A Hybrid Model of Tumor-Stromal Interactions in Breast Cancer

Bulletin of Mathematical Biology

Volumn 75, Issue 8, 2013, Pages 1304-1350

  Kim, Yangjin ^a   Othmer, Hans G ^b  

^a Konkuk University   (South Korea)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Microenvironment invasion

Indexed keywords

EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BIOLOGICAL MODEL; BREAST TUMOR; FEMALE; HUMAN; INTRADUCTAL CARCINOMA; MATHEMATICAL PHENOMENA; PAGET NIPPLE DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR INVASION; TUMOR MICROENVIRONMENT;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; MATHEMATICAL CONCEPTS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT;

EID: 84881377835     PISSN: 00928240     EISSN: 15229602     Source Type: Journal    
DOI: 10.1007/s11538-012-9787-0     Document Type: Article

References (71)

1. Abdollah, S., Macias-Silva, M., Tsukazaki, T., Hayashi, H., Attisano, L., & Wrana, J. L. (1997). TbetaRI phosphorylation of smad2 on ser465 and ser467 is required for smad2-smad4 complex formation and signaling. J. Biol. Chem., 272(44), 27678-27685.
2. Adams, S., Miller, G. T., Jesson, M. I., Watanabe, T., Jones, B., & Wallner, B. P. (2004). PT-100, a small molecule dipeptidyl peptidase inhibitor, has potent antitumor effects and augments antibody-mediated cytotoxicity via a novel immune mechanism. Cancer Res., 64(15), 5471-5480.
3. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., & Saltiel, A. R. (1995). PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase in vitro and in vivo. J. Biol. Chem., 270(46), 27489-27494.
4. Alexander, S., & Friedl, P. (2012). Cancer invasion and resistance: interconnected processes of disease progression and therapy failure. Trends Mol. Med., 18(1), 13-26.
5. Almholt, K., Green, K., Juncker-Jensen, A., Nielsen, B., Lund, L., & Romer, J. (2007). Extracellular proteolysis in transgenic mouse models of breast cancer. J. Mammary Gland Biol. Neoplasia, 12(1), 83-97.
6. Annabi, B., Bouzeghrane, M., Currie, J. C., Hawkins, R., Dulude, H., Daigneault, L., Ruiz, M., Wisniewski, J., Garde, S., Rabbani, S. A., Panchal, C., Wu, J. J., & Beliveau, R. (2005). A PSP94-derived peptide PCK3145 inhibits MMP-9 secretion and triggers CD44 cell surface shedding: implication in tumor metastasis. Clin. Exp. Metastasis, 22(5), 429-439.
7. Basbaum, C. B., & Werb, Z. (1996). Focalized proteolysis: a spatial and temporal regulation of extracellular matrix degradation at the cell surface. Curr. Opin. Cell Biol., 8, 731-738.
8. Beacham, D. A., & Cukierman, E. (2005). Stromagenesis: the changing face of fibroblastic microenvironments during tumor progression. In Seminars in cancer biology. (Vol. 15, pp. 329-341). Amsterdam: Elsevier.
9. Brown, D. R. (1999). Dependence of neurones on astrocytes in a coculture system renders neurones sensitive to transforming growth factor beta1-induced glutamate toxicity. J. Neurochem., 72(3), 943-953.
10. Burrai, G. P., Mohammed, S. I., Miller, M. A., Marras, V., Pirino, S., Addis, M. F., Uzzau, S., & Antuofermo, E. (2010). Spontaneous feline mammary intraepithelial lesions as a model for human estrogen receptor- and progesterone receptor-negative breast lesions. BMC Cancer, 10, 156.
11. Chen, S. T., Pan, T. L., Juan, H. F., Chen, T. Y., Lin, Y. S., & Huang, C. M. (2008). Breast tumor microenvironment: proteomics highlights the treatments targeting secretome. J. Proteome Res., 7, 1379-1387.
