Lattice-Based Model of Ductal Carcinoma In Situ Suggests Rules for Breast Cancer Progression to an Invasive State

PLoS Computational Biology

Volumn 10, Issue 12, 2014, Pages

  Boghaert, Eline ^a   Radisky, Derek C ^b   Nelson, Celeste M ^a,c  

^a Princeton University   (United States)

^b MAYO CLINIC   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; CELL DEATH; CELL PROLIFERATION; DISEASES; DUCTS; TUMORS;

BREAST CANCER; CANCER PROGRESSION; CONDITION; DUCTAL CARCINOMA IN SITU; IN-VIVO; LATTICE-BASED MODELS; MAMMARY EPITHELIAL CELLS; TISSUE MORPHOLOGY; TUMOUR CELLS; TWO-DIMENSIONAL;

MORPHOLOGY;

APOPTOSIS; ARTICLE; CANCER GROWTH; CELL ADHESION; CELL DIVISION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; INTRADUCTAL CARCINOMA; MATHEMATICAL MODEL; MEDICAL PARAMETERS; TISSUE CONTRACTILITY; TUMOR INVASION; BIOLOGICAL MODEL; BIOLOGY; BREAST TUMOR; FEMALE; HUMAN; PATHOPHYSIOLOGY; PHENOTYPE; TUMOR CELL CULTURE;

APOPTOSIS; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL ADHESION; COMPUTATIONAL BIOLOGY; FEMALE; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; PHENOTYPE; TUMOR CELLS, CULTURED;

EID: 84919683936     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003997     Document Type: Article

References (76)

