Cell-scaffold adhesion dynamics measured in first seconds predicts cell growth on days scale - Optical tweezers study

ACS Applied Materials and Interfaces

Volumn 7, Issue 12, 2015, Pages 6782-6791

  Podlipec, Rok ^a   Štrancar, Janez ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

cell adhesion; cell growth; optical tweezers; scaffold biocompatibility; single cell manipulation

Indexed keywords

BIOCOMPATIBILITY; CELL ADHESION; CELL GROWTH; CELL PROLIFERATION; CELLS; DYNAMICS; FLUORESCENCE; FLUORESCENCE MICROSCOPY; GROWTH KINETICS; MOLECULAR BIOLOGY; OPTICAL CORRELATION; OPTICAL TWEEZERS;

ADHESION DYNAMICS; ANALYTICAL METHOD; CELL MANIPULATION; CONFOCAL FLUORESCENCE MICROSCOPY; EXPERIMENTAL TECHNIQUES; POSITION DETECTION; SINGLE CELL MANIPULATION; STRENGTH ANALYSIS;

SCAFFOLDS (BIOLOGY);

BIOMATERIAL;

ANIMAL; CELL ADHESION; CELL LINE; CELL PROLIFERATION; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DEVICES; FIBROBLAST; FLUORESCENCE MICROSCOPY; MOUSE; OPTICAL TWEEZERS; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL ADHESION; CELL LINE; CELL PROLIFERATION; FIBROBLASTS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; OPTICAL TWEEZERS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84926284104     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b00235     Document Type: Article

References (57)

