Solid stress inhibits the growth of multicellular tumor spheroids

Nature Biotechnology

Volumn 15, Issue 8, 1997, Pages 778-783

  Helmlinger, Gabriel ^a   Netti, Paolo A ^a   Lichtenbeld, Hera C ^a   Melder, Robert J ^a   Jain, Rakesh K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Apoptosis; Proliferation; Tumor growth

Indexed keywords

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DENSITY; CELL SHAPE; CELL VOLUME; GROWTH INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRESS; TUMOR BLOOD FLOW; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; APOPTOSIS; CELL COUNT; CELL DIVISION; HUMANS; MICE; MODELS, BIOLOGICAL; NEOPLASMS, EXPERIMENTAL; STRESS, MECHANICAL; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0030744722     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt0897-778     Document Type: Article

References (42)

1. Wolff, J. 1870. Über die innere Architektur der Knochen urtd ihre Bedeutung für die Frage vom Knochenwachsum. Virchow. Arch. 50:389-453.
2. Fung, YC. 1990. Biomechanical aspects of growth and tissue engineering, pp. 499-546 in Biomechanics, motion, flow, stress, and growth. Fung, YC. (ed). Springer-Verlag, New York.
3. Fung, YC. and Liu, S.Q. 1989. Change of residual strain in arteries due to hypertrophy caused by aortic constriction. Circ. Res. 65:1340-1349.
4. Burton, K. and Taylor, D.L 1997. Traction forces of cytokinesis measured with optically modified elastic substrata. Nature 385:450-454.
5. Fung, YC. 1991. What are the residual stresses doing in our blood vessels? Ann. Biomed. Eng. 19:237-249.
6. Omens, J.H. and Fung, YC. 1990. Residual strain in rat left ventricle. Circ. Res. 66:37-45.
7. Han, H.C. and Fung, YC. 1991. Residual strain in porcine and canine trachea. J. Biomech. Eng. 24:307-315.
8. Vaage, J. 1992. Fibrosis in immune control of mammary-tumor growth. Int. J. Cancer 51:325-328.
9. Gartner, M.F.R.M., Feams, C, Lynette Wilson, E, Campbell, J.A.H. and Dowdle, E.B. 1992. Unusual growth characteristics of human melanoma xenografts in the nude mouse: a model for desmoplasia, dormancy and progression. Br. J. Cancer 65:487-490.
10. Eaves, G. 1973. The invasive growth of malignant tumours as a purely mechanical process. J. Pathol. 109:233-237.
11. Young, J.S. 1959. The invasive growth of malignant tumours: an experimental interpretation based on elastic-jelly models. J. Path. Bact. 77:321-326.
12. Falk, R. 1978. Patterns of vasculature in two pairs of related fibrosarcomas in the rat and their relation to tumour responses to single large doses of radiation. Eur. J. Cancer 14:237-250.
13. Falk, R 1980. The vascular pattern of the spontaneous C3H mouse mammary carcinoma and its significance in radiation response and in hyperthermia Eur. J. Cancer 16:203-217.
14. Tozer, G.M., Lewis, S., Michalowski, A., and Aber, V. 1990. The relationship between regional variations in blood flow and histology in a transplanted rat fibrosarcoma. Br. J. Cancer 61:250-257.
15. Li, L., Price, J.E., Fan, D., Zhang, R.D., Bucana, CD., Fidler, I.J., et al. 1989. Correlation of growth capacity of human tumor cells in hard agarose with their in vivo proliferative capacity at specific metastatic sites. J. Natl Cancer Inst. 81:1406-1412.
16. Jain, R.K. 1988. Determinants of tumor blood flow: a review. Cancer Res. 48:2641-58.
17. Knight, M.M., Lee, DA, and Bader, D.L. 1996. Distribution of chondrocyte deformation in compressed agarose gel using confocal microscopy. Cell. Eng. 1:97-102.
18. Sutherland, R.M. 1988. Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240:177-184.
19. Freyer, J.P. 1988. Role of necrosis in regulating the growth saturation of multicellular spheroids. Cancer Res. 48:2432-2439.
20. Gompertz, B. 1825. On the nature of the function expressive of the law of human mortality, and on a new method of determining the value of life contingencies. Phil. Trans. R. Soc. 115:513-585.
