Nonlinear Behavior of Gelatin Networks Reveals a Hierarchical Structure

Biomacromolecules

Volumn 17, Issue 2, 2016, Pages 590-600

  Yang, Zhi ^a   Hemar, Yacine ^a,e,f   Hilliou, Loic ^c   Gilbert, Elliot P ^d   McGillivray, Duncan J ^a,e,g   Williams, Martin A K ^e,f,g   Chaieb, Sahraoui ^b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSITY OF MINHO   (Portugal)

^d AUSTRALIAN NUCLEAR SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^e MASSEY UNIVERSITY   (New Zealand)

^f RIDDET INSTITUTE   (New Zealand)

^g MacDiarmid Institute for AdVanced Materials Nanotechnology   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; FRACTAL DIMENSION; FRACTALS; GELS; NEUTRON SCATTERING; STRAIN HARDENING; STRESS-STRAIN CURVES;

CHEMICAL CROSS-LINKING; CROSS-LINKED GELATINS; CROSS-LINKED NETWORKS; HIERARCHICAL STRUCTURES; HOMOGENEOUS STRUCTURE; LARGE AMPLITUDE OSCILLATION; STRAIN HARDENING BEHAVIOR; STRUCTURAL PARAMETER;

CROSSLINKING;

GELATIN; POLYMER;

ARTICLE; CHEMICAL STRUCTURE; CROSS LINKING; FLOW KINETICS; GEL; GELATION; NEUTRON SCATTERING; NONLINEAR SYSTEM; OSCILLATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TEMPERATURE; ANIMAL; CHEMISTRY; MOLECULAR MODEL; NEUTRON DIFFRACTION; PIG; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; SHEAR STRENGTH; SMALL ANGLE SCATTERING; YOUNG MODULUS;

ANIMALS; ELASTIC MODULUS; GELATIN; MODELS, MOLECULAR; NEUTRON DIFFRACTION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SCATTERING, SMALL ANGLE; SHEAR STRENGTH; SUS SCROFA;

EID: 84957824920     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.5b01538     Document Type: Article

References (69)

1. Kuijpers, A. J.; Engbers, G. H. M.; Feijen, J.; De Smedt, S. C.; Meyvis, T. K. L.; Demeester, J.; Krijgsveld, J.; Zaat, S. A. J.; Dankert, J. Characterization of the Network Structure of Carbodiimide Cross-Linked Gelatin Gels Macromolecules 1999, 32 (10) 3325-3333 10.1021/ma981929v
2. Fan, H.; Dash, A. K. Effect of cross-linking on the in vitro release kinetics of doxorubicin from gelatin implants Int. J. Pharm. 2001, 213 (1) 103-116 10.1016/S0378-5173(00)00651-7
3. Kang, H.-W.; Tabata, Y.; Ikada, Y. Fabrication of porous gelatin scaffolds for tissue engineering Biomaterials 1999, 20 (14) 1339-1344 10.1016/S0142-9612(99)00036-8
4. Guo, L.; Colby, R. H.; Lusignan, C. P.; Whitesides, T. H. Kinetics of Triple Helix Formation in Semidilute Gelatin Solutions Macromolecules 2003, 36 (26) 9999-10008 10.1021/ma034264s
5. Guo, L.; Colby, R. H.; Lusignan, C. P.; Howe, A. M. Physical gelation of gelatin studied with rheo-optics Macromolecules 2003, 36 (26) 10009-10020 10.1021/ma034266c
6. Djabourov, M. Architecture of gelatin gels Contemp. Phys. 1988, 29 (3) 273-297 10.1080/00107518808224377
7. Babin, H.; Dickinson, E. Influence of transglutaminase treatment on the thermoreversible gelation of gelatin Food Hydrocolloids 2001, 15 (3) 271-276 10.1016/S0268-005X(01)00025-X
8. Mohtar, N. F.; Perera, C. O.; Quek, S.-Y.; Hemar, Y. Optimization of gelatin gel preparation from New Zealand hoki (Macruronus novaezelandiae) skins and the effect of transglutaminase enzyme on the gel properties Food Hydrocolloids 2013, 31 (2) 204-209 10.1016/j.foodhyd.2012.10.011
9. Chiou, B.-S.; Avena-Bustillos, R. J.; Shey, J.; Yee, E.; Bechtel, P. J.; Imam, S. H.; Glenn, G. M.; Orts, W. J. Rheological and mechanical properties of cross-