Role of constitutive behavior and tumor-host mechanical interactions in the state of stress and growth of solid tumors

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Voutouri, Chrysovalantis ^a   Mpekris, Fotios ^a   Papageorgis, Panagiotis ^a   Odysseos, Andreani D ^a,b   Stylianopoulos, Triantafyllos ^a  

^a UNIVERSITY OF CYPRUS   (Cyprus)

^b EPOS Iasis R and D Division of Biomedical Research   (Cyprus)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; FEMALE; GROWTH RATE; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MECHANICAL STRESS; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; SOLID TUMOR; TUMOR GROWTH; TUMOR MICROENVIRONMENT; VISCOELASTICITY; YOUNG MODULUS; BIOLOGICAL MODEL; BIOMECHANICS; BREAST TUMOR; COLON TUMOR; DISEASE COURSE; MATERIALS TESTING; NONLINEAR SYSTEM; PATHOLOGY; TUMOR CELL LINE;

BIOMECHANICAL PHENOMENA; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; DISEASE PROGRESSION; HUMANS; MATERIALS TESTING; MODELS, BIOLOGICAL; NONLINEAR DYNAMICS; STRESS, MECHANICAL;

EID: 84905833834     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104717     Document Type: Article

References (48)

1. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, et al. (2004) Pathology: cancer cells compress intratumour vessels. Nature 427: 695. (Pubitemid 38294577)
2. Stylianopoulos T, Martin JD, Chauhan VP, Jain SR, Diop-Frimpong B, et al. (2012) Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors. Proceedings of the National Academy of Sciences of the United States of America 109: 15101-15108.
3. Stylianopoulos T, Martin JD, Snuderl M, Mpekris F, Jain SR, et al. (2013) Coevolution of solid stress and interstitial fluid pressure in tumors during progression: Implications for vascular collapse. Cancer research 73: 3833-3841.
4. Jain RK, Martin JD, Stylianopoulos T (2014) The role of mechanical forces in tumor growth and therapy. Annu Rev Biomed Eng 16: 321-346.
5. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, Jain RK (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15: 778-783. (Pubitemid 27329482)
6. Cheng G, Tse J, Jain RK, Munn LL (2009) Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4: e4632.
7. Kaufman LJ, Brangwynne CP, Kasza KE, Filippidi E, Gordon VD, et al. (2005) Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophys J 89: 635-650. (Pubitemid 41098315)
8. Demou ZN (2010) Gene expression profiles in 3D tumor analogs indicate compressive strain differentially enhances metastatic potential. Ann Biomed Eng 38: 3509-3520.
9. Tse JM, Cheng G, Tyrrell JA, Wilcox-Adelman SA, Boucher Y, et al. (2012) Mechanical compression drives cancer cells toward invasive phenotype. Proceedings of the National Academy of Science 109: 911-916.
10. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139: 891-906.
11. Butcher DT, Alliston T, Weaver VM (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9: 108-122.
12. Wirtz D, Konstantopoulos K, Searson PC (2011) The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nature reviews-Cancer 11: 512-522.
13. Shieh AC (2011) Biomechanical forces shape the tumor microenvironment. Annals of Biomedical Engineering 39: 1379-1389.
14. Wipff PJ, Rifkin DB, Meister JJ, Hinz B (2007) Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179: 1311-1323. (Pubitemid 350277747)
15. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363. (Pubitemid 34619269)
16. Karagiannis GS, Poutahidis T, Erdman SE, Kirsch R, Riddell RH, et al. (2012) Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Molecular cancer research : MCR 10: 1403-1418.
17. Swartz MA, Lund AW (2012) Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity. Nature Reviews Cancer 12: 210-219.
18. Chauhan VP, Martin JD, Liu H, Lacorre DA, Jain SR, et al. (2013) Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumor blood vessels. Nature Communications 4: 10.1038/ncomms.3516.
19. Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, et al. (2012) Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer cell 21: 418-429.
20. Jain RK, Stylianopoulos T (2010) Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol 7: 653-664.
