Real-Time Motion Analysis Reveals Cell Directionality as an Indicator of Breast Cancer Progression

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Weiger, Michael C ^a   Vedham, Vidya ^a   Stuelten, Christina H ^a   Shou, Karen ^a   Herrera, Mark ^b   Sato, Misako ^a   Losert, Wolfgang ^b   Parent, Carole A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b University of Maryland   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; EPIDERMAL GROWTH FACTOR; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CELL ADHESION; CELL DENSITY; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; METASTASIS; MOTION ANALYSIS SYSTEM; PARTICLE IMAGE VELOCIMETRY; QUANTITATIVE ANALYSIS; REACTION TIME; TIME LAPSE IMAGING;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MIGRATION ASSAYS; CELL MOVEMENT; DISEASE PROGRESSION; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; LYSOPHOSPHOLIPIDS; NEOPLASM METASTASIS; PHENOTYPE; TUMOR STEM CELL ASSAY;

EID: 84875112484     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058859     Document Type: Article

References (66)

1. Friedl P, Gilmour D, (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10: 445-457.
2. Friedl P, Wolf K, (2010) Plasticity of cell migration: a multiscale tuning model. J Cell Biol 188: 11-19.
3. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
4. Howlader N NA, Krapcho M, Neyman N, Aminou R, Altekruse SF,et al. (2009) SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations). Bethesda, MD: National Cancer Institute.
5. Gupta GP, Massague J, (2006) Cancer metastasis: building a framework. Cell 127: 679-695.
6. Chaffer CL, Weinberg RA, (2011) A perspective on cancer cell metastasis. Science 331: 1559-1564.
7. Valastyan S, Weinberg RA, (2011) Tumor metastasis: molecular insights and evolving paradigms. Cell 147: 275-292.
8. Coghlin C, Murray GI, (2010) Current and emerging concepts in tumour metastasis. J Pathol 222: 1-15.
9. Tyan SW, Kuo WH, Huang CK, Pan CC, Shew JY, et al. (2011) Breast cancer cells induce cancer-associated fibroblasts to secrete hepatocyte growth factor to enhance breast tumorigenesis. PLoS One 6: e15313.
10. Stuelten CH, Busch JI, Tang B, Flanders KC, Oshima A, et al. (2010) Transient tumor-fibroblast interactions increase tumor cell malignancy by a TGF-β mediated mechanism in a mouse xenograft model of breast cancer. PLoS One 5: e9832.
11. Wells A, Kassis J, Solava J, Turner T, Lauffenburger DA, (2002) Growth factor-induced cell motility in tumor invasion. Acta Oncol 41: 124-130.
12. Joslin EJ, Opresko LK, Wells A, Wiley HS, Lauffenburger DA, (2007) EGF-receptor-mediated mammary epithelial cell migration is driven by sustained ERK signaling from autocrine stimulation. J Cell Sci 120: 3688-3699.
13. Nie F, Yang J, Wen S, An YL, Ding J, et al. (2012) Involvement of epidermal growth factor receptor overexpression in the promotion of breast cancer brain metastasis. Cancer 118: 5198-5209.
14. Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, et al. (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64: 7022-7029.
15. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, et al. (2005) Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res 65: 5278-5283.
16. Ferrero JM, Ramaioli A, Largillier R, Formento JL, Francoual M, et al. (2001) Epidermal growth factor receptor expression in 780 breast cancer patients: a reappraisal of the prognostic value based on an eight-year median follow-up. Ann Oncol 12: 841-846.
17. Stern DF, (2000) Tyrosine kinase signalling in breast cancer: ErbB family receptor tyrosine kinases. Breast Cancer Res 2: 176-183.
18. Xue C, Wyckoff J, Liang F, Sidani M, Violini S, et al. (2006) Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis. Cancer Res 66: 192-197.
19. Barnes CJ, Kumar R, (2003) Epidermal growth factor receptor family tyrosine kinases as signal integrators and therapeutic targets. Cancer Metastasis Rev 22: 301-307.
20. Pradeep CR, Zeisel A, Kostler WJ, Lauriola M, Jacob-Hirsch J, et al. (2012) Modeling invasive breast cancer: growth factors propel progression of HER2-positive premalignant lesions. Oncogene 31: 3569-3583.
