Three-Dimensional Cell Entrapment as a Function of the Weight Percent of Peptide-Amphiphile Hydrogels

Langmuir

Volumn 31, Issue 22, 2015, Pages 6122-6129

  Scott, Carolyn M ^a   Forster, Colleen L ^b   Kokkoli, Efrosini ^a  

^a University of Minnesota   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHILES; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; BIOMIMETICS; CELL CULTURE; CELL PROLIFERATION; CELLS; CYTOLOGY; ELASTIC MODULI; GELATION; GELS; HYDROGELS; MOBILE SECURITY; NANOFIBERS; PEPTIDES; STIFFNESS MATRIX; TISSUE ENGINEERING;

CELLULAR RESPONSE; GELATION KINETICS; NANO-FIBER STRUCTURE; NANOFIBER SCAFFOLD; NATIVE EXTRACELLULAR MATRIX; PEPTIDE AMPHIPHILES; THREE-DIMENSIONAL (3D) ENVIRONMENTS; TWO DIMENSIONAL (2 D);

SCAFFOLDS (BIOLOGY);

HYDROGEL; PEPTIDE; SURFACTANT;

3T3 CELL LINE; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; EXTRACELLULAR MATRIX; FIBROBLAST; HYDROGEL; METABOLISM; MOLECULAR WEIGHT; MOUSE; YOUNG MODULUS;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ELASTIC MODULUS; EXTRACELLULAR MATRIX; FIBROBLASTS; HYDROGELS; MICE; MOLECULAR WEIGHT; NIH 3T3 CELLS; PEPTIDES; SURFACE-ACTIVE AGENTS;

EID: 84931281694     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/acs.langmuir.5b00196     Document Type: Article

References (63)