21. Ambrosi D, Mollica F (2002) On the mechanics of a growing tumor. International journal of engineering science 40: 1297-1316. (Pubitemid 34715668)
22. Roose T, Netti PA, Munn LL, Boucher Y, Jain RK (2003) Solid stress generated by spheroid growth estimated using a linear poroelasticity model. Microvasc Res 66: 204-212. (Pubitemid 37373595)
23. Sarntinoranont M, Rooney F, Ferrari M (2003) Interstitial stress and fluid pressure within a growing tumor. Ann Biomed Eng 31: 327-335.
24. Byrne H, Preziosi L (2003) Modelling solid tumour growth using the theory of mixtures. Mathematical medicine and biology : a journal of the IMA 20: 341-366.
25. Ciarletta P (2013) Buckling instability in growing tumor spheroids. Phys Rev Lett 110: 158102.
26. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK (2000) Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60: 2497-2503. (Pubitemid 30262444)
27. Levental I, Levental KR, Klein EA, Assoian R, Miller RT, et al. (2010) A simple indentation device for measuring micrometer-scale tissue stiffness. J Phys Condens Matter 22: 194120.
28. Plodinec M, Loparic M, Monnier CA, Obermann EC, Zanetti-Dallenbach R, et al. (2012) The nanomechanical signature of breast cancer. Nature nanotechnology 7: 757-765.
29. Santner SJ, Dawson PJ, Tait L, Soule HD, Eliason J, et al. (2001) Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast cancer research and treatment 65: 101-110. (Pubitemid 32193613)
30. Rodriguez EK, Hoger A, McCulloch AD (1994) Stress-dependent finite growth in soft elastic tissues. J Biomech 27: 455-467. (Pubitemid 24102058)
31. Ambrosi D, Preziosi L (2009) Cell adhesion mechanisms and stress relaxation in the mechanics of tumours. Biomechanics and modeling in mechanobiology 8: 397-413.
32. Kim Y, Stolarska MA, Othmer HG (2011) The role of the microenvironment in tumor growth and invasion. Progress in biophysics and molecular biology 106: 353-379.
33. MacLaurin J, Chapman J, Jones GW, Roose T (2012) The buckling of capillaries in solid tumours. Proc R Soc A 468: 4123-4145.
34. Omens JH, Vaplon SM, Fazeli B, McCulloch AD (1998) Left ventricular geometric remodeling and residual stress in the rat heart. J Biomech Eng 120: 715-719. (Pubitemid 29004085)
35. Xu G, Bayly PV, Taber LA (2009) Residual stress in the adult mouse brain. Biomech Model Mechanobiol 8: 253-262.
36. Fung YC (1993) Biomechanics: Mechanical properties of living tissues. New York: Spinger-Verlag.
37. Taber LA (2008) Theoretical study of Beloussov's hyper-restoration hypothesis for mechanical regulation of morphogenesis. Biomech Model Mechanobiol 7: 427-441.
38. Hagendoorn J, Tong R, Fukumura D, Lin Q, Lobo J, et al. (2006) Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res 66: 3360-3364.
39. Branton MH, Kopp JB (1999) TGF-beta and fibrosis. Microbes Infect 1: 1349-1365.
40. Egeblad M, Rasch MG, Weaver VM (2010) Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 22: 697-706.
41. Roy S, Silacci P, Stergiopulos N (2005) Biomechanical properties of decellularized porcine common carotid arteries. American journal of physiologyHeart and circulatory physiology 289: H1567-1576. (Pubitemid 41368999)
42. Stylianopoulos T, Jain RK (2013) Combining two strategies to improve perfusion and drug delivery in solid tumors. Proc Natl Acad Sci U S A 110: 18632-18637.
43. Swartz MA, Fleury ME (2007) Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9: 229-256. (Pubitemid 350246657)
44. Boucher Y, Baxter LT, Jain RK (1990) Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy. Cancer Res 50: 4478-4484. (Pubitemid 20230379)
45. Nagy JA, Dvorak AM, Dvorak HF (2012) Vascular hyperpermeability, angiogenesis, and stroma generation. Cold Spring Harbor perspectives in medicine 2: a006544.
46. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nature reviewsCancer 6: 392-401.
47. Stylianopoulos T, Barocas VH (2007) Multiscale, structure-based modeling for the elastic mechanical behavior of arterial walls. J Biomech Eng 129: 611-618. (Pubitemid 47315540)
48. Sander E, Stylianopoulos T, Tranquillo R, Barocas V (2009) Image-based biomechanics of collagen-based tissue equivalents. IEEE Eng Med Biol Mag 28: 10-18.