21. Mills GB, Moolenaar WH, (2003) The emerging role of lysophosphatidic acid in cancer. Nat Rev Cancer 3: 582-591.
22. Panupinthu N, Lee HY, Mills GB, (2010) Lysophosphatidic acid production and action: critical new players in breast cancer initiation and progression. Br J Cancer 102: 941-946.
23. Liu S, Umezu-Goto M, Murph M, Lu Y, Liu W, et al. (2009) Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15: 539-550.
24. Boucharaba A, Serre CM, Gres S, Saulnier-Blache JS, Bordet JC, et al. (2004) Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. J Clin Invest 114: 1714-1725.
25. Zhang H, Xu X, Gajewiak J, Tsukahara R, Fujiwara Y, et al. (2009) Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression in vivo. Cancer Res 69: 5441-5449.
26. Marella NV, Malyavantham KS, Wang J, Matsui S, Liang P, et al. (2009) Cytogenetic and cDNA microarray expression analysis of MCF10 human breast cancer progression cell lines. Cancer Res 69: 5946-5953.
27. Kadota M, Yang HH, Gomez B, Sato M, Clifford RJ, et al. (2010) Delineating genetic alterations for tumor progression in the MCF10A series of breast cancer cell lines. PLoS One 5: e9201.
28. Tang B, Vu M, Booker T, Santner SJ, Miller FR, et al. (2003) TGF-β switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. JClinInvest 112: 1116-1124.
29. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, et al. (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50: 6075-6086.
30. Dawson PJ, Wolman SR, Tait L, Heppner GH, Miller FR, (1996) MCF10AT: a model for the evolution of cancer from proliferative breast disease. AmJPathol 148: 313-319.
31. 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 Res Treat 65: 101-110.
32. Stephens PJ, Tarpey PS, Davies H, Van Loo P, Greenman C, et al. (2012) The landscape of cancer genes and mutational processes in breast cancer. Nature 486: 400-404.
33. Comprehensive molecular portraits of human breast tumours. Nature 490: 61-70.
34. Petitjean L, Reffay M, Grasland-Mongrain E, Poujade M, Ladoux B, et al. (2010) Velocity fields in a collectively migrating epithelium. Biophys J 98: 1790-1800.
35. Puliafito A, Hufnagel L, Neveu P, Streichan S, Sigal A, et al. (2012) Collective and single cell behavior in epithelial contact inhibition. Proc Natl Acad Sci U S A 109: 739-744.
36. Poujade M, Grasland-Mongrain E, Hertzog A, Jouanneau J, Chavrier P, et al. (2007) Collective migration of an epithelial monolayer in response to a model wound. Proc Natl Acad Sci U S A 104: 15988-15993.
37. Nnetu KD, Knorr M, Strehle D, Zink M, Kas JA, (2012) Directed persistent motion maintains sheet integrity during multi-cellular spreading and migration. Soft Matter 8: 6913-6921.
38. Nikolic DL, Boettiger AN, Bar-Sagi D, Carbeck JD, Shvartsman SY, (2006) Role of boundary conditions in an experimental model of epithelial wound healing. Am J Physiol Cell Physiol 291: C68-75.
39. Rosen P, Misfeldt DS, (1980) Cell density determines epithelial migration in culture. Proc Natl Acad Sci U S A 77: 4760-4763.
40. Chen M, Towers LN, O'Connor KL, (2007) LPA2 (EDG4) mediates Rho-dependent chemotaxis with lower efficacy than LPA1 (EDG2) in breast carcinoma cells. Am J Physiol Cell Physiol 292: C1927-1933.
41. Li TT, Alemayehu M, Aziziyeh AI, Pape C, Pampillo M, et al. (2009) Beta-arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Mol Cancer Res 7: 1064-1077.
42. Doll F, Pfeilschifter J, Huwiler A, (2005) The epidermal growth factor stimulates sphingosine kinase-1 expression and activity in the human mammary carcinoma cell line MCF7. Biochim Biophys Acta 1738: 72-81.
43. Ohta H, Sato K, Murata N, Damirin A, Malchinkhuu E, et al. (2003) Ki16425, a subtype-selective antagonist for EDG-family lysophosphatidic acid receptors. Mol Pharmacol 64: 994-1005.
44. Palmieri D, Halverson DO, Ouatas T, Horak CE, Salerno M, et al. (2005) Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptor-negative breast cancer. J Natl Cancer Inst 97: 632-642.
