Characterizing the micro-scale elastic modulus of hydrogels for use in regenerative medicine

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 27, Issue , 2013, Pages 115-127

  Markert, Chad D ^a   Guo, Xinyi ^b   Skardal, Aleksander ^a   Wang, Zhan ^a   Bharadwaj, Shantaram ^a   Zhang, Yuanyuan ^a   Bonin, Keith ^b   Guthold, Martin ^b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST UNIVERSITY   (United States)

Author keywords

Atomic force microscopy (AFM); Biomaterials; Elastic modulus; Hydrogel; Substrates; Tissue engineering

Indexed keywords

AGAROSE; IN-VIVO; LAMININ; MEASUREMENTS OF; POLYETHYLENE GLYCOL DIACRYLATE; REGENERATIVE MEDICINE; SILICONE ELASTOMERS; YOUNG'S MODULUS;

ATOMIC FORCE MICROSCOPY; BIOCOMPATIBILITY; BIOLOGICAL MATERIALS; BIOMATERIALS; ELASTIC MODULI; ELASTICITY; HYALURONIC ACID; SILICONES; SUBSTRATES; TISSUE ENGINEERING;

HYDROGELS;

AGAROSE; ALGINIC ACID; COLLAGEN; FIBRIN; HYALURONIC ACID; KERATIN; LAMININ; MACROGOL; MATRIGEL; POLYACRYLAMIDE; SILASTIC;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HUMAN; HYDROGEL; IN VIVO STUDY; MANIPULATIVE MEDICINE; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE; YOUNG MODULUS;

ATOMIC FORCE MICROSCOPY (AFM); BIOMATERIALS; ELASTIC MODULUS; HYDROGEL; SUBSTRATES; TISSUE ENGINEERING;

ACRYLIC RESINS; ALGINATES; BIOCOMPATIBLE MATERIALS; COLLAGEN; DRUG COMBINATIONS; ELASTIC MODULUS; FIBRINOGEN; GLUCURONIC ACID; HEXURONIC ACIDS; HYALURONIC ACID; HYDROGELS; LAMININ; MICROSPHERES; POLYETHYLENE GLYCOLS; PROTEOGLYCANS; REGENERATIVE MEDICINE; THROMBIN;

EID: 84884287328     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2013.07.008     Document Type: Article

References (83)