12. Cheng, J. D., & Weiner, L. M. (2003). Tumors and their microenvironments: tilling the soil commentary re: A. M. Scott et al., A phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin. Cancer Res., 9(5), 1590-1595.
13. Cheng, G., Tse, J., Jain, R. K., & Minn, L. L. (2009). Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing aopotosis in cancer cells. PLoS ONE, 4, e4632.
14. Chivukula, M., Bhargava, R., Tseng, G., & Dabbs, D. J. (2009). Clinicopathologic implications of flat epithelial atypia in core needle biopsy specimens of the breast. Am. J. Clin. Pathol., 131, 802-808.
15. Chung, S. W., Miles, F. L., Sikes, R. A., Cooper, C. R., Farach-Carson, M. C., & Ogunnaike, B. A. (2009). Quantitative modeling and analysis of the transforming growth factor beta signaling pathway. Biophys. J., 96(5), 1733-1750.
16. Dallon, J. C., & Othmer, H. G. (1997). A discrete cell model with adaptive signalling for aggregation of Dictyostelium discoideum. Philos. Trans. R. Soc. Lond. B, 352, 391-417.
17. Dallon, J. C., & Othmer, H. G. (2004). How cellular movement determines the collective force generated by the Dictyostelium discoideum slug. J. Theor. Biol., 231, 203-222.
18. Danielsen, T., & Rofstad, E. K. (1998). VEGF, bFGF and EGF in the angiogenesis of human melanoma xenografts. Int. J. Cancer, 76(6), 836-841.
19. Davis, R. J. (1993). The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem., 268(20), 14553-14556.
20. Friedl, P., & Alexander, S. (2011). Cancer invasion and the microenvironment: plasticity and reciprocity. Cell, 147(5), 992-1009.
21. Geho, D. H., Bandle, R. W., Clair, T., & Liotta, L. A. (2005). Physiological mechanisms of tumor-cell invasion and migration. Physiology (Bethesda), 20, 194-200.
22. Hanamura, N., Yoshida, T., Matsumoto, E., Kawarada, Y., & Sakakura, T. (1997). Expression of fibronectin and tenascin-c mrna by myofibroblasts, vascular cells and epithelial cells in human colon adenomas and carcinomas. Int. J. Cancer, 73(1), 10-15.
23. Helmlinger, G., Netti, P. A., Lichtenbeld, H. C., Melder, R. J., & Jain, R. K. (1997). Solid stress inhibits the growth of multicellular tumor spheroids. Nat. Biotechnol., 15(8), 778-783.
24. Hendriks, B. S., Orr, G., Wells, A., Wiley, H. S., & Lauffenburger, D. A. (2005). Parsing ERK activation reveals quantitatively equivalent contributions from epidermal growth factor receptor and HER2 in human mammary epithelial cells. J. Biol. Chem., 280(7), 6157-6169.
25. 5 mesoscopic and macroscopic models for mesenchymal motion. J. Math. Biol., 53, 585-616.
26. Hillen, T., Hinow, P., & Wang, Z. A. (2010). Mathematical analysis of a kinetic model for cell movement in network tissues. Discrete Contin. Dyn. Syst., Ser. B, 14(3), 1055-1080.
27. Hinshelwood, R. A., Huschtscha, L. I., Melki, J., Stirzaker, C., Abdipranoto, A., Vissel, B., Ravasi, T., Wells, C. A., Hume, D. A., Reddel, R. R., & Clark, S. J. (2007). Concordant epigenetic silencing of transforming growth factor-signaling pathway genes occurs early in breast carcinogenesis. Cancer Res., 67(24), 11517.
28. Ilina, O., Bakker, G. J., Vasaturo, A., Hofman, R. M., & Friedl, P. (2011). Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion. Phys Biol., 8(1), 015010.
29. Kaufman, L. J., Brangwynne, C. P., Kasza, K. E., Filippidi, E., Gordon, V. D., Deisboeck, T. S., & Weitz, D. A. (2005). Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophys. J. BioFAST, 89, 635-650.
30. Kim, Y., & Friedman, A. (2010). Interaction of tumor with its microenvironment: a mathematical model. Bull. Math. Biol., 72(5), 1029-1068.