1. Williams, D. F. On the Mechanisms of Biocompatibility Biomaterials 2008, 29, 2941-2953
2. Fisher, M. B.; Mauck, R. L. Tissue Engineering and Regenerative Medicine: Recent Innovations and the Transition to Translation Tissue Eng., Part B 2013, 19, 1-13
3. Lee, M. H.; Arcidiacono, J. A.; Bilek, A. M.; Wille, J. J.; Hamill, C. A.; Wonnacott, K. M.; Wells, M. A.; Oh, S. S. Considerations for Tissue-Engineered and Regenerative Medicine Product Development Prior to Clinical Trials in the United States Tissue Eng., Part B 2010, 16, 41-54
4. Hynes, R. O. Integrins: Bidirectional, Allosteric Signaling Machines Cell 2002, 110, 673-687
5. Schwarz, U. S.; Safran, S. S. Physics of Adherent Cells Rev. Mod. Phys. 2013, 85, 1327-1381
6. Bausch, A. R.; Schwarz, U. S. Cellular Mechanosensing: Sharing the Force Nat. Mater. 2013, 12, 948-949
7. Hoffman, B. D.; Grashoff, C.; Schwartz, M. A. Dynamic Molecular Processes Mediate Cellular Mechanotransduction Nature 2011, 475, 316-323
8. O'Brien, F. J. Biomaterials & Scaffolds for Tissue Engineering Mater. Today 2011, 14, 88-95
9. Jin, G. Z.; Kim, H. W. Nanocomposite Bioactive Polymeric Scaffold Promotes Adhesion, Proliferation and Osteogenesis of Rat Bone Marrow Stromal Cells Tissue Eng. Regener. Med. 2014, 11, 284-290
10. Huang, W. C.; Liu, K. H.; Liu, T. C.; Liu, D. M.; Chen, S. Y. Synergistic Hierarchical Silicone-Modified Polysaccharide Hybrid as a Soft Scaffold to Control Cell Adhesion and Proliferation Acta Biomater. 2014, 10, 3546-3556
11. Collart-Dutilleul, P. Y.; Secret, E.; Panayotov, I.; Deville de Périère, D.; Martín-Palma, R. J.; Torres-Costa, V.; Martin, M.; Gergely, C.; Durand, J. O.; Cunin, F.; Cuisinier, F. J. Adhesion and Proliferation of Human Mesenchymal Stem Cells from Dental Pulp on Porous Silicon Scaffolds ACS Appl. Mater. Interfaces 2014, 6, 1719-1728
12. García, A. J.; Ducheyne, P.; Boettiger, D. Quantification of Cell Adhesion Using a Spinning Disc Device and Application to Surface-Reactive Materials Biomaterials 1997, 18, 1091-1098
13. Sniadecki, N. J.; Chen, C. S. Microfabricated Silicone Elastomeric Post Arrays for Measuring Traction Forces of Adherent Cells Methods Cell Biol. 2007, 83, 313-328
14. Nugiel, D. J.; Wood, D. J.; Sung, K. L. Quantification of Adhesiveness of Osteoblasts to Titanium Surfaces In Vitro by the Micropipette Aspiration Technique Tissue Eng. 1996, 2, 127-140
15. Reyes, C. D.; García, A. J. A Centrifugation Cell Adhesion Assay for High-Throughput Screening of Biomaterial Surfaces J. Biomed. Mater. Res., Part A 2003, 67, 328-333
16. Helenius, J.; Heisenberg, C. P.; Gaub, H. E.; Muller, D. J. Single-Cell Force Spectroscopy J. Cell Sci. 2008, 121, 1785-1791
17. Zhang, H.; Liu, K. K. Optical Tweezers for Single Cells J. R. Soc., Interface 2008, 5, 671-690
18. Taubenberger, A.; Cisneros, D. A.; Friedrichs, J.; Puech, P. H.; Muller, D. J.; Franz, C. M. Revealing Early Steps of α21 Integrin-Mediated Adhesion to Collagen Type I by Using Single-Cell Force Spectroscopy Mol. Biol. Cell 2007, 18, 1634-1644
19. Thoumine, O.; Kocian, P.; Kottelat, A.; Meister, J. J. Short-Term Binding of Fibroblasts to Fibronectin: Optical Tweezers Experiments and Probabilistic Analysis Eur. Biophys. J. 2000, 29, 398-408
20. Wang, X.; Ha, T. Defining Single Molecular Forces Required to Activate Integrin and Notch Signaling Science 2013, 340, 991-994
21. Zhang, Y.; Ge, C.; Zhu, C.; Salaita, K. DNA-Based Digital Tension Probes Reveal Integrin Forces During Early Cell Adhesion Nat. Commun. 2014, 5, 1-10
22. Capitanio, M.; Pavone, F. S. Interrogating Biology with Force: Single Molecule High-Resolution Measurements with Optical Tweezers Biophys. J. 2013, 105, 1293-1303
23. Difato, F.; Pinato, G.; Cojoc, D. Cell Signaling Experiments Driven by Optical Manipulation Int. J. Mol. Sci. 2013, 14, 8963-8984
24. Bowman, R. W.; Padgett, M. J. Optical Trapping and Binding Rep. Prog. Phys. 2013, 76, 026401
25. Ashkin, A. In Optical Trapping and Manipulation of Neutral Particles Using Lasers; Ashkin, A., Ed.; World Scientific Publishing Co. Pte. Ltd.: Singapore, 2006; pp 1-915.
26. Richardson, A. C.; Reihani, N.; Oddershede, L. B. Combining Confocal Microscopy with Precise Force-Scope Optical Tweezers Proc. SPIE 2006, 632628
27. Comstock, M. J.; Ha, T.; Chemia, Y. R. Ultrahigh-Resolution Optical Trap with Single-Fluorophore Sensitivity Nat. Methods 2011, 8, 335-340
28. Thoumine, O.; Bard, L.; Saint-Michel, E.; Dequidt, C.; Choquet, D. Optical Tweezers and Fluorescence Recovery After Photo-Bleaching to Measure Molecular Interactions at the Cell Surface Cell. Mol. Bioeng. 2008, 1, 301-311
29. Andersson, M.; Madgavkar, A.; Stjerndahl, M.; Wu, Y.; Tan, W.; Duran, R.; Niehren, S.; Mustafa, K.; Arvidson, K.; Wennerberg, A. Using Optical Tweezers for Measuring the Interaction Forces Between Human Bone Cells and Implant Surfaces: System Design and Force Calibration Rev. Sci. Instrum. 2007, 78, 074302