1. Nelson CM, Bissell MJ, (2005) Modeling dynamic reciprocity: Engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 15: 342–352.
2. Nelson CM, Bissell MJ, (2006) Of extracellular matrix, scaffolds, and signaling: Tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22: 287–309.
3. Debnath J, Brugge JS, (2005) Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 5: 675–688.
4. Tavassoli FA, (1998) Ductal carcinoma in situ: introduction of the concept of ductal intraepithelial neoplasia. Mod Pathol 11: 140–154.
5. Burstein HJ, Polyak K, Wong JS, Lester SC, Kaelin CM, (2004) Ductal carcinoma in situ of the breast. N Engl J Med 350: 1430–1441.
6. Silverstein MJ, (2000) Ductal carcinoma in situ of the breast. Annu Rev Med 51: 17–32.
7. Sanders ME, Schuyler PA, Dupont WD, Page DL, (2005) The natural history of low-grade ductal carcinoma in situ of the breast in women treated by biopsy only revealed over 30 years of long-term follow-up. Cancer 103: 2481–2484.
8. Erbas B, Provenzano E, Armes J, Gertig D, (2006) The natural history of ductal carcinoma in situ of the breast: a review. Breast Cancer Res Treat 97: 135–144.
9. Jaffer S, Bleiweiss IJ, (2002) Histologic classification of ductal carcinoma in situ. Microsc Res Tech 59: 92–101.
10. Norton KA, Wininger M, Bhanot G, Ganesan S, Barnard N, et al. (2010) A 2D mechanistic model of breast ductal carcinoma in situ (DCIS) morphology and progression. J Theor Biol 263: 393–406.
11. Kerlikowske K, Molinaro A, Cha I, Ljung BM, Ernster VL, et al. (2003) Characteristics associated with recurrence among women with ductal carcinoma in situ treated by lumpectomy. J Natl Cancer Inst 95: 1692–1702.
12. Kerlikowske K, (2010) Epidemiology of ductal carcinoma in situ. J Natl Cancer Inst Monogr 2010: 139–141.
13. Page DL, Dupont WD, Rogers LW, Jensen RA, Schuyler PA, (1995) Continued local recurrence of carcinoma 15–25 years after a diagnosis of low grade ductal carcinoma in situ of the breast treated only by biopsy. Cancer 76: 1197–1200.
14. Fisher B, Dignam J, Wolmark N, Mamounas E, Costantino J, et al. (1998) Lumpectomy and radiation therapy for the treatment of intraductal breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-17. J Clin Oncol 16: 441–452.
15. Kricker A, Goumas C, Armstrong B, (2004) Ductal carcinoma in situ of the breast, a population-based study of epidemiology and pathology. Br J Cancer 90: 1382–1385.
16. Camps JL, Chang SM, Hsu TC, Freeman MR, Hong SJ, et al. (1990) Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci U S A 87: 75–79.
17. 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.
18. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241–254.
19. Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, et al. (2006) Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 4: 38.
20. Radisky DC, Przybylo JA, (2008) Matrix metalloproteinase-induced fibrosis and malignancy in breast and lung. P Am Thorac Soc 5: 316–322.
21. Samuel MS, Lopez JI, McGhee EJ, Croft DR, Strachan D, et al. (2011) Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 19: 776–791.
22. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, et al. (1997) Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137: 231–245.
23. Nelson CM, Khauv D, Bissell MJ, Radisky DC, (2008) Change in cell shape is required for matrix metalloproteinase-induced epithelial-mesenchymal transition of mammary epithelial cells. J Cell Biochem 105: 25–33.
24. Nielsen M, Thomsen JL, Primdahl S, Dyreborg U, Andersen JA, (1987) Breast cancer and atypia among young and middle-aged women: A study of 110 medicolegal autopsies. Br J Cancer 56: 814–819.
25. Boghaert E, Gleghorn JP, Lee K, Gjorevski N, Radisky DC, et al. (2012) Host epithelial geometry regulates breast cancer cell invasiveness. Proc Natl Acad Sci U S A 109: 19632–19637.
26. Soto AM, Sonnenschein C, (2011) The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory. BioEssays 33: 332–340.
27. Silberstein GB, (2001) Tumour-stromal interactions: Role of the stroma in mammary development. Breast Cancer Res 3: 218–223.
28. Simpson PT, Reis-Filho JS, Gale T, Lakhani SR, (2005) Molecular evolution of breast cancer. J Pathol 205: 248–254.
29. Gjorevski N, Nelson CM, (2010) Endogenous patterns of mechanical stress are required for branching morphogenesis. Integr Biol 2: 424–434.
30. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ, (2006) Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 314: 298–300.
31. Gjorevski N, Nelson CM, (2012) Mapping of mechanical strains and stresses around quiescent engineered three-dimensional epithelial tissues. Biophys J 103: 152–162.
32. Lennington WJ, Jensen RA, Dalton LW, Page DL, (1994) Ductal carcinoma in situ of the breast. Heterogeneity of individual lesions. Cancer 73: 118–124.
33. Swat MH, Hester SD, Balter AI, Heiland RW, Zaitlen BL, et al. (2009) Multicell simulations of development and disease using the CompuCell3D simulation environment. Methods Mol Biol 500: 361–428.
34. Swat MH, Thomas GL, Belmonte JM, Shirinifard A, Hmeljak D, et al. (2012) Multi-scale modeling of tissues using CompuCell3D. Methods Cell Biol 110: 325–366.
35. Poplawski NJ, Swat M, Gens JS, Glazier JA, (2007) Adhesion between cells, diffusion of growth factors, and elasticity of the AER produce the paddle shape of the chick limb. Physica A 373: 521–532.
36. Poplawski NJ, Agero U, Gens JS, Swat M, Glazier JA, et al. (2009) Front instabilities and invasiveness of simulated avascular tumors. Bull Math Biol 71: 1189–1227.
37. Giverso C, Scianna M, Preziosi L, Buono N, Funaro A, (2010) Individual cell-based model for in vitro mesothelial invasion of ovarian cancer. Math Model Nat Phenom 5: 203–223.
38. 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.
39. Andasari V, Roper RT, Swat MH, Chaplain MA, (2012) Integrating intracellular dynamics using CompuCell3D and Bionetsolver: applications to multiscale modelling of cancer cell growth and invasion. PLoS One 7: e33726.
40. Steinkamp MP, Winner KK, Davies S, Muller C, Zhang Y, et al. (2013) Ovarian tumor attachment, invasion, and vascularization reflect unique microenvironments in the peritoneum: insights from xenograft and mathematical models. Front Oncol 3: 97.
41. Swat M, Hester SD, Heiland RW, Zaitlen BL, Glazier JA, et al., CompuCell3D Manual and Tutorial Version 3.6.0. 2011, Biocomplexity Institute and Department of Physics, Indiana University: Bloomington, IN.
