The phenotype of cancer cell invasion controlled by fibril diameter and pore size of 3D collagen networks

Biomaterials

Volumn 52, Issue 1, 2015, Pages 367-375

  Sapudom, Jiranuwat ^a   Rubner, Stefan ^a   Martin, Steve ^a   Kurth, Tony ^a   Riedel, Stefanie ^a   Mierke, Claudia T ^a   Pompe, Tilo ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Cell morphology; Collagen; ECM (extracellular matrix); Invasion; Mechanical properties; Microstructure

Indexed keywords

ACCESS CONTROL; BIOMECHANICS; BIOMIMETICS; CELL CULTURE; COLLAGEN; COMPLEX NETWORKS; CYTOLOGY; DISEASES; ELASTICITY; MECHANICAL PROPERTIES; MECHANISMS; MICROSTRUCTURE; MORPHOLOGY; PORE SIZE; STIFFNESS MATRIX; TOPOLOGY;

CELL MORPHOLOGY; COMPLEX RELATIONSHIPS; CONFOCAL LASER SCANNING MICROSCOPY; CONTROL OF PORE SIZE; ECM (EXTRACELLULAR MATRIX); EXTRACELLULAR MATRICES; IMAGE ANALYSIS TOOLS; INVASION;

CELLS;

COLLAGEN; COLLAGEN TYPE 1; COLLOID;

ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER CELL LINE; BREAST CARCINOMA; CANCER CELL; CELL CULTURE; CELL FUNCTION; CELL INVASION; CELL PROLIFERATION; CELL STRUCTURE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; MCF 7 CELL LINE; PH; PHENOTYPE; PRIORITY JOURNAL; ROOM TEMPERATURE; TUMOR INVASION; BIOMIMETICS; CELL MOTION; CHEMISTRY; COLLOID; CONFOCAL MICROSCOPY; CULTURE TECHNIQUE; ELASTICITY; MECHANICAL STRESS; METASTASIS; NEOPLASM; PATHOLOGY; TUMOR CELL LINE;

BIOMIMETICS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MOVEMENT; COLLAGEN TYPE I; COLLOIDS; ELASTICITY; EXTRACELLULAR MATRIX; HUMANS; HYDROGEN-ION CONCENTRATION; MCF-7 CELLS; MICROSCOPY, CONFOCAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; PHENOTYPE; STRESS, MECHANICAL;

EID: 84932631326     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.022     Document Type: Article

References (50)

1. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003, 3:362-374.
2. Braun S., Naume B. Circulating and disseminated tumor cells. JClin Oncol 2005, 23:1623-1626.
3. Bacac M., Stamenkovic I. Metastatic cancer cell. Annu Rev Pathol 2008, 3:221-247.
4. Rocken M. Early tumor dissemination, but late metastasis: insights into tumor dormancy. JClin Invest 2010, 120:1800-1803.
5. Friedl P., Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011, 147:992-1009.
6. Brabek J., Mierke C.T., Rosel D., Vesely P., Fabry B. The role of the tissue microenvironment in the regulation of cancer cell motility and invasion. Cell Commun Signal 2010, 8:22.
7. Lu P., Weaver V.M., Werb Z. The extracellular matrix: a dynamic niche in cancer progression. JCell Biol 2012, 196:395-406.
8. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
9. Baker E.L., Lu J., Yu D., Bonnecaze R.T., Zaman M.H. Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys J 2010, 99:2048-2057.
10. Mierke C.T., Frey B., Fellner M., Herrmann M., Fabry B. Integrin alpha5beta1 facilitates cancer cell invasion through enhanced contractile forces. JCell Sci 2011, 124:369-383.
11. Kraning-Rush C.M., Califano J.P., Reinhart-King C.A. Cellular traction stresses increase with increasing metastatic potential. PLoS One 2012, 7. e32572.
12. Katira P., Zaman M.H., Bonnecaze R.T. How changes in cell mechanical properties induce cancerous behavior. Phys Rev Lett 2012, 108.
13. Seewaldt V. ECM stiffness paves the way for tumor cells. Nat Med 2014, 20:332-333.
14. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
15. Griffith L.G., Swartz M.A. Capturing complex 3D tissue physiology invitro. Nat Rev Mol Cell Biol 2006, 7:211-224.
16. Infanger D.W., Lynch M.E., Fischbach C. Engineered culture models for studies of tumor-microenvironment interactions. Annu Rev Biomed Eng 2013, 15:29-53.
17. Even-Ram S., Yamada K.M. Cell migration in 3D matrix. Curr Opin Cell Biol 2005, 17:524-532.
18. Nyga A., Cheema U., Loizidou M. 3D tumour models: novel invitro approaches to cancer studies. JCell Commun Signal 2011, 5:239-248.
19. Stamov D.R., Pompe T. Structure and function of ECM-inspired composite collagen type I scaffolds. Soft Matter 2012, 8:10200.
20. Jokinen J., Dadu E., Nykvist P., Kapyla J., White D.J., Ivaska J., et al. Integrin-mediated cell adhesion to type I collagen fibrils. JBiol Chem 2004, 279:31956-31963.
21. Popov C., Radic T., Haasters F., Prall W.C., Aszodi A., Gullberg D., et al. Integrins alpha2beta1 and alpha11beta1 regulate the survival of mesenchymal stem cells on collagen I. Cell Death Dis 2011, 2. e186.
22. Carlson M.A., Smith L.M., Cordes C.M., Chao J., Eudy J.D. Attachment-regulated signaling networks in the fibroblast-populated 3D collagen matrix. Sci Rep 2013, 3:1880.
23. Franke K., Sapudom J., Kalbitzer L., Anderegg U., Pompe T. Topologically defined composites of collagen types I and V as invitro cell culture scaffolds. Acta Biomater 2014, 10:2693-2702.
24. Wolf K., Te Lindert M., Krause M., Alexander S., Te Riet J., Willis A.L., et al. Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. JCell Biol 2013, 201:1069-1084.
25. Harjanto D., Maffei J.S., Zaman M.H. Quantitative analysis of the effect of cancer invasiveness and collagen concentration on 3D matrix remodeling. PLoS One 2011, 6. e24891.
26. Friedl P., Sahai E., Weiss S., Yamada K.M. New dimensions in cell migration. Nat Rev Mol Cell Biol 2012, 13:743-747.
27. Guzman A., Ziperstein M.J., Kaufman L.J. The effect of fibrillar matrix architecture on tumor cell invasion of physically challenging environments. Biomaterials 2014, 35:6954-6963.
28. Sun M., Chen S., Adams S.M., Florer J.B., Liu H., Kao W.W., et al. Collagen V is a dominant regulator of collagen fibrillogenesis: dysfunctional regulation of structure and function in a corneal-stroma-specific Col5a1-null mouse model. JCell Sci 2011, 124:4096-4105.
29. Doyle A.D., Wang F.W., Matsumoto K., Yamada K.M. One-dimensional topography underlies three-dimensional fibrillar cell migration. JCell Biol 2009, 184:481-490.
30. Leikin S., Rau D.C., Parsegian V.A. Temperature-favoured assembly of collagen is driven by hydrophilic not hydrophobic interactions. Nat Struct Biol 1995, 2:205-210.
31. Harris J.R., Soliakov A., Lewis R.J. Invitro fibrillogenesis of collagen type I in varying ionic and pH conditions. Micron 2013, 49:60-68.
32. Raub C.B., Unruh J., Suresh V., Krasieva T., Lindmo T., Gratton E., et al. Image correlation spectroscopy of multiphoton images correlates with collagen mechanical properties. Biophys J 2008, 94:2361-2373.
33. Raub C.B., Suresh V., Krasieva T., Lyubovitsky J., Mih J.D., Putnam A.J., et al. Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy. Biophys J 2007, 92:2212-2222.
34. Pompe T., Zschoche S., Herold N., Salchert K., Gouzy M.F., Sperling C., et al. Maleic anhydride copolymers-a versatile platform for molecular biosurface engineering. Biomacromolecules 2003, 4:1072-1079.
35. Hutter J.L., Bechhoefer J. Calibration of atomic-force microscope tips. Rev Sci Instrum 1993, 64:1868.
36. Carey S.P., Kraning-Rush C.M., Williams R.M., Reinhart-King C.A. Biophysical control of invasive tumor cell behavior by extracellular matrix microarchitecture. Biomaterials 2012, 33:4157-4165.
37. Wood G.C., Keech M.K. The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J 1960, 75:588-598.
38. Li Y., Asadi A., Monroe M.R., Douglas E.P. pH effects on collagen fibrillogenesis invitro: electrostatic interactions and phosphate binding. Mater Sci Eng C 2009, 29:1643-1649.
39. Charras G., Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol 2014, 15:813-824.
40. Roeder B.A., Kokini K., Sturgis J.E., Robinson J.P., Voytik-Harbin S.L. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. JBiomechanical Eng 2002, 124:214.
41. Mertz E.L., Leikin S. Interactions of inorganic phosphate and sulfate anions with collagen. Biochemistry 2004, 43:14901-14912.
42. Kurniawan N.A., Enemark S., Rajagopalan R. The role of structure in the nonlinear mechanics of cross-linked semiflexible polymer networks. JChem Phys 2012, 136. 065101.
43. Vargo-Gogola T., Rosen J.M. Modelling breast cancer: one size does not fit all. Nat Rev Cancer 2007, 7:659-672.
44. Holliday D.L., Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Res 2011, 13:215.
45. Geiger B., Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 2001, 13:584-592.
46. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol 2004, 16:14-23.
47. Weigelin B., Bakker G.-J., Friedl P. Intravital third harmonic generation microscopy of collective melanoma cell invasion. IntraVital 2014, 1:32-43.
48. Provenzano P.P., Inman D.R., Eliceiri K.W., Trier S.M., Keely P.J. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 2008, 95:5374-5384.
49. Zaman M.H., Trapani L.M., Sieminski A.L., Mackellar D., Gong H., Kamm R.D., et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U. S. A 2006, 103:10889-10894.
50. Ehrbar M., Sala A., Lienemann P., Ranga A., Mosiewicz K., Bittermann A., et al. Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys J 2011, 100:284-293.