1. Ahearne M., Siamantouras E., Yang Y., Liu K.K. Mechanical characterization of biomimetic membranes by micro-shaft poking. Journal of the Royal Society, Interface 2009, 6:471-478.
2. Ainsworth C. Cell biology: stretching the imagination. Nature 2008, 456:696-699.
3. Anderson D.G., Levenberg S., Langer R. Nanoliter-scale synthesis of arrayed biomaterials and application to human embryonic stem cells. Nature Biotechnology 2004, 22:863-866.
4. Aymard P., Martin D.R., Plucknett K., Foster T.J., Clark A.H., Norton I.T. Influence of thermal history on the structural and mechanical properties of agarose gels. Biopolymers 2001, 59:131-144.
5. Banerjee A., Arha M., Choudhary S., Ashton R.S., Bhatia S.R., Schaffer D.V., Kane R.S. The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials 2009, 30:4695-4699.
6. Bharadwaj S., Liu G., Shi Y., Markert C., Andersson K.E., Atala A., Zhang Y. Characterization of urine-derived stem cells obtained from upper urinary tract for use in cell-based urological tissue engineering. Tissue Engineering Part A 2011, 17:2123-2132.
7. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Physical Review Letters 1986, 56:930-933.
8. Brown X.Q., Ookawa K., Wong J.Y. Evaluation of polydimethylsiloxane scaffolds with physiologically-relevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 2005, 26:3123-3129.
9. Buckley C.T., Thorpe S.D., O'Brien F.J., Robinson A.J., Kelly D.J. The effect of concentration, thermal history and cell seeding density on the initial mechanical properties of agarose hydrogels. Journal of the Mechanical Behavior of Biomedical Materials 2009, 2:512-521.
10. Candiello J., Singh S.S., Task K., Kumta P.N., Banerjee I. Early differentiation patterning of mouse embryonic stem cells in response to variations in alginate substrate stiffness. Journal of Biological Engineering 2013, 7.
11. Carlisle C.R., Coulais C., Namboothiry M., Carroll D.L., Hantgan R.R., Guthold M. The mechanical properties of individual, electrospun fibrinogen fibers. Biomaterials 2009, 30:1205-1213.
12. Cha C., Kim S.Y., Cao L., Kong H. Decoupled control of stiffness and permeability with a cell-encapsulating poly(ethylene glycol) dimethacrylate hydrogel. Biomaterials 2010, 31:4864-4871.
13. Chia H.N., Vigen M., Kasko A.M. Effect of substrate stiffness on pulmonary fibroblast activation by TGF-beta. Acta Biomaterialia 2012, 8:2602-2611.
14. Choi Y.S., Vincent L.G., Lee A.R., Dobke M.K., Engler A.J. Mechanical derivation of functional myotubes from adipose-derived stem cells. Biomaterials 2012, 33:2482-2491.
15. Chowdhury F., Na S., Li D., Poh Y.C., Tanaka T.S., Wang F., Wang N. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nature Materials 2010, 9:82-88.
16. Costa K.D. Single-cell elastography: probing for disease with the atomic force microscope. Disease Markers 2003, 19:139-154.
17. Csete M. Oxygen in the cultivation of stem cells. Annals of the New York Academy of Sciences 2005, 1049:1-8.
18. De Coppi P., Bartsch G., Siddiqui M.M., Xu T., Santos C.C., Perin L., Mostoslavsky G., Serre A.C., Snyder E.Y., Yoo J.J., Furth M.E., Soker S., Atala A. Isolation of amniotic stem cell lines with potential for therapy. Nature Biotechnology 2007, 25:100-106.
19. Dellatore S.M., Garcia A.S., Miller W.M. Mimicking stem cell niches to increase stem cell expansion. Current Opinion in Biotechnology 2008, 19:534-540.
20. Discher D.E., Mooney D.J., Zandstra P.W. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324:1673-1677.
21. Domogatskaya A., Rodin S., Boutaud A., Tryggvason K. Laminin-511 but not -332, -111, or -411 enables mouse embryonic stem cell self-renewal in vitro. Stem Cells 2008, 26:2800-2809.
22. Engler A.J., Griffin M.A., Sen S., Bonnemann C.G., Sweeney H.L., Discher D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. Journal of Cell Biology 2004, 166:877-887.
23. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
24. Estrada J.C., Albo C., Benguria A., Dopazo A., Lopez-Romero P., Carrera-Quintanar L., Roche E., Clemente E.P., Enriquez J.A., Bernad A., Samper E. Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death & Differentiation 2012, 19:743-755.
25. Georges P.C., Miller W.J., Meaney D.F., Sawyer E.S., Janmey P.A. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophysical Journal 2006, 90:3012-3018.
26. Gilbert P.M., Blau H.M. Engineering a stem cell house into a home. Stem Cell Research & Therapy 2011, 2:3.
27. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends in Cell Biology 2003, 13:264-269.
28. Holst J., Watson S., Lord M.S., Eamegdool S.S., Bax D.V., Nivison-Smith L.B., Kondyurin A., Ma L., Oberhauser A.F., Weiss A.S., Rasko J.E. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nature Biotechnology 2010, 28:1123-1128.
29. Janmey P.A., McCulloch C.A. Cell mechanics: integrating cell responses to mechanical stimuli. Annual Review of Biomedical Engineering 2007, 9:1-34.