1. Ma, Z.; Kotaki, M.; Inai, R.; Ramakrishna, S. Potential of Nanofiber Matrix as Tissue-Engineering Scaffolds Tissue Eng. 2005, 11, 101-109
2. Chen, M.; Patra, P. K.; Warner, S. B.; Bhowmick, S. Role of Fiber Diameter in Adhesion and Proliferation of NIH 3T3 Fibroblast on Electrospun Polycaprolactone Scaffolds Tissue Eng. 2007, 13, 579-587
3. Badami, A. S.; Kreke, M. R.; Thompson, M. S.; Riffle, J. S.; Goldstein, A. S. Effect of Fiber Diameter on Spreading, Proliferation, and Differentiation of Osteoblastic Cells on Electrospun Poly(lactic Acid) Substrates Biomaterials 2006, 27, 596-606
4. Flemming, R. G.; Murphy, C. J.; Abrams, G. A.; Goodman, S. L.; Nealey, P. F. Effects of Synthetic Micro- and Nano-Structured Surfaces on Cell Behavior Biomaterials 1999, 20, 573-588
5. Cukierman, E.; Pankov, R.; Stevens, D. R.; Yamada, K. M. Taking Cell-Matrix Adhesions to the Third Dimension Science 2001, 294, 1708-1712
6. Gluck, J. M.; Delman, C.; Full, S.; Shemin, R. J.; Heydarkhan-Hagvall, S. Stem Cell Extracellular Matrix Interactions in Three- Dimensional System via Integrins J. Regen. Med. 2013, 2, 1000107
7. Birgersdotter, A.; Sandberg, R.; Ernberg, I. Gene Expression Perturbation in Vitro-A Growing Case for Three-Dimensional (3D) Culture Systems Semin. Cancer Biol. 2005, 15, 405-412
8. Yokoi, H.; Kinoshita, T.; Zhang, S. Dynamic Reassembly of Peptide RADA16 Nanofiber Scaffold Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 8414-8419
9. Kleinman, H. K.; Martin, G. R. Matrigel: Basement Membrane Matrix with Biological Activity Semin. Cancer Biol. 2005, 15, 378-386
10. Anderson, S. B.; Lin, C.-C.; Kuntzler, D. V.; Anseth, K. S. The Performance of Human Mesenchymal Stem Cells Encapsulated in Cell-Degradable Polymer-Peptide Hydrogels Biomaterials 2011, 32, 3564-3574
11. Salinas, C. N.; Anseth, K. S. The Enhancement of Chondrogenic Differentiation of Human Mesenchymal Stem Cells by Enzymatically Regulated RGD Functionalities Biomaterials 2008, 29, 2370-2377
12. Kokkoli, E.; Mardilovich, A.; Wedekind, A.; Rexeisen, E. L.; Garg, A.; Craig, J. A. Self-Assembly and Applications of Biomimetic and Bioactive Peptide-Amphiphiles Soft Matter 2006, 2, 1015-1024
13. Galler, K. M.; Cavender, A.; Yuwono, V.; Dong, H.; Shi, S.; Ph, D.; Schmalz, G.; Hartgerink, J. D.; Souza, R. N. D. Self-Assembling Peptide Amphiphile Nanofibers as a Scaffold for Dental Stem Cells Tissue Eng., Part A 2008, 14, 2051-2058
14. Galler, K. M.; Aulisa, L.; Regan, K. R.; D'Souza, R. N.; Hartgerink, J. D. Self-Assembling Multidomain Peptide Hydrogels: Designed Susceptibility to Enzymatic Cleavage Allows Enhanced Cell Migration and Spreading J. Am. Chem. Soc. 2010, 132, 3217-3223
15. Anderson, J. M.; Kushwaha, M.; Tambralli, A.; Bellis, S. L.; Camata, R. P.; Jun, H.-W. Osteogenic Differentiation of Human Mesenchymal Stem Cells Directed by Extracellular Matrix-Mimicking Ligands in a Biomimetic Self-Assembled Peptide Amphiphile Nanomatrix Biomacromolecules 2009, 10, 2935-2944
16. Hosseinkhani, H.; Hosseinkhani, M.; Tian, F.; Kobayashi, H.; Tabata, Y. Osteogenic Differentiation of Mesenchymal Stem Cells in Self-Assembled Peptide-Amphiphile Nanofibers Biomaterials 2006, 27, 4079-4086
17. Hosseinkhani, H.; Hosseinkhani, M.; Kobayashi, H. Proliferation and Differentiation of Mesenchymal Stem Cells Using Self-Assembled Peptide Amphiphile Nanofibers Biomed. Mater. 2006, 1, 8-15
18. Silva, G. A.; Czeisler, C.; Niece, K. L.; Beniash, E.; Harrington, D. A.; Kessler, J. A.; Stupp, S. I. Selective Differentiation of Neural Progenitor Cells by High-Epitope Density Nanofibers Science 2004, 303, 1352-1355
19. Tysseling-Mattiace, V. M.; Sahni, V.; Niece, K. L.; Birch, D.; Czeisler, C.; Fehlings, M. G.; Stupp, S. I.; Kessler, J. A. Self-Assembling Nanofibers Inhibit Glial Scar Formation and Promote Axon Elongation after Spinal Cord Injury J. Neurosci. 2008, 28, 3814-3823
20. Sur, S.; Pashuck, E. T.; Guler, M. O.; Ito, M.; Stupp, S. I.; Launey, T. A Hybrid Nanofiber Matrix to Control the Survival and Maturation of Brain Neurons Biomaterials 2012, 33, 545-555
