How Changes in Extracellular Matrix Mechanics and Gene Expression Variability Might Combine to Drive Cancer Progression

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Werfel, Justin ^a   Krause, Silva ^b   Bischof, Ashley G ^a,b   Mannix, Robert J ^b   Tobin, Heather ^b   Bar Yam, Yaneer ^c   Bellin, Robert M ^d   Ingber, Donald E ^a,b,e  

^a HARVARD UNIVERSITY   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c NEW ENGLAND COMPLEX SYSTEMS INSTITUTE   (United States)

^d Department of Biology   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER TISSUE; CELL DENSITY; CELL DIVISION; CELL EXPANSION; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; COMPUTER PREDICTION; COMPUTER SIMULATION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION; GROWTH INHIBITION; MOUSE; NONHUMAN; PHENOTYPE; TUMOR MICROENVIRONMENT;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MODELS, BIOLOGICAL; NEOPLASM STAGING; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84884896705     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076122     Document Type: Article

References (60)

1. Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier JP, et al. (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98: 137-146.
2. DeCosse JJ, Gossens C, Kuzma JF, Unsworth BR, (1975) Embryonic inductive tissues that cause histologic differentiation of murine mammary carcinoma in vitro. J Natl Cancer Inst 54: 913-922.
3. DeCosse JJ, Gossens CL, Kuzma JF, Unsworth BR, (1973) Breast cancer: induction of differentiation by embryonic tissue. Science 181: 1057-1058.
4. Maffini MV, Calabro JM, Soto AM, Sonnenschein C, (2005) Stromal regulation of neoplastic development: age-dependent normalization of neoplastic mammary cells by mammary stroma. Am J Pathol 167: 1405-1410.
5. Ingber DE, (2008) Can cancer be reversed by engineering the tumor microenvironment? Semin Cancer Biol 18: 356-364.
6. Mintz B, Illmensee K, (1975) Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci U S A 72: 3585-3589.
7. Watanabe TK, Hansen LJ, Reddy NK, Kanwar YS, Reddy JK, (1984) Differentiation of pancreatic acinar carcinoma cells cultured on rat testicular seminiferous tubular basement membranes. Cancer Res 44: 5361-5368.
8. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, et al. (2002) beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2: 205-216.
9. 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.
10. Sternlicht MD, Bissell MJ, Werb Z, (2000) The matrix metalloproteinase stromelysin-1 acts as a natural mammary tumor promoter. Oncogene 19: 1102-1113.
11. Venugopalan G, Fletcher DA (2012) Breast cancer cells growing in 3D-matrix revert to normal. American Society for Cell Biology. San Francisco, CA.
12. Folkman J, Moscona A, (1978) Role of cell shape in growth control. Nature 273: 345-349.
13. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE, (1997) Geometric control of cell life and death. Science 276: 1425-1428.
14. Huang S, Ingber DE, (2000) Shape-dependent control of cell growth, differentiation, and apoptosis: switching between attractors in cell regulatory networks. Exp Cell Res 261: 91-103.
15. Mammoto A, Ingber DE, (2009) Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol 21: 864-870.
16. Discher DE, Janmey P, Wang YL, (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143.
17. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
18. Moore KA, Polte T, Huang S, Shi B, Alsberg E, et al. (2005) Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232: 268-281.
19. Ingber DE, Madri JA, Jamieson JD, (1981) Role of basal lamina in neoplastic disorganization of tissue architecture. Proc Natl Acad Sci U S A 78: 3901-3905.
20. Ingber DE, Madri JA, Jamieson JD, (1985) Neoplastic disorganization of pancreatic epithelial cell-cell relations. Role of basement membrane. Am J Pathol 121: 248-260.
21. Hoffmann M, Chang HH, Huang S, Ingber DE, Loeffler M, et al. (2008) Noise-driven stem cell and progenitor population dynamics. PLoS One 3: e2922.
22. Huang S, (2012) Tumor progression: chance and necessity in Darwinian and Lamarckian somatic (mutationless) evolution. Prog Biophys Mol Biol 110: 69-86.
23. Kashiwagi A, Urabe I, Kaneko K, Yomo T, (2006) Adaptive response of a gene network to environmental changes by fitness-induced attractor selection. PLoS One 1: e49.
24. Kalmar T, Lim C, Hayward P, Munoz-Descalzo S, Nichols J, et al. (2009) Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol 7: e1000149.
25. Brock A, Chang H, Huang S, (2009) Non-genetic heterogeneity-a mutation-independent driving force for the somatic evolution of tumours. Nat Rev Genet 10: 336-342.
26. Capp JP, (2005) Stochastic gene expression, disruption of tissue averaging effects and cancer as a disease of development. Bioessays 27: 1277-1285.
27. Huang S, Ingber DE, (2006) A non-genetic basis for cancer progression and metastasis: self-organizing attractors in cell regulatory networks. Breast Dis 26: 27-54.
28. Laforge B, Guez D, Martinez M, Kupiec JJ, (2005) Modeling embryogenesis and cancer: an approach based on an equilibrium between the autostabilization of stochastic gene expression and the interdependence of cells for proliferation. Prog Biophys Mol Biol 89: 93-120.