30. Janmey P.A., Miller R.T. Mechanisms of mechanical signaling in development and disease. Journal of Cell Science 2011, 124:9-18.
31. Justice B.A., Badr N.A., Felder R.A. 3D cell culture opens new dimensions in cell-based assays. Drug Discovery Today 2009, 14:102-107.
32. Kiel M.J., Morrison S.J. Uncertainty in the niches that maintain haematopoietic stem cells. Nature Reviews Immunology 2008, 8:290-301.
33. Kim J., Song H., Park I., Carlisle C.R., Bonin K., Guthold M. Denaturing of single electrospun fibrinogen fibers studied by deep ultraviolet fluorescence microscopy. Microscopy Research and Technique 2010, 74:219-224.
34. Kloxin A.M., Kloxin C.J., Bowman C.N., Anseth K.S. Mechanical properties of cellularly responsive hydrogels and their experimental determination. Advanced Materials 2010, 22:3484-3494.
35. Kloxin A.M., Tibbitt M.W., Kasko A.M., Fairbairn J.A., Anseth K.S. Tunable hydrogels for external manipulation of cellular microenvironments through controlled photodegradation. Advanced Materials 2010, 22:61-66.
36. Kuhn N.Z., Tuan R.S. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. Journal of Cellular Physiology 2010, 222:268-277.
37. Kuraitis D., Giordano C., Ruel M., Musaro A., Suuronen E.J. Exploiting extracellular matrix-stem cell interactions: a review of natural materials for therapeutic muscle regeneration. Biomaterials 2012, 33:428-443.
38. Lander A.D., Kimble J., Clevers H., Fuchs E., Montarras D., Buckingham M., Calof A.L., Trumpp A., Oskarsson T. What does the concept of the stem cell niche really mean today?. BMC Biology 2012, 10:19.
39. Lawyer T., McIntosh K., Clavijo C., Potekhina L., Mann B.K. Formulation changes affect material properties and cell behavior in HA-based hydrogels. International Journal of Cell Biology 2012, 9. 10.1155/2012/737421.
40. Lee K.Y., Mooney D.J. Alginate: properties and biomedical applications. Progress in Polymer Science 2012, 37:106-126.
41. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327:542-545.
42. 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 Biomaterialia 2008, 4:1161-1171.
43. Liu W., Bonin K., Guthold M. An easy and direct method for calibrating AFM lateral force measurements. Review of Scientific Instruments 2007, 78:063707.
44. Liu W., Jawerth L.M., Sparks E.A., Falvo M.R., Hantgan R.R., Superfine R., Lord S.T., Guthold M. Fibrin fibers have extraordinary extensibility and elasticity. Science 2006, 313:634.
45. Ludwig T.E., Levenstein M.E., Jones J.M., Berggren W.T., Mitchen E.R., Frane J.L., Crandall L.J., Daigh C.A., Conard K.R., Piekarczyk M.S., Llanas R.A., Thomson J.A. Derivation of human embryonic stem cells in defined conditions. Nature Biotechnology 2006, 24:185-187.
46. Markert C.D., Bharadwaj S., Zhang Y., Childers M.K., Furth M.E. Immunofluorescence microscopy for imaging of nuclear p63 in human primary keratinocytes: a comparison of antibodies and fixation methods. Journal of Immunological Methods 2010, 352:174-177.
47. Moore S.W., Roca-Cusachs P., Sheetz M.P. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Developmental Cell 2010, 19:194-206.
48. Murphy, K.C., Leach, J., 2012. A reproducible, high throughput method for fabricating fibrin gels. BMC Research Notes 2012, 5:423 (8 August 2012) 5, (4 pages).
49. Nemir S., Hayenga H.N., West J.L. PEGDA hydrogels with patterned elasticity: novel tools for the study of cell response to substrate rigidity. Biotechnology and Bioengineering 2010, 105:636-644.
50. Ng K.W., Wang C.C.B., Mauck R.L., Kelly T.A.N., Chahine N.O., Costa K.D., Ateshian G.A., Hung C.T. A layered agarose approach to fabricate depth-dependent inhomogeneity in chondrocyte-seeded constructs. Journal of Orthopaedic Research 2005, 23:134-141.
51. Normand V., Lootens D.L., Amici E., Plucknett K.P., Aymard P. New insight into agarose gel mechanical properties. Biomacromolecules 2000, 1:730-738.
52. Ocalan M., Goodman S.L., Kuhl U., Hauschka S.D., von der Mark K. Laminin alters cell shape and stimulates motility and proliferation of murine skeletal myoblasts. Developmental Biology 1988, 125:158-167.
53. Ouasti S., Donno R., Cellesi F., Sherratt M.J., Terenghi G., Tirelli N. Network connectivity, mechanical properties and cell adhesion for hyaluronic acid/PEG hydrogels. Biomaterials 2011, 32:6456-6470.
54. Park, S.-J., Goodman, M.B., Pruitt, B.L., 2005. Measurement of mechanical properties of Caenorhabditis elegans with a piezoresistive microcantilever system. In: Third IEEE/EMBS Special Topic Conference on Microtechnology in Medicine and Biology. Piscataway, NJ: IEEE, Oahu, HI, p. http://dx.doi.org/10.1109/MMB.2005.1548488.
55. Park S., Costa K.D., Ateshian G.A., Hong K.S. Mechanical properties of bovine articular cartilage under microscale indentation loading from atomic force microscopy. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine 2009, 223:339-347.