21. Shah, R. N.; Shah, N. A.; Del Rosario Lim, M. M.; Hsieh, C.; Nuber, G.; Stupp, S. I. Supramolecular Design of Self-Assembling Nanofibers for Cartilage Regeneration Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 3293-3298
22. Lim, D.-J.; Antipenko, S. V.; Vines, J. B.; Andukuri, A.; Hwang, P. T. J.; Hadley, N. T.; Rahman, S. M.; Corbett, J. A.; Jun, H.-W. Improved MIN6 B-Cell Function on Self-Assembled Peptide Amphiphile Nanomatrix Inscribed with Extracellular Matrix-Derived Cell Adhesive Ligands Macromol. Biosci. 2013, 13, 1404-1412
23. Stendahl, J. C.; Wang, L.-J.; Chow, L. W.; Kaufman, D. B.; Stupp, S. I. Growth Factor Delivery from Self-Assembling Nanofibers to Facilitate Islet Transplantation Transplantation 2008, 86, 478-481
24. Ghanaati, S.; Webber, M. J.; Unger, R. E.; Orth, C.; Hulvat, J. F.; Kiehna, S. E.; Barbeck, M.; Rasic, A.; Stupp, S. I.; Kirkpatrick, C. J. Dynamic in Vivo Biocompatibility of Angiogenic Peptide Amphiphile Nanofibers Biomaterials 2009, 30, 6202-6212
25. Beniash, E.; Hartgerink, J. D.; Storrie, H.; Stendahl, J. C.; Stupp, S. I. Self-Assembling Peptide Amphiphile Nanofiber Matrices for Cell Entrapment Acta Biomater. 2005, 1, 387-397
26. Rexeisen, E. L.; Fan, W.; Pangburn, T. O.; Taribagil, R. R.; Bates, F. S.; Lodge, T. P.; Tsapatsis, M.; Kokkoli, E. Self-Assembly of Fibronectin Mimetic Peptide-Amphiphile Nanofibers Langmuir 2010, 26, 1953-1959
27. Mardilovich, A.; Craig, J. A.; McCammon, M. Q.; Garg, A.; Kokkoli, E. Design of a Novel Fibronectin-Mimetic Peptide-Amphiphile for Functionalized Biomaterials Langmuir 2006, 22, 3259-3264
28. Craig, J. A.; Rexeisen, E. L.; Mardilovich, A.; Shroff, K.; Kokkoli, E. Effect of Linker and Spacer on the Design of a Fibronectin-Mimetic Peptide Evaluated via Cell Studies and AFM Adhesion Forces Langmuir 2008, 24, 10282-10292
29. Shroff, K.; Pearce, T. R.; Kokkoli, E. Enhanced Integrin Mediated Signaling and Cell Cycle Progression on Fibronectin Mimetic Peptide Amphiphile Monolayers Langmuir 2012, 28, 1858-1865
30. Shroff, K.; Rexeisen, E. L.; Arunagirinathan, M. A.; Kokkoli, E. Fibronectin-Mimetic Peptide-Amphiphile Nanofiber Gels Support Increased Cell Adhesion and Promote ECM Production Soft Matter 2010, 6, 5064-5072
31. Behanna, H. A.; Donners, J. J. J. M.; Gordon, A. C.; Stupp, S. I. Coassembly of Amphiphiles with Opposite Peptide Polarities into Nanofibers J. Am. Chem. Soc. 2005, 127, 1193-1200
32. Webber, M. J.; Tongers, J.; Renault, M.-A.; Roncalli, J. G.; Losordo, D. W.; Stupp, S. I. Development of Bioactive Peptide Amphiphiles for Therapeutic Cell Delivery Acta Biomater. 2010, 6, 3-11
33. Storrie, H.; Guler, M. O.; Abu-Amara, S. N.; Volberg, T.; Rao, M.; Geiger, B.; Stupp, S. I. Supramolecular Crafting of Cell Adhesion Biomaterials 2007, 28, 4608-4618
34. Sur, S.; Matson, J. B.; Webber, M. J.; Newcomb, C. J.; Stupp, S. I. Photodynamic Control of Bioactivity in a Nanofiber Matrix ACS Nano 2012, 6, 10776-10785
35. Lei, Y.; Gojgini, S.; Lam, J.; Segura, T. The Spreading, Migration and Proliferation of Mouse Mesenchymal Stem Cells Cultured inside Hyaluronic Acid Hydrogels Biomaterials 2011, 32, 39-47
36. Li, Y. J.; Chung, E. H.; Rodriguez, R. T.; Firpo, M. T.; Healy, K. E. Hydrogels as Artificial Matrices for Human Embryonic Stem Cell Self-Renewal J. Biomed. Mater. Res., Part A 2006, 79, 1-5
37. Burdick, J. A.; Anseth, K. S. Photoencapsulation of Osteoblasts in Injectable RGD-Modified PEG Hydrogels for Bone Tissue Engineering Biomaterials 2002, 23, 4315-4323
38. Jung, J. P.; Nagaraj, A. K.; Fox, E. K.; Rudra, J. S.; Devgun, J. M.; Collier, J. H. Co-Assembling Peptides as Defined Matrices for Endothelial Cells Biomaterials 2009, 30, 2400-2410
39. Kamgoué, A.; Ohayon, J.; Tracqui, P. Estimation of Cell Young's Modulus of Adherent Cells Probed by Optical and Magnetic Tweezers: Influence of Cell Thickness and Bead Immersion J. Biomech. Eng. 2007, 129, 523-530
40. Laurent, V. M.; Hénon, S.; Planus, E.; Fodil, R.; Balland, M.; Isabey, D.; Gallet, F. Assessment of Mechanical Properties of Adherent Living Cells by Bead Micromanipulation: Comparison of Magnetic Twisting Cytometry vs Optical Tweezers J. Biomech. Eng. 2002, 124, 408-421
41. Dokukin, M. E.; Guz, N. V.; Sokolov, I. Quantitative Study of the Elastic Modulus of Loosely Attached Cells in AFM Indentation Experiments Biophys. J. 2013, 104, 2123-2131