45. Chavez KJ, Garimella SV, Lipkowitz S, (2010) Triple negative breast cancer cell lines: one tool in the search for better treatment of triple negative breast cancer. Breast Dis 32: 35-48.
46. Friedl P, Wolf K, (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362-374.
47. Friedl P, Noble PB, Walton PA, Laird DW, Chauvin PJ, et al. (1995) Migration of coordinated cell clusters in mesenchymal and epithelial cancer explants in vitro. Cancer Res 55: 4557-4560.
48. Christiansen JJ, Rajasekaran AK, (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66: 8319-8326.
49. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, et al. (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9: 1392-1400.
50. Friedl P, Sahai E, Weiss S, Yamada KM, (2012) New dimensions in cell migration. Nat Rev Mol Cell Biol 13: 743-747.
51. Yarrow JC, Totsukawa G, Charras GT, Mitchison TJ, (2005) Screening for cell migration inhibitors via automated microscopy reveals a Rho-kinase inhibitor. Chem Biol 12: 385-395.
52. Simpson KJ, Selfors LM, Bui J, Reynolds A, Leake D, et al. (2008) Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 10: 1027-1038.
53. Lara R, Mauri FA, Taylor H, Derua R, Shia A, et al. (2011) An siRNA screen identifies RSK1 as a key modulator of lung cancer metastasis. Oncogene 30: 3513-3521.
54. Philippar U, Roussos ET, Oser M, Yamaguchi H, Kim HD, et al. (2008) A Mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. Dev Cell 15: 813-828.
55. Meyer AS, Hughes-Alford SK, Kay JE, Castillo A, Wells A, et al. (2012) 2D protrusion but not motility predicts growth factor-induced cancer cell migration in 3D collagen. J Cell Biol 197: 721-729.
56. Du J, Sun C, Hu Z, Yang Y, Zhu Y, et al. (2010) Lysophosphatidic acid induces MDA-MB-231 breast cancer cells migration through activation of PI3K/PAK1/ERK signaling. PLoS One 5: e15940.
57. Garcia R, Franklin RA, McCubrey JA, (2006) EGF induces cell motility and multi-drug resistance gene expression in breast cancer cells. Cell Cycle 5: 2820-2826.
58. Verbeek BS, Adriaansen-Slot SS, Vroom TM, Beckers T, Rijksen G, (1998) Overexpression of EGFR and c-erbB2 causes enhanced cell migration in human breast cancer cells and NIH3T3 fibroblasts. FEBS Lett 425: 145-150.
59. Yang Z, Bagheri-Yarmand R, Wang RA, Adam L, Papadimitrakopoulou VV, et al. (2004) The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 (Iressa) suppresses c-Src and Pak1 pathways and invasiveness of human cancer cells. Clin Cancer Res 10: 658-667.
60. Boucharaba A, Serre CM, Guglielmi J, Bordet JC, Clezardin P, et al. (2006) The type 1 lysophosphatidic acid receptor is a target for therapy in bone metastases. Proc Natl Acad Sci U S A 103: 9643-9648.
61. Giampieri S, Manning C, Hooper S, Jones L, Hill CS, et al. (2009) Localized and reversible TGF-β signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 11: 1287-1296.
62. Celia-Terrassa T, Meca-Cortes O, Mateo F, de Paz AM, Rubio N, et al. (2012) Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest 122: 1849-1868.
63. Choi JW, Herr DR, Noguchi K, Yung YC, Lee CW, et al. (2010) LPA receptors: subtypes and biological actions. Annu Rev Pharmacol Toxicol 50: 157-186.
64. Harma V, Knuuttila M, Virtanen J, Mirtti T, Kohonen P, et al. (2012) Lysophosphatidic acid and sphingosine-1-phosphate promote morphogenesis and block invasion of prostate cancer cells in three-dimensional organotypic models. Oncogene 31: 2075-2089.
65. Komachi M, Tomura H, Malchinkhuu E, Tobo M, Mogi C, et al. (2009) LPA1 receptors mediate stimulation, whereas LPA2 receptors mediate inhibition, of migration of pancreatic cancer cells in response to lysophosphatidic acid and malignant ascites. Carcinogenesis 30: 457-465.
66. Roberts AB, Wakefield LM, (2003) The two faces of transforming growth factor beta in carcinogenesis. ProcNatlAcadSciUSA 100: 8621-8623.