42. Bussolati G, Bongiovanni M, Cassoni P, Sapino A, (2000) Assessment of necrosis and hypoxia in ductal carcinoma in situ of the breast: basis for a new classification. Virchows Arch 437: 360–364.
43. Man YG, Tai L, Barner R, Vang R, Saenger JS, et al. (2003) Cell clusters overlying focally disrupted mammary myoepithelial cell layers and adjacent cells within the same duct display different immunohistochemical and genetic features: implications for tumor progression and invasion. Breast Cancer Res 5: R231–241.
44. Chanson L, Brownfield D, Garbe JC, Kuhn I, Stampfer MR, et al. (2011) Self-organization is a dynamic and lineage-intrinsic property of mammary epithelial cells. Proc Natl Acad Sci U S A 108: 3264–3269.
45. Zhang Y, Thomas GL, Swat M, Shirinifard A, Glazier JA, (2011) Computer simulations of cell sorting due to differential adhesion. PLoS One 6: e24999.
46. Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ, (1992) Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A 89: 9064–9068.
47. Rejniak KA, Anderson AR, (2008) A computational study of the development of epithelial acini: II. Necessary conditions for structure and lumen stability. Bull Math Biol 70: 1450–1479.
48. Rejniak KA, Anderson AR, (2008) A computational study of the development of epithelial acini: I. Sufficient conditions for the formation of a hollow structure. Bull Math Biol 70: 677–712.
49. Tang J, Enderling H, Becker-Weimann S, Pham C, Polyzos A, et al. (2011) Phenotypic transition maps of 3D breast acini obtained by imaging-guided agent-based modeling. Integr Biol 3: 408–421.
50. Edgerton ME, Chuang YL, Macklin P, Yang W, Bearer EL, et al. (2011) A novel, patient-specific mathematical pathology approach for assessment of surgical volume: application to ductal carcinoma in situ of the breast. Anal Cell Pathol (Amst) 34: 247–263.
51. Macklin P, Edgerton ME, Thompson AM, Cristini V, (2012) Patient-calibrated agent-based modelling of ductal carcinoma in situ (DCIS): from microscopic measurements to macroscopic predictions of clinical progression. J Theor Biol 301: 122–140.
52. Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, et al. (2012) Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484: 546–549.
53. Rosenblatt J, Raff MC, Cramer LP, (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11: 1847–1857.
54. Engels K, Fox SB, Whitehouse RM, Gatter KC, Harris AL, (1997) Distinct angiogenic patterns are associated with high-grade in situ ductal carcinomas of the breast. J Pathol 181: 207–212.
55. Guidi AJ, Fischer L, Harris JR, Schnitt SJ, (1994) Microvessel density and distribution in ductal carcinoma in situ of the breast. J Natl Cancer Inst 86: 614–619.
56. Werling RW, Hwang H, Yaziji H, Gown AM, (2003) Immunohistochemical distinction of invasive from noninvasive breast lesions: a comparative study of p63 versus calponin and smooth muscle myosin heavy chain. Am J Surg Pathol 27: 82–90.
57. Hill CB, Yeh IT, (2005) Myoepithelial cell staining patterns of papillary breast lesions: from intraductal papillomas to invasive papillary carcinomas. Am J Clin Pathol 123: 36–44.
58. Iwase H, Ando Y, Ichihara S, Toyoshima S, Nakamura T, et al. (2001) Immunohistochemical analysis on biological markers in ductal carcinoma in situ of the breast. Breast Cancer 8: 98–104.
59. Bijker N, Peterse JL, Duchateau L, Julien JP, Fentiman IS, et al. (2001) Risk factors for recurrence and metastasis after breast-conserving therapy for ductal carcinoma-in-situ: analysis of European Organization for Research and Treatment of Cancer Trial 10853. J Clin Oncol 19: 2263–2271.
60. Pinder SE, (2010) Ductal carcinoma in situ (DCIS): pathological features, differential diagnosis, prognostic factors and specimen evaluation. Mod Pathol 23 Suppl 2: S8–13.
61. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, et al. (2013) A Mechanical Checkpoint Controls Multicellular Growth through YAP/TAZ Regulation by Actin-Processing Factors. Cell 154: 1047–1059.
62. Li JF, Lowengrub J, (2013) The effects of cell compressibility, motility and contact inhibition on the growth of tumor cell clusters using the Cellular Potts Model. J Theor Biol
63. Bankhead A, 3rdMagnuson NS, Heckendorn RB, (2007) Cellular automaton simulation examining progenitor hierarchy structure effects on mammary ductal carcinoma in situ. J Theor Biol 246: 491–498.
64. Franks SJ, Byrne HM, Underwood JC, Lewis CE, (2005) Biological inferences from a mathematical model of comedo ductal carcinoma in situ of the breast. J Theor Biol 232: 523–543.
65. Albonico G, Querzoli P, Ferretti S, Rinaldi R, Nenci I, (1998) Biological profile of in situ breast cancer investigated by immunohistochemical technique. Cancer Detect Prev 22: 313–318.
66. Lari SA, Kuerer HM, (2011) Biological Markers in DCIS and Risk of Breast Recurrence: A Systematic Review. J Cancer 2: 232–261.
67. Skinner KA, Silverstein MJ, (2001) The management of ductal carcinoma in situ of the breast. Endocr Relat Cancer 8: 33–45.
68. Cerruti B, Puliafito A, Shewan AM, Yu W, Combes AN, et al. (2013) Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures. J Cell Biol 203: 359–372.
69. Kim Y, Othmer HG, (2013) A hybrid model of tumor-stromal interactions in breast cancer. Bull Math Biol 75: 1304–1350.
70. Dvorak HF, Weaver VM, Tlsty TD, Bergers G, (2011) Tumor microenvironment and progression. J Surg Oncol 103: 468–474.
71. 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.
72. Edinger AL, Thompson CB, (2004) Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663–669.
73. Poller DN, Silverstein MJ, Galea M, Locker AP, Elston CW, et al. (1994) Ideas in pathology. Ductal carcinoma in situ of the breast: a proposal for a new simplified histological classification association between cellular proliferation and c-erbB-2 protein expression. Mod Pathol 7: 257–262.
74. Silverstein MJ, Poller DN, Waisman JR, Colburn WJ, Barth A, et al. (1995) Prognostic classification of breast ductal carcinoma-in-situ. Lancet 345: 1154–1157.
75. Mammoto T, Mammoto A, Ingber DE, (2013) Mechanobiology and developmental control. Annu Rev Cell Dev Biol 29: 27–61.
76. Infanger DW, Lynch ME, Fischbach C, (2013) Engineered culture models for studies of tumor-microenvironment interactions. Annu Rev Biomed Eng 15: 29–53.