Molecular mobility of scaffolds' biopolymers influences cell growth

ACS Applied Materials and Interfaces

Volumn 6, Issue 18, 2014, Pages 15980-15990

  Podlipec, Rok ^a   Gorgieva, Selestina ^b   Jurašin, Darija ^c   Urbančič, Iztok ^d   Kokol, Vanja ^a,b   Štrancar, Janez ^a,d  

^a Centre of Excellence NAMASTE   (Slovenia)

^b UNIVERSITY OF MARIBOR   (Slovenia)

^c RUDER BO KOVI INSTITUTE   (Croatia)

^d JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Cell growth; Morphology; Polymer mobility; Scaffold biocompatibility; Viscoelasticity

Indexed keywords

BIOCOMPATIBILITY; BIOPOLYMERS; CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELLS; ELECTRON SPIN RESONANCE SPECTROSCOPY; GROWTH KINETICS; MORPHOLOGY; PARAMAGNETIC RESONANCE; ROTATIONAL FLOW; VISCOELASTICITY;

CELL-BIOMATERIAL INTERACTIONS; CONSTANT IMPROVEMENT; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR PROPERTIES; POLYMER MOBILITY; SCAFFOLD MORPHOLOGY; SITE-DIRECTED SPIN LABELING; SURFACE CHARACTERISTICS;

SCAFFOLDS (BIOLOGY);

BIOMATERIAL; BIOPOLYMER; GELATIN;

ANIMAL; CELL LINE; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; ELASTICITY; MOUSE; TISSUE SCAFFOLD;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOPOLYMERS; CELL LINE; CELL PROLIFERATION; ELASTICITY; GELATIN; MICE; TISSUE SCAFFOLDS;

EID: 84908064464     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am5037719     Document Type: Article

References (67)