31. Kim, Y., Stolarska, M., & Othmer, H. G. (2007). A hybrid model for tumor spheroid growth in vitro I: theoretical development and early results. Math. Models Methods Appl. Sci., 17, 1773-1798.
32. Kim, Y., Lawler, S., Nowicki, M., Chiocca, E., & Friedman, A. (2009). A mathematical model of brain tumor: pattern formation of glioma cells outside the tumor spheroid core. J. Theor. Biol., 260, 359-371.
33. Kim, Y., Stolarska, M. A., & Othmer, H. G. (2011). The role of the microenvironment in tumor growth and invasion. Prog. Biophys. Mol. Biol., 106, 353-379.
34. Kloft, C., Graefe, E., Tanswell, P., Scott, A., Hofheinz, R., Amelsberg, A., & Karlsson, M. (2004). Population pharmacokinetics of sibrotuzumab, a novel therapeutic monoclonal antibody, in cancer patients. Invest. New Drugs, 22(1), 39-52.
35. Koka, S., Vance, J. B., & Maze, G. I. (1995). Bone growth factors: potential for use as an osseointegration enhancement technique (OET). J. West. Soc. Periodontol., Periodontal Abstr., 43(3), 97-104.
36. Kretzschmar, M., Doody, J., & Massagué, J. (1997). Opposing BMP and EGF signalling pathways converge on the TGFb family mediator smad1. Nature, 389(6651), 618-622.
37. Kretzschmar, M., Doody, J., Timokhina, I., & Massagué, J. (1999). A mechanism of repression of TGFbeta/ smad signaling by oncogenic ras. Genes Dev., 13(7), 804-816.
38. Krouskop, T. A., Wheeler, T. M., Kallel, F., Garra, B. S., & Hall, T. (1998). Elastic moduli of breast and prostate tissues under compression. Ultrason. Imag., 20(4), 260-274.
39. Kudlow, J. E., Cheung, C. Y., & Bjorge, J. D. (1986). Epidermal growth factor stimulates the synthesis of its own receptor in a human breast cancer cell line. J. Biol. Chem., 261(9), 4134-4138.
40. Kunz-Schughart, L. A., Wenninger, S., Neumeier, T., Seidl, P., & Knuechel, R. (2003). Three-dimensional tissue structure affects sensitivity of fibroblasts to TGF-beta 1. Am. J. Physiol., Cell Physiol., 284(1), C209-C219.
41. Liu, X., Sun, Y., Constantinescu, S. N., Karam, E., Weinberg, R. A., & Lodish, H. F. (1997). Transforming growth factor beta-induced phosphorylation of smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc. Natl. Acad. Sci. USA, 94(20), 10669-10674.
42. Mantzaris, N., Webb, S., & Othmer, H. G. (2004). Mathematical modeling of tumor-induced angiogenesis. J. Math. Biol., 49, 111-187.
43. Marino, S., Hogue, I. B., Ray, C. J., & Kirschner, D. E. (2008). A methodology for performing global uncertainty and sensitivity analysis in systems biology. J. Theor. Biol., 254(1), 178-196.
44. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell, 80(2), 179-185.
45. Massagué, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem., 67(1), 753.
46. Massagué, J. (2008). TGF [beta] in cancer. Cell, 134(2), 215-230.
47. Mercapide, J., Cicco, R., Castresana, J. S., & Klein-Szanto, A. J. (2003). Stromelysin-1/matrix metalloproteinase-3 (MMP-3) expression accounts for invasive properties of human astrocytoma cell lines. Int. J. Cancer, 106(5), 676-682.
48. Palsson, E., & Othmer, H. G. (2000). A model for individual and collective cell movement in dictyostelium discoideum. Proc. Natl. Acad. Sci., 97, 11448-11453.
49. Paszek, M. J., & Weaver, V. M. (2004). The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia, 9(4), 325-342. Review.
50. Preziosi, L., & Vitale, G. (2011). A multiphase model of tumour and tissue growth including cell adhesion and plastic re-organisation. Math. Models Methods Appl. Sci., 21, 1901-1932.
51. Provenzano, P., Inman, D., Eliceiri, K., & Keely, P. (2009). Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene, 28, 4326-4343.