56. Park S., Duong C.T., Lee J.H., Lee S.S., Son K. Effect of tip geometry of atomic force microscope on mechanical responses of bovine articular cartilage and agarose gel. International Journal of Precision Engineering and Manufacturing 2010, 11:129-136.
57. Patel P.N., Smith C.K., Patrick C.W. Rheological and recovery properties of poly(ethylene glycol) diacrylate hydrogels and human adipose tissue. Journal of Biomedial Materials Research Part A 2005, 73:313-319.
58. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:13661-13665.
59. Peng L., Stephens B.J., Bonin K., Cubicciotti R., Guthold M. A combined atomic force/fluorescence microscopy technique to select aptamers in a single cycle from a small pool of random oligonucleotides. Microscopy Research and Technique 2007, 70:372-381.
60. Prestwich G.D. Simplifying the extracellular matrix for 3-D cell culture and tissue engineering: a pragmatic approach. Journal of Cellular Biochemistry 2007, 101:1370-1383.
61. Rehfeldt F., Engler A.J., Eckhardt A., Ahmed F., Discher D.E. Cell responses to the mechanochemical microenvironment-implications for regenerative medicine and drug delivery. Advanced Drug Delivery Reviews 2007, 59:1329-1339.
62. Richert L., Engler A.J., Discher D.E., Picart C. Elasticity of native and cross-linked polyelectrolyte multilayer films. Biomacromolecules 2004, 5:1908-1916.
63. Roeder I., Loeffler M., Glauche I. Towards a quantitative understanding of stem cell-niche interaction: experiments, models, and technologies. Blood Cells, Molecules and Diseases 2011, 46:308-317.
64. Roth E.A., Xu T., Das M., Gregory C., Hickman J.J., Boland T. Inkjet printing for high-throughput cell patterning. Biomaterials 2004, 25:3707-3715.
65. Sader J.E., Larson I., Mulvaney P., White L.R. Method for the calibration of atomic-force microscope cantilevers. Review of Scientific Instruments 1995, 66:3789-3798.
66. Salerno M., Dante S., Patra N., Diaspro A. AFM measurement of the stiffness of layers of agarose gel patterned with polylysine. Microscopy Research and Technique 2010, 73:982-990.
67. Scadden D.T. The stem-cell niche as an entity of action. Nature 2006, 441:1075-1079.
68. Semler E.J., Moghe P.V. Engineering hepatocyte functional fate through growth factor dynamics: the role of cell morphologic priming. Biotechnology and Bioengineering 2001, 75:510-520.
69. Shu X.Z., Liu Y.C., Luo Y., Roberts M.C., Prestwich G.D. Disulfide cross-linked hyaluronan hydrogels. Biomacromolecules 2002, 3:1304-1311.
70. Skardal A., Sarker S.F., Crabbe A., Nickerson C.A., Prestwich G.D. The generation of 3-D tissue models based on hyaluronan hydrogel-coated microcarriers within a rotating wall vessel bioreactor. Biomaterials 2010, 31:8426-8435.
71. Skardal A., Zhang J., McCoard L., Oottamasathien S., Prestwich G.D. Dynamically crosslinked gold nanoparticle-hyaluronan hydrogels. Advanced Materials 2010, 22:4736-4740.
72. Skardal A., Zhang J., McCoard L., Xu X., Oottamasathien S., Prestwich G.D. Photocrosslinkable hyaluronan-gelatin hydrogels for two-step bioprinting. Tissue Engineering Part A 2010, 16:2675-2685.
73. Skardal A., Zhang J., Prestwich G.D. Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates. Biomaterials 2010, 31:6173-6181.
74. Stephens B.J. Construction and Application of a Combined AFM/FM (with TIRF), Dept. of Physics 2005, Wake Forest University, Winston-Salem.
75. Stolz M., Raiteri R., Daniels A.U., VanLandingham M.R., Baschong W., Aebi U. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophysical Journal 2004, 86:3269-3283.
76. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:1484-1489.
77. Unger C., Skottman H., Blomberg P., Dilber M.S., Hovatta O. Good manufacturing practice and clinical-grade human embryonic stem cell lines. Human Molecular Genetics 2008, 17:R48-R53.
78. Vanderhooft J.L., Alcoutlabi M., Magda J.J., Prestwich G.D. Rheological properties of cross-linked hyaluronan-gelatin hydrogels for tissue engineering. Macromolecular Bioscience 2009, 9:20-28.
79. Varghese D., Deshpande M., Xu T., Kesari P., Ohri S., Boland T. Advances in tissue engineering: cell printing. The Journal of Thoracic and Cardiovascular Surgery 2005, 129:470-472.
80. Xu T., Gregory C.A., Molnar P., Cui X., Jalota S., Bhaduri S.B., Boland T. Viability and electrophysiology of neural cell structures generated by the inkjet printing method. Biomaterials 2006, 27:3580-3588.
81. Xu T., Jin J., Gregory C., Hickman J.J., Boland T. Inkjet printing of viable mammalian cells. Biomaterials 2005, 26:93-99.
82. Yang Y., Bagnaninchi P.O., Ahearne M., Wang R.K., Liu K.K. A novel optical coherence tomography-based micro-indentation technique for mechanical characterization of hydrogels. Journal of the Royal Society, Interface 2007, 4:1169-1173.
83. Zhu J., Tang C., Kottke-Marchant K., Marchant R.E. Design and synthesis of biomimetic hydrogel scaffolds with controlled organization of cyclic RGD peptides. Bioconjugate Chemistry 2009, 20:333-339.