1. Langer, R.; Vacanti, J. P. Tissue Engineering. Science 1993, 260, 920-926.
2. Harrison, R. H.; St-Pierre, J. P.; Stevens, M. M. Tissue Engineering and Regenerative Medicine: A Year in Review. Tissue Eng., Part B 2014, 20, 1-14.
3. Owen, S. C.; Shoichet, M. S. Design of Three-Dimensional Biomimetic Scaffolds. J. Biomed. Mater. Res., Part A 2010, 15, 1321-1331.
4. Gauvin, R.; Chen, Y.-C.; Lee, J. W.; Soman, P.; Zorlutana, P.; Nichol, J. W.; Bae, H.; Chen, S.; Khademhosseini, A. Microfabrication of Complex Porous Tissue Engineering Scaffolds Using 3D Projection Stereolithography. Biomaterials 2012, 33, 3824-3834.
5. Giannitelli, S. M.; Accoto, D.; Trombetta, M.; Rainer, A. Current Trends in the Design of Scaffolds for Computer-Aided Tissue Engineering. Acta Biomater. 2014, 10, 580-594.
6. Sun, J.-Y.; Zhao, X.; Illeperuma, W. R. K.; Chaudhuri, O.; Oh, K. H.; Mooney, D. J.; Vlassak, J. J.; Suo, Z. Highly Stretchable and Tough Hydrogels. Nature 2012, 489, 133-136.
7. Bhat, S.; Tripathi, A.; Kumar, A. Supermacroprous Chitosan-Agarose-Gelatin Cryogels: In Vitro Characterization and In Vivo Assessment for Cartilage Tissue Engineering. J. R. Soc. Interface 2011, 8, 540-554.
8. Patnaik, S. S.; Wang, B.; Weed, B.; Wertheim, J. A.; Liao, J. In Tissue Regeneration: Where Nanostructure Meets Biology; Liu, Q.; Wang, H., Eds.; World Scientific Publishing Co Pte Ltd: Singapore, 2014; Chapter 3, pp 77-124.
9. Badylak, S. F.; Taylor, D.; Uygun, K. Whole-Organ Tissue Engineering: Decellularization and Recellularization of Three-Dimensional Matrix Scaffolds. Annu. Rev. Biomed. Eng. 2011, 13, 27-53.
10. Radisic, M.; Yang, L.; Boublik, J.; Cohen, R. J.; Langer, R.; Freed, L. E.; Vunjak-Novakovic, G. Medium Perfusion Enables Engineering of Compact and Contractile Cardiac Tissue. Am. J. Physiol.: Heart Circ. Physiol. 2004, 286, 507-516.
11. Griffith, L. G.; Swartz, M. A. Capturing Complex 3D Tissue Physiology In Vitro. Nat. Rev. Mol. Cell Biol. 2006, 7, 211-224.
12. Sampson, S. L.; Saravia, L.; Gustafsson, K.; Jayasinghe, S. N.; Robertson, B. D. Cell Electrospinning: An In Vitro and In Vivo Study. Small 2014, 10, 78-82.
13. Hacker, M. C.; Mikos, A. G. Trends in Tissue Engineering Research. Tissue Eng. 2006, 12, 2049-2057.
14. Sanz-Herrera, J. A.; Reina-Romo, E. Cell-Biomaterial Mechanical Interaction in the Framework of Tissue Engineering: Insights, Computational Modeling and Perspectives. Int. J. Mol. Sci. 2011, 12, 8217-8244.
15. 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.
16. O'Dea, R. D.; Osborne, J. M.; El Haj, A. J.; Byrne, H. M.; Waters, S. L. The Interplay between Tissue Growth and Scaffold Degradation in Engineered Tissue Constructs. J. Math. Biol. 2012, 67, 1199-1225.
17. Kohane, D.; Langer, R. Biocompatibility and Drug Delivery Systems. Chem. Sci. 2010, 1, 441-446.
18. Gonzalez-Simon, A. L.; Eniola-Adefeso, O. In Engineering Biomaterials for Regenerative Medicine; Bhatia, S. K., Ed.; Springer: NY, 2012; Chapter 6, pp 143-159.
19. Place, E. S.; Evans, N. D.; Stevens, M. M. Complexity in Biomaterials for Tissue Engineering. Nat. Mater. 2009, 8, 457-470.
20. Kim, T. G.; Shin, H.; Lim, D. W. Biomimetic Scaffolds for Tissue Engineering. Adv. Funct. Mater. 2012, 22, 2446-2468.
21. Duron, A., Laurencin, C. T. In Nanotechnology and Tissue Engineering: The Scaffold; Laurencin, C. T., Nair, L. S., Eds.; CRC Press: Boca Raton, 2008; Chapter 6, pp 163-196.
22. Romano, N. H.; Sengupta, D.; Chung, C.; Heilshorn, S. C. Protein-Engineered Biomaterials: Nanoscale Mimics of the Extracellular Matrix. Biochim. Biophys. Acta 2011, 1810, 339-349.
23. Discher, D. E.; Janmey, P.; Wang, Y. Tissue Cells Feel and Respond to the Stiffness of Their Substrate. Science 2005, 310, 1139-1143.
24. Brandl, F.; Sommer, F.; Goepferich, A. Rational Design of Hydrogels for Tissue Engineering: Impact of Physical Factors on Cell Behavior. Biomaterials 2007, 28, 134-146.
25. Schlie-Wolter, S.; Ngezahayo, A.; Chichkov, B. N. The Selective Role of ECM Components on Cell Adhesion, Morphology, Proliferation and Communication In Vitro. Exp. Cell Res. 2013, 319, 1553-1561.