29. Wittelsberger SC, Kleene K, Penman S, (1981) Progressive loss of shape-responsive metabolic controls in cells with increasingly transformed phenotype. Cell 24: 859-866.
30. Bissell MJ, Hall HG, Parry G, (1982) How does the extracellular matrix direct gene expression? J Theor Biol 99: 31-68.
31. Bissell MJ, Hines WC, (2011) Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 17: 320-329.
32. Ingber DE, (2002) Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation. Differentiation 70: 547-560.
33. Bissell MJ, Weaver VM, Lelievre SA, Wang F, Petersen OW, et al. (1999) Tissue structure, nuclear organization, and gene expression in normal and malignant breast. Cancer Res 59: 1757-1763s; discussion 1763s-1764s.
34. Ingber DEaJ, J.D. (1985) Cells as tensegrity structures: architectural regulation of histodifferentiation by physical forces transduced over basement membrane. In: Andersson LC, Gahmberg, C.G and Ekblom P., editor. Gene expression during normal and malignant differentiation: Academic Press Orlando, FL. 13-32.
35. Pienta KJ, Partin AW, Coffey DS, (1989) Cancer as a disease of DNA organization and dynamic cell structure. Cancer Res 49: 2525-2532.
36. Galle J, Loeffler M, Drasdo D, (2005) Modeling the effect of deregulated proliferation and apoptosis on the growth dynamics of epithelial cell populations in vitro. Biophys J 88: 62-75.
37. Jeon J, Quaranta V, Cummings PT, (2010) An off-lattice hybrid discrete-continuum model of tumor growth and invasion. Biophys J 98: 37-47.
38. Quaranta V, Rejniak KA, Gerlee P, Anderson AR, (2008) Invasion emerges from cancer cell adaptation to competitive microenvironments: quantitative predictions from multiscale mathematical models. Semin Cancer Biol 18: 338-348.
39. Shirinifard A, Gens JS, Zaitlen BL, Poplawski NJ, Swat M, et al. (2009) 3D multi-cell simulation of tumor growth and angiogenesis. PLoS One 4: e7190.
40. Amyot F, Small A, Boukari H, Camphausen K, Gandjbakhche A, (2009) Topology of the heterogeneous nature of the extracellular matrix on stochastic modeling of tumor-induced angiogenesis. Microvasc Res 77: 87-95.
41. Cai Y, Gulnar K, Zhang H, Jinfeng C, Shixiong X, et al. (2009) Numerical simulation of tumor-induced angiogenesis influenced by the extra-cellular matric mechanical environment. Acta Mechanica Sinica 25: 889-895.
42. Cristini V, Lowengrub J, Nie Q, (2003) Nonlinear simulation of tumor growth. J Math Biol 46: 191-224.
43. Enderling H, Chaplain MA, Anderson AR, Vaidya JS, (2007) A mathematical model of breast cancer development, local treatment and recurrence. J Theor Biol 246: 245-259.
44. Macklin P, Lowengrub J, (2007) Nonlinear simulation of the effect of microenvironment on tumor growth. J Theor Biol 245: 677-704.
45. Zheng X, Wise SM, Cristini V, (2005) Nonlinear simulation of tumor necrosis, neo-vascularization and tissue invasion via an adaptive finite-element/level-set method. Bull Math Biol 67: 211-259.
46. Sanga S, Frieboes HB, Zheng X, Gatenby R, Bearer EL, et al. (2007) Predictive oncology: a review of multidisciplinary, multiscale in silico modeling linking phenotype, morphology and growth. Neuroimage 37Suppl 1: S120-134.
47. Polte TR, Eichler GS, Wang N, Ingber DE, (2004) Extracellular matrix controls myosin light chain phosphorylation and cell contractility through modulation of cell shape and cytoskeletal prestress. Am J Physiol Cell Physiol 286: C518-528.
48. Numaguchi Y, Huang S, Polte TR, Eichler GS, Wang N, et al. (2003) Caldesmon-dependent switching between capillary endothelial cell growth and apoptosis through modulation of cell shape and contractility. Angiogenesis 6: 55-64.
49. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
50. Gilmore AP, (2005) Anoikis. Cell Death Differ 12Suppl 2: 1473-1477.
51. Green JE, Shibata MA, Yoshidome K, Liu ML, Jorcyk C, et al. (2000) The C3(1)/SV40 T-antigen transgenic mouse model of mammary cancer: ductal epithelial cell targeting with multistage progression to carcinoma. Oncogene 19: 1020-1027.
52. Maroulakou IG, Anver M, Garrett L, Green JE, (1994) Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci U S A 91: 11236-11240.
53. McCullough KD, Coleman WB, Ricketts SL, Wilson JW, Smith GJ, et al. (1998) Plasticity of the neoplastic phenotype in vivo is regulated by epigenetic factors. Proc Natl Acad Sci U S A 95: 15333-15338.
54. Bissell MJ, Radisky D, (2001) Putting tumours in context. Nat Rev Cancer 1: 46-54.
55. Folkman J, (2006) Angiogenesis. Annu Rev Med 57: 1-18.
56. Ahangar R, Iqbal K. Biodynamic Modeling and Simulation of Multi-Stage Carcinogenesis; 2004; San Francisco, CA.
57. Crawley WA, Dellon AL, Ryan JJ, (1978) Does host response determine the prognosis in scar carcinoma? Plast Reconstr Surg 62: 407-414.
58. Gowing NF, (1961) The relationship of trauma to tumour formation. J Forensic Med 8: 116-121.
59. Haddow A, (1974) Addendum to "molecular repair, wound healing, and carcinogenesis: tumor production a possible overhealing"? Adv Cancer Res 20: 343-366.
60. Keenan KP, Saffiotti U, Stinson SF, Riggs CW, McDowell EM, (1989) Multifactorial hamster respiratory carcinogenesis with interdependent effects of cannula-induced mucosal wounding, saline, ferric oxide, benzo[a]pyrene and N-methyl-N-nitrosourea. Cancer Res 49: 1528-1540.