21. Gyllenberg, M. and Webb, G.F. 1989. Quiescence as an explanation of Gompertzian tumor growth. Growth Dev. Aging 53:25-33.
22. Nicolson, G.L, Lembo, T.M., and Welch, D.R. 1988. Growth of rat mammary adenocarcinoma cells in semisolid clonogenic medium not correlated with spontaneous metastatic behavior: heterogeneity in the metastatic, antigenic, enzymatic, and drug sensitivity properties of cells from different sized colonies. Cancer Res. 48:399-404.
23. Johnson, E.M., Berk, D.A., Jain, R.K., and Deen, W.M. 1996. Hindered diffusion in agarose gels: test of effective medium model. Biophys. J. 70:1017-1026.
24. Raff, M.C. 1992. Social controls on cell survival and cell death. Nature 356:397-400.
25. Bates, R.C., Buret, A., van Helden, D.F., Horton, MA, and Bums, G.F. 1994. Apoptosis induced by inhibition of intercellular contact. J. Cell Biol. 125:403-415.
26. Freyer, J.P. 1994. Rates of oxygen consumption for proliferating and quiescent cells isolated from multicellular tumor spheroids. Adv. Exp. Med. Biol. 345:335-342.
27. Olive, P.L. and Durand, R.E. 1994. Drugs and radiation resistance in spheroids: cell contact and kinetics. Cancer Metastasis Rev. 13:121-138.
28. Kobayashi, H., Man, S., Graham, C.H., Kapitain, S.J., Teicher, B.A., Kerbel, R.S., et al. 1993. Acquired multicellular-mediated resistance to alkylating agents in cancer. Proc. Natl. Acad. Sci. USA 90:3294-3298.
29. Kerbel, R.S., Rak, J.W., Kobayashi, H, Man, S., St. Croix, B., Graham, C.H., et al. 1994. Multicellular resistance: a new paradigm to explain aspects of acquired drug resistance of solid tumors. Cold Spring Harbor Symp. Quant. Biol. (Motec. Sen. Cancer) 59:661-672.
30. St. Croix, B., Rak, J.W., Kapitain, S.J., Sheehan, C, Graham, C.H., Kerbel, R.S., et al. 1996. Reversal by hyaluronidase of adhesion-dependent multicellular drug resistance in mammary carcinoma cells. J. Natl. Cancer Inst. 88:1285-1296.
31. Rak, J.W. and Kerbel, R.S. 1993. Growth advantage (“clonal dominance”) of metastatically competent tumor cell variants expressed under selective two- or three-dimensional tissue culture conditions. In Vitro Cell. Dev. Biol. 29A:742-748.
32. Holmgren, L., O’Reilly, M.S., and Folkman, J. 1995. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Med. 1:149-153.
33. Freyer, J.P. and Schor, P.L. 1989. Regrowth kinetics of cells from different regions of multicellular spheroids of four cell lines. J. Cell. Physiol. 138:384-392.
34. lozzo, R.V. 1995.Tumor stroma as a regulator of neoplastic behavior. Agonistic and antagonistic elements embedded in the same connective tissue. Lab. Invest 73:157-160.
35. Stetler-Stevenson, W.G. 1996. Dynamics of matrix turnover during pathologic remodeling of the extracellular matrix. Am. J. Pathol. 148:1345-1350.
36. Boucher, Y and Jain, R.K. 1992, Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res. 52:5110-4.
37. Boucher, Y, Baxter, L.T., and Jain, R.K. 1990. Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy. Cancer Res. 50:4478-84.
38. Boucher, Y, Leunig, M., and Jain, R.K. 1996. Tumor angiogenesis and interstitial hypertension. Cancer Res. 56:4264-4266.
39. MacPhee, P.J. and Michel, C.C. 1995. Subatmospheric closing pressures in individual microvessels of rats and frogs. J. Physiol. 484:183-187.
40. Netti, P.A., Roberge, S., Boucher, Y, Baxter, L.T., and Jain, R.K. 1996. Effect of transvascular fluid exchange on pressure - flow relationship in tumors: a proposed mechanism for tumor blood flow heterogeneity. Microvasc. Res. 52:27-46.
41. Tanigawa, N., Kanazawa, T, Satomura, K., Kikasa, Y, Hashida, M., Muranishi, S., et al. 1981. Experimental study on lymphatic vascular changes in the development of cancer. Lymphology 14:149-154.
42. Iscove, N.N. and Schreier, M.H. 1979. Clonal growth of cells in semisolid or viscous medium, pp. 379-385 in Immunological methods. Academic Press.