26. Oh, S. H.; Kim, T. H.; Im, G. I.; Lee, J. H. Investigation of Pore Size Effect on Chondrogenic Differentiation of Adipose Stem Cells Using a Pore Size Gradient Scaffold. Biomacromolecules 2010, 11, 1948-1955.
27. Lien, S. M.; Ko, L. Y.; Huang, T. J. Effect of Pore Size on ECM Secretion and Cell Growth in Gelatin Scaffold for Articular Cartilage Tissue Engineering. Acta Biomater. 2009, 5, 670-679.
28. Oh, S. H.; Park, I. K.; Kim, J. M.; Lee, J. H. In Vitro and in Vivo Characteristics of PCL Scaffolds with Pore Size Gradient Fabricated by a Centrifugation Method. Biomaterials 2007, 28, 1664-1671.
29. Harley, B. A.; Kim, H. D.; Zaman, M. H.; Yannas, I. V.; Lauffenburger, D. A.; Gibson, L. J. Microarchitecture of Three-Dimensional Scaffolds Influences Cell Migration Behavior via Junction Interactions. Biophys. J. 2008, 95, 4013-4024.
30. Murphy, C. M.; Haugh, M. G.; O'Brien, F. J. The Effect of Mean Pore Size on Cell Attachment, Proliferation and Migration in Collagen-Glycosaminoglycan Scaffolds for Bone Tissue Engineering. Biomaterials 2010, 31, 461-466.
31. Lee, M.; Wu, B. M.; Dunn, J. C. Y. Effect of Scaffold Architecture and Pore Size on Smooth Muscle Cell Growth. J. Biomed. Mater. Res., Part A 2008, 87, 1010-1016.
32. Van Bael, S.; Chai, Y. C.; Truscello, S.; Moesen, M.; Kerckhofs, G.; Van Oosterwyck, H.; Kruth, J. P.; Schrooten, J. The Effect of Pore Geometry on the In Vitro Biological Behavior of Human Periosteum-Derived Cells Seeded on Selective Laser-melted Ti6Al4V Bone Scaffolds. Acta Biomater. 2012, 8, 2824-2834.
33. Sobral, J. M.; Caridade, S. G.; Sousa, R. A.; Mano, J. F.; Reis, R. L. Three-Dimensional Plotted Scaffolds with Controlled Pore Size Gradients: Effect of Scaffold Geometry on Mechanical Performance and Cell Seeding Efficiency. Acta Biomater. 2011, 7, 1009-1018.
34. Griffon, D. J.; Sedighi, M. R.; Schaeffer, D. V.; Eurell, J. A.; Johnson, A. L. Chitosan Scaffolds: Interconnective Pore Size and Cartilage Engineering. Acta Biomater. 2006, 2, 313-320.
35. Hadjipanayi, E.; Mudera, V.; Brown, R. A. Close Dependence of Fibroblast Proliferation on Collagen Scaffold Matrix Stiffness. J. Tissue Eng. Regener. Med. 2009, 3, 77-84.
36. Haugh, M. G.; Murphy, C. M.; McKiernan, R. C.; Altenbuchner, C.; O'Brien, F. J. Crosslinking and Mechanical Properties Significantly Influence Cell Attachment, Proliferation, and Migration Within Collagen Glycosaminoglycan Scaffolds. Tissue Eng., Part A 2011, 17, 1201-1208.
37. Ghosh, K.; Pan, Z.; Guan, E.; Ge, S.; Liu, Y.; Nakamura, T.; Ren, X. D.; Rafailovich, M.; Clark, R. A. Cell Adaptation to a Physiologically Relevant ECM Mimic with Different Viscoelastic Properties. Biomaterials 2007, 28, 671-679.
38. Chen, J.; Irianto, J.; Inamdar, S.; Pravincumar, P.; Lee, D. A.; Bader, D. L.; Knight, M. M. Cell Mechanics, Structure, and Function are Regulated by the Stiffness of the Three-Dimensional Microenvironment. Biophys. J. 2012, 103, 1188-1197.
39. Saha, K.; Keung, A. J.; Irwin, E. F.; Li, Y.; Little, L.; Schaffer, D. V.; Healy, K. E. Substrate Modulus Directs Neural Stem Cell Behavior. Biophys. J. 2008, 95, 4426-4438.
40. Reinhart-King, C. A.; Dembo, M.; Hammer, D. A. Cell-Cell Mechanical Communication Through Compliant Substrates. Biophys. J. 2008, 95, 6044-6051.
41. Dikovsky, D.; Bianco-Peled, H.; Seliktar, D. Defining the Role of Matrix Compliance and Proteolysis in Three-Dimensional Cell Spreading and Remodeling. Biophys. J. 2008, 94, 2914-2925.
42. Liu, C.; Abedian, R.; Meister, R.; Haasper, C.; Hurschler, C.; Krettek, C.; Lewinski, G. V.; Jagodzinski, M. Influence of Perfusion and Compression on the Proliferation and Differentiation of Bone Mesenchymal Stromal Cells Seeded on Polyurethane Scaffolds. Biomaterials 2012, 33, 1052-1064.
43. Keselowsky, B. G.; Collard, D. M.; García, A. J. Integrin Binding Specificity Regulates Biomaterial Surface Chemistry Effects on Cell Differentiation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 5953-5957.
44. Koo, L. Y.; Irvine, D. J.; Mayes, A. M.; Lauffenburger, D. A.; Griffith, L. G. Co-Regulation of Cell Adhesion by Nanoscale RGD Organization and Mechanical Stimulus. J. Cell Sci. 2002, 115, 1423-1433.