30. Gou, X.; Han, H. C.; Hu, S.; Leung, A. Y. H.; Sun, D. Applying Combined Optical Tweezers and Fluorescence Microscopy Technologies to Manipulate Cell Adhesions for Cell-to-Cell Interaction Study IEEE Trans. Biomed. Eng. 2013, 60, 2308-2315
31. Hu, S.; Gou, X.; Han, H.; Leung, A. Y. H.; Sun, D. Manipulating Cell Adhesions with Optical Tweezers for Study of Cell-to-Cell Interactions J. Biomed. Nanotechnol. 2013, 9, 281-285
32. Podlipec, R.; Gorgieva, S.; Jurašin, D.; Urbančič, I.; Kokol, V.; Štrancar, J. Molecular Mobility of Scaffolds' Biopolymers Influences Cell Growth ACS Appl. Mater. Interfaces 2014, 6, 15980-15990
33. König, K. Laser Tweezers are Sources of Two-Photon Excitation Cell. Mol. Biol. 1998, 44, 721-733
34. Plieva, F. M.; Kumar, A.; Galaev, I. Y.; Mattiasson, B. In Advanced Biomaterials; Basu, B.; Katti, D. S.; Kumar, A., Eds.; John Wiley & Sons, Inc.: New Jersey, 2010; Chapter 14, pp 499-531.
35. Gornall, J. L.; Terentjev, E. M. Concentration-Temperature Superposition of Helix Folding Rates in Gelatin Phys. Rev. Lett. 2007, 99, 028304
36. Arsov, Z.; Urbančič, I.; Garvas, M.; Biglino, D.; Ljubetič, A.; Koklič, T.; Strancar, J. Fluorescence Microspectroscopy as a Tool to Study Mechanism of Nanoparticles Delivery into Living Cancer Cells Biomed. Opt. Express 2011, 2, 2083-2095
37. Liu, Y.; Cheng, D. K.; Sonek, G. J.; Berns, M. W.; Chapman, C. F.; Tromberg, B. J. Evidence for Localized Cell Heating Induced by Infrared Optical Tweezers Biophys. J. 1995, 68, 2137-2144
38. Ayano, S.; Wakamoto, Y.; Yamashita, S.; Yasuda, K. Quantitative Measurement of Damage Caused by 1064-nm Wavelength Optical Trapping of Escherichia Coli Cells Using On-Chip Single Cell Cultivation System Biochem. Biophys. Res. Commun. 2006, 350, 678-684
39. Urbančič, I. Response of Biomembrane Domains to External Stimuli, Ph.D. dissertation, University in Maribor, Maribor, 2013.
40. Litvinov, R. I.; Shuman, H.; Bennett, J. S.; Weisel, J. W. Binding Strength and Activation State of Single Fibrinogen-Integrin Pairs on Living Cells Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 7426-7431
41. Castelain, M.; Rouxhet, P. G.; Pignon, F.; Magnin, A.; Piau, J. M. Single-Cell Adhesion Probed In-Situ using Optical Tweezers: A Case Study with Saccharomyces Cerevisiae J. Appl. Phys. 2012, 111, 114701
42. Simmons, R. M.; Finer, J. T.; Chu, S.; Spudich, J. A. Quantitative Measurements of Force and Displacement using an Optical Trap Biophys. J. 1996, 70, 1813-1822
43. Schwingel, M.; Bastmeyer, M. Force Mapping during the Formation and Maturation of Cell Adhesion Sites with Multiple Optical Tweezers PLoS One 2013, 8, e54850
44. Svoboda, K.; Block, S. M. Biological Applications of Optical Forces Annu. Rev. Biophys. Biomol. Struct. 1994, 23, 247-285
45. Wu, Y.; Sun, D.; Huang, W. Mechanical Force Characterization in Manipulating Live Cells with Optical Tweezers J. Biomech. 2011, 44, 741-746
46. Evans, E. A.; Calderwood, D. A. Forces and Bond Dynamics in Cell Adhesion Science 2007, 316, 1148-1153
47. Bell, G. I. Models for the Specific Adhesion of Cells to Cells Science 1978, 200, 618-627
48. Page, B.; Page, M.; Noel, C. A New Fluorometric Assay for Cytotoxicity Measurements In-Vitro Int. J. Oncol. 1993, 3, 473-476
49. Gorelik, J.; Shevchuk, A. I.; Frolenkov, G. I.; Diakonov, I. A.; Lab, M. J.; Kros, C. J.; Richardson, G. P.; Vodyanoy, I.; Edwards, C. R. W.; Klenerman, D.; Korchev, Y. E. Dynamic Assembly of Surface Structures in Living Cells Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 5819-5822
50. Guck, J.; Ananthakrishnan, R.; Mahmood, H.; Moon, T. J.; Cunningham, C. C.; Kas, J. The Optical Stretcher: a Novel Laser Tool to Micromanipulate Cells Biophys. J. 2001, 81, 767-784
51. Alon, R.; Hammer, D. A.; Springer, T. A. Lifetime of the P-Selectin-Carbohydrate Bond and its Response to Tensile Force in Hydrodynamic Flow Nature 1995, 374, 539-542
52. Dong, C.; Cao, J.; Struble, E. J.; Lipowsky, H. H. Mechanics of Leukocyte Deformation and Adhesion to Endothelium in Shear Flow Ann. Biomed. Eng. 1999, 27, 298-312
53. Spillmann, C. M.; Lomakina, E.; Waugh, R. E. Neutrophil Adhesive Contact Dependence on Impingement Force Biophys. J. 2004, 87, 4237-4245
54. Schmitz, J.; Benoit, M.; Gottschalk, K. E. The Viscoelasticity of Membrane Tethers and its Importance for Cell Adhesion Biophys. J. 2008, 95, 1448-1459
55. Schakenraad, J. M.; Busscher, H. J.; Wildevuur, C. R. H.; Arends, J. The Influence of Substratum Surface Free Energy on Growth and Spreading of Human Fibroblasts in the Presence and Absence of Serum Proteins J. Biomed. Mater. Res. 1986, 20, 773-784
56. Dubruel, P.; Unger, R.; Van Vlierberghe, S.; Cnudde, V.; Jacobs, P. J. S.; Schacht, E.; Kirkpatrick, C. J. Porous Gelatin Hydrogels: 2. In Vitro Cell Interaction Study Biomacromolecules 2007, 8, 338-344
57. Dong, C.; Lei, X. X. Biomechanics of Cell Rolling: Shear Flow, Cell-Surface Adhesion, and Cell Deformability J. Biomech. 2000, 33, 35-43