anti-angiogenic therapy: implications for combination therapy. Harvard University-MIT Division of Health Sciences and Technology, Vol. PhD. Cambridge (MA): MIT; 2005. pp. 167.