42. Li, Z.; Guo, X.; Palmer, A. F.; Das, H.; Guan, J. High-Efficiency Matrix Modulus-Induced Cardiac Differentiation of Human Mesenchymal Stem Cells inside a Thermosensitive Hydrogel Acta Biomater. 2012, 8, 3586-3595
43. Almany, L.; Seliktar, D. Biosynthetic Hydrogel Scaffolds Made from Fibrinogen and Polyethylene Glycol for 3D Cell Cultures Biomaterials 2005, 26, 2467-2477
44. Liu, S. Q.; Ee, P. L. R.; Ke, C. Y.; Hedrick, J. L.; Yang, Y. Y. Biodegradable Poly(ethylene Glycol)-Peptide Hydrogels with Well-Defined Structure and Properties for Cell Delivery Biomaterials 2009, 30, 1453-1461
45. 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
46. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689
47. Janmey, P. A.; Miller, R. T. Mechanisms of Mechanical Signaling in Development and Disease J. Cell Sci. 2011, 124, 9-18
48. Wex, C.; Frochlich, M.; Brandstadter, K.; Bruns, C.; Stoll, A. Experimental Analysis of the Mechanical Behavior of the Viscoelastic Porcine Pancreas and Preliminary Case Study on the Human Pancreas J. Mech. Behav. Biomed. Mater. 2015, 41, 199-207
49. Kraning-Rush, C. M.; Carey, S. P.; Califano, J. P.; Smith, B. N.; Reinhart-King, C. A. The Role of the Cytoskeleton in Cellular Force Generation in 2D and 3D Environments Phys. Biol. 2011, 8, 015009
50. 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
51. Raeber, G. P.; Lutolf, M. P.; Hubbell, J. A. Molecularly Engineered PEG Hydrogels: A Novel Model System for Proteolytically Mediated Cell Migration Biophys. J. 2005, 89, 1374-1388
52. Lutolf, M. P.; Lauer-Fields, J. L.; Schmoekel, H. G.; Metters, A. T.; Weber, F. E.; Fields, G. B.; Hubbell, J. A. Synthetic Matrix Metalloproteinase-Sensitive Hydrogels for the Conduction of Tissue Regeneration: Engineering Cell-Invasion Characteristics Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 5413-5418
53. Mandal, B. B.; Kundu, S. C. Cell Proliferation and Migration in Silk Fibroin 3D Scaffolds Biomaterials 2009, 30, 2956-2965
54. Bott, K.; Upton, Z.; Schrobback, K.; Ehrbar, M.; Hubbell, J. A.; Lutolf, M. P.; Rizzi, S. C. The Effect of Matrix Characteristics on Fibroblast Proliferation in 3D Gels Biomaterials 2010, 31, 8454-8464
55. Friedl, P.; Bröcker, E. B. The Biology of Cell Locomotion within Three-Dimensional Extracellular Matrix Cell. Mol. Life Sci. 2000, 57, 41-64
56. Halter, M.; Tona, A.; Bhadriraju, K.; Plant, A. L.; Elliott, J. T. Automated Live Cell Imaging of Green Fluorescent Protein Degradation in Individual Fibroblasts Cytometry A 2007, 71, 827-834
57. Strebel, A.; Harr, T.; Bachmann, F.; Wernli, M.; Erb, P. Green Fluorescent Protein as a Novel Tool to Measure Apoptosis and Necrosis Cytometry 2001, 43, 126-133
58. Steff, A.; Arguin, C.; Hugo, P. Detection of a Decrease in Green Fluorescent Protein Fluorescence for the Monitoring of Cell Death: An Assay Amenable to High-Throughput Screening Technologies Cytometry 2001, 243, 237-243
59. Liao, H.; Munoz-Pinto, D.; Qu, X.; Hou, Y.; Grunlan, M. A.; Hahn, M. S. Influence of Hydrogel Mechanical Properties and Mesh Size on Vocal Fold Fibroblast Extracellular Matrix Production and Phenotype Acta Biomater. 2008, 4, 1161-1171
60. Jeong, C. G.; Hollister, S. J. Mechanical and Biochemical Assessments of Three-Dimensional Poly(1,8-Octanediol- co -Citrate) Scaffold Pore Shape and Permeability Effects on In Vitro Chondrogenesis Using Primary Chondrocytes Tissue Eng., Part A 2010, 16, 3759-3768
61. Bryant, S. J.; Anseth, K. S. Hydrogel Properties Influence ECM Production by Chondrocytes Photoencapsulated in Poly (Ethylene Glycol) Hydrogels J. Biomed. Mater. Res. 2001, 59, 63-72
62. Lamande, S. R.; Sigalas, E.; Pan, T. C.; Chu, M. L.; Dziadek, M.; Timpl, R.; Bateman, J. F. The Role of the α3(VI) Chain in Collagen VI Assembly. Expression of an α3(VI) Chain Lacking N-Terminal Modules N10-N7 Restores Collagen VI Assembly, Secretion, and Matrix Deposition in an α3(VI)-Deficient Cell Line J. Biol. Chem. 1998, 273, 7423-7430
63. Hatamochis, A.; Mauch, C.; Chull, M.; Timplg, R.; Krieg, T. Regulation of Collagen VI Expression in Fibroblasts J. Biol. Chem. 1989, 264, 3494-3499