45. Brown, B. N.; Barnes, C. A.; Kasick, R. T.; Michel, R.; Gilbert, T. W.; Beer-Stolz, D.; Castner, D. G.; Ratner, B. D.; Badylak, S. F. Surface Characterization of Extracellular Matrix Scaffolds. Biomaterials 2010, 31, 428-437.
46. Kisiday, J.; Jin, M.; Kurz, B.; Hung, H.; Semino, C.; Zhang, S.; Grodzinsky, A. J. Self-Assembling Peptide Hydrogel Fosters Chondrocyte Extracellular Matrix Production and Cell Division: Implications for Cartilage Tissue Repair. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 9996-10001.
47. Ivirico, J. L.; Salmeron-Sanchez, M.; Ribelles, J. L.; Pradas, M. M.; Soria, J. M.; Gomes, M. E.; Reis, R. L.; Mano, J. F. Proliferation and Differentiation of Goat Bone Marrow Stromal Cells in 3D Scaffolds with Tunable Hydrophilicity. J. Biomed. Mater. Res., Part B 2009, 91, 277-286.
48. Koh, H. S.; Yong, T.; Chan, C. K.; Ramakrishna, S. Enhancement of Neurite Outgrowth Using Nano-Structured Scaffolds Coupled with Laminin. Biomaterials 2008, 29, 3574-3582.
49. Jithendra, P.; Rajam, A. M.; Kalaivani, T.; Mandal, A. B.; Rose, C. Preparation and Characterization of Aloe Vera Blended Collagen-Chitosan Composite Scaffold for Tissue Engineering Applications. ACS Appl. Mater. Interfaces 2013, 5, 7291-7298.
50. Santos, E.; Hernández, R. M.; Pedraz, J. L.; Orive, G. Novel Advances in the Design of Three-Dimensional Bio-Scaffolds to Control Cell Fate: Translation from 2D to 3D. Trends Biotechnol. 2012, 30, 331-341.
51. Williams, D. F. On the Mechanisms of Biocompatibility. Biomaterials 2008, 29, 2941-2953.
52. Gornall, J. L.; Terentjev, E. M. Universal Kinetics of Helix-Coil Transition in Gelatin. Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2008, 77, 031908.
53. Mckinney, R. M.; Spillane, J. T.; Pearce, G. W. Factors Affecting the Rate of Reaction of Fluorescein Isothiocyanate with Serum Proteins. J. Immunol. 1964, 93, 232-242.
54. Griffith, O. H.; McConnell, H. M. A Nitroxide-Maleimide Spin Label. Proc. Natl. Acad. Sci. U.S.A. 1966, 55, 8-11.
55. 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.
56. Klare, J. P.; Steinhoff, H.-J. Spin Labelling EPR. Photosynth. Res. 2009, 102, 377-390.
57. Nesmelov, Y. E.; Thomas, D. D. Protein Structural Dynamics Revealed by Site-Directed Spin Labeling and Multifrequency EPR. Biophys. Rev. 2010, 2, 91-99.
58. Štrancar, J. In ESR Spectroscopy in Membrane Biophysics; Hemminga, M. A., Berliner, L. J., Eds.; Springer Science: New York, 2007; Chapter 3, pp 49-93.
59. Stopar, D.; Štrancar, J.; Spruijt, R. B.; Hemminga, M. A. Motional Restrictions of Membrane Proteins: A Site-Directed Spin Labeling Study. Biophy. J. 2006, 91, 3341-3348.
60. Štrancar, J.; Kavalenka, A.; Urbančič, I.; Ljubetič, A.; Hemminga, M. A. SDSL-ESR-Based Protein Structure Characterization. Eur. Biophys. J. 2010, 39, 499-511.
61. Kavalenka, A.; Urbančič, I.; Belle, V.; Rouger, S.; Constanzo, S.; Kure, S.; Fournel, A.; Longhi, S.; Guigliarelli, B.; Štrancar, J. Conformational Analysis of the Partially Disordered Measles Virus NTAIL-XD Complex by SDSL EPR Spectroscopy. Biophys. J. 2010, 98, 1055-1064.
62. Schmidt, A.; Gaul, L. In Proceedings of the International Model Analysis Conference; Society for Experimental Mechanics, Bethel, 2008; Vol. 3, pp 1557-1566.
63. Banks, H. T.; Hu, S.; Kenz, Z. R. A Brief Review of Elasticity and Viscoelasticity for Solids. J. Appl. Math. Mech. 2011, 3, 1-51.
64. Page, B.; Page, M.; Noel, C. A New Fluorometric Assay for Cytotoxicity Measurements In-Vitro. Int. J. Oncol. 1993, 3, 473-476.
65. Sengers, B. G.; Taylor, M.; Please, C. P.; Oreffo, R. O. C. Computational Modelling of Cell Spreading and Tissue Regeneration in Porous Scaffolds. Biomaterials 2007, 28, 1926-1940.
66. Sung, H. J.; Meredith, C.; Johnson, C.; Galis, Z. S. The Effect of Scaffold Degradation Rate on Three-Dimensional Cell Growth and Angiogenesis. Biomaterials 2004, 25, 5735-5742.
67. Karamichos, D.; Brown, R. A.; Mudera, V. Collagen Stiffness Regulates Cellular Contraction and Matrix Remodeling Gene Expression. J. Biomed. Mater. Res., Part A 2007, 83, 887-894.