Coevolution of solid stress and interstitial fluid pressure in tumors during progression: Implications for vascular collapse

Cancer Research

Volumn 73, Issue 13, 2013, Pages 3833-3841

  Stylianopoulos, Triantafyllos ^a   Martin, John D ^b,c   Snuderl, Matija ^c,d   Mpekris, Fotios ^a   Jain, Saloni R ^b,c   Jain, Rakesh K ^c  

^a UNIVERSITY OF CYPRUS   (Cyprus)

^b Massachusetts Institute of Technology Cambridge   (United Kingdom)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER CELL; CELL PROLIFERATION; COEVOLUTION; COLLAPSE; CONTROLLED STUDY; GROWTH RATE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IN VIVO STUDY; MALE; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRESS; TISSUE PRESSURE; TUMOR GROWTH; TUMOR VOLUME; VASCULAR FRAGILITY;

ALGORITHMS; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; EXTRACELLULAR FLUID; HUMANS; HYDROSTATIC PRESSURE; MALE; MICE; MICE, SCID; MODELS, BIOLOGICAL; NEOPLASM TRANSPLANTATION; NEOPLASMS; STRESS, PHYSIOLOGICAL; TUMOR BURDEN;

EID: 84880079914     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4521     Document Type: Article

References (32)

1. Skalak R, Zargaryan S, Jain RK, Netti PA, Hoger A. Compatibility and the genesis of residual stress by volumetric growth. J Math Biol 1996;34: 889-914.
2. Stylianopoulos T, Martin JD, Chauhan VP, Jain SR, Diop-Frimpong B, Bardeesy N, et al. Causes, consequences, and remedies for growthinduced solid stress in murine and human tumors. Proc Natl Acad Sci U S A 2012;109: 15101-8.
3. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, Jain RK. Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 1997;15: 778-83.
4. Koike C, McKee TD, Pluen A, Ramanujan S, Burton K, Munn LL, et al. Solid stress facilitates spheroid formation: potential involvement of hyaluronan. Br J Cancer 2002;86: 947-53.
5. Cheng G, Tse J, Jain RK, Munn LL. Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 2009;4: e4632.
6. Tse JM, Cheng G, Tyrrell JA, Wilcox-Adelman SA, Boucher Y, Jain RK, et al. Mechanical compression drives cancer cells toward invasive phenotype. PNAS 2012;109: 911-6.
7. Steel GG. Growth kinetics of tumours: cell population kinetics in relation to the growth and treatment of cancer. New York, NY: Oxford University Press, 1978.
8. Roose T, Netti PA, Munn LL, Boucher Y, Jain RK. Solid stress generated by spheroid growth estimated using a linear poroelasticity model. Microvasc Res 2003;66: 204-12.
9. Bardeesy N, Aguirre AJ, Chu GC, Cheng KH, Lopez LV, Hezel AF, et al. Both p16(Ink4a) and the p19(arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc Natl Acad Sci U S A 2006;103: 5947-52.
10. Hagendoorn J, Tong R, Fukumura D, Lin Q, Lobo J, Padera TP, et al. Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res 2006;66: 3360-4.
11. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000;60: 2497-503.
12. Fung YC. Biomechanics: mechanical properties of living tissues. New York, NY: Spinger-Verlag; 1993.
13. Sarntinoranont M, Rooney F, Ferrari M. Interstitial stress and fluid pressure within a growing tumor. Ann Biomed Eng 2003;31: 327-35.
14. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK. Pathology: cancer cells compress intratumour vessels. Nature 2004; 427: 695.
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. Provenzano PP, Hingorani SR. Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer. Br J Cancer 2013;108: 1-8.
17. Von Hoff DD, Ervin TJ, Arena FP, Chiorean EG, Infante JR, Moore MJ, et al. Randomized phase III study of weekly nab-paclitaxel plus gemcitabine versus gemcitabine alone in patients with metastatic adenocarcinoma of the pancreas (MPACT). J Clin Oncol 2012; 30 (34 suppl); abstr LBA148.
18. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR. Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 2012;21: 418-29.
19. Chauhan VP, Stylianopoulos T, Martin JD, Popovic Z, Chen O, Kamoun WS, et al. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat Nanotechnol 2012;7: 383-8.
20. Baxter LT, Jain RK. Transport of fluid and macromolecules in tumors. II. Role of heterogeneous perfusion and lymphatics. Microvasc Res 1990; 40: 246-63.
21. 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.
22. Jones AF, Byrne HM, Gibson JS, Dold JW. A mathematical model of the stress induced during avascular tumour growth. J Math Biol 2000;40: 473-99.
23. Ambrosi D, Preziosi L. Cell adhesion mechanisms and stress relaxation in the mechanics of tumours. Biomech Model Mechanobiol 2009;8: 397-413.
24. Macklin P, McDougall S, Anderson AR, Chaplain MA, Cristini V, Lowengrub J. Multiscale modelling and nonlinear simulation of vascular tumour growth. J Math Biol 2009;58: 765-98.
25. Jain RK. Determinants of tumor blood flow: a review. Cancer Res 1988;48: 2641-58.
26. 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 (24 Pt 1): 7022-32.
27. Boucher Y, Baxter LT, Jain RK. Interstitial pressure gradients in tissueisolated and subcutaneous tumors: implications for therapy. Cancer Res 1990;50: 4478-84.
28. Jain RK, Tong RT, Munn LL. Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res 2007;67: 2729-35.
29. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307: 58-62.
30. Jain RK. Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers. J Clin Oncol 2013;31: 2205-18.
31. Ambrosi D, Mollica F. On the mechanics of a growing tumor. Int J Eng Sci 2002;40: 1297-316.
32. MacLaurin J, Chapman J, Jones GW, Roose T. The buckling of capillaries in solid tumours. Proc R Soc A 2012;468: 4123-45. Oncology