52. Renkawitz, J., & Sixt, M. (2010). Mechanisms of force generation and force transmission during interstitial leukocyte migration. EMBO Rep., 11(10), 744-750.
53. Renkawitz, J., Schumann, K., Weber, M., Lämmermann, T., Pflicke, H., Piel, M., Polleux, J., Spatz, J. P., & Sixt, M. (2009). Adaptive force transmission in amoeboid cell migration. Nat. Cell Biol., 11(12), 1438-1443.
54. Saffarian, S., Collier, I. E., Marmer, B. L., Elson, E. L., & Goldberg, G. (2004). Interstitial collagenase is a Brownian ratchet driven by proteolysis of collagen. Science, 306(5693), 108-111.
55. Samoszuk, M., Tan, J., & Chorn, G. (2005). Clonogenic growth of human breast cancer cells co-cultured in direct contact with serum-activated fibroblasts. Breast Cancer Res., 7, R274-R283.
56. Santos, S. D. M., Verveer, P. J., & Bastiaens, P. I. H. (2007). Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol., 9(3), 324-330.
57. Sappino, A. P., Skalli, O., Jackson, B., Schurch, W., & Gabbiani, G. (1988). Smooth-muscle differentiation in stromal cells of malignant and non-malignant breast tissues. Int. J. Cancer, 41(5), 707-712.
58. Schmierer, B., Tournier, A. L., Bates, P. A., & Hill, C. S. (2008). Mathematical modeling identifies smad nucleocytoplasmic shuttling as a dynamic signal-interpreting system. Proc. Natl. Acad. Sci. USA, 105(18), 6608-6613.
59. Sherratt, J. A., & Murray, J. D. (1990). Models of epidermal wound healing. Proc. R. Soc. Lond. B, 241, 29-36.
60. Shi, Y., & Massagué, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell, 113(6), 685-700.
61. Souchelnytskyi, S., Tamaki, K., Engstrom, U., Wernstedt, C., ten Dijke, P., & Heldin, C. H. (1997). Phosphorylation of ser465 and ser467 in the C terminus of smad2 mediates interaction with smad4 and is required for transforming growth factor-beta signaling. J. Biol. Chem., 272(44), 28107-28115.
62. Stein, A. M., Demuth, T., Mobley, D., Berens, M., & Sander, L. M. (2007). A mathematical model of glioblastoma tumor spheroid invasion in a three-dimensional in vitro experiment. Biophys. J., 92(1), 356-365.
63. Stein, A. M., Vader, D. A., Weitz, D. A., & Sander, L. M. (2011). The micromechanics of three-dimensional collagen-I gels. Complexity, 16(4), 22-28.
64. Thorne, R. G., Hrabetova, S., & Nicholson, C. (2004). Diffusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging. J. Neurophysiol., 92(6), 3471-3481.
65. Tlsty, T. D. (2001). Stromal cells can contribute oncogenic signals. Semin. Cancer Biol., 11(2), 97-104.
66. van den Hooff, A. (1988). Stromal involvement in malignant growth. Adv. Cancer Res., 50, 159-196.
67. Wakefield, L. M., Smith, D. M., Masui, T., Harris, C. C., & Sporn, M. B. (1987). Distribution and modulation of the cellular receptor for transforming growth factor-beta. J. Cell Biol., 105(2), 965-975.
68. Wells, C. A., & El-Ayat, G. A. (2007). Non-operative breast pathology: apocrine lesions. J. Clin. Pathol., 60, 1313-1320.
69. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., Stack, M. S., & Friedl, P. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol., 9(8), 893-904.
70. Woodcock, E. A., Land, S. L., & Andrews, R. K. (1993). A low affinity, low molecular weight endothelin-A receptor present in neonatal rat heart. Clin. Exp. Pharmacol. Physiol., 20(5), 331-334.
71. Zi, Z., Feng, Z., Chapnick, D. A., Dahl, M., Deng, D., Klipp, E., Moustakas, A., & Liu, X. (2011). Quantitative analysis of transient and sustained transforming growth factor-beta signaling dynamics. Mol. Syst. Biol., 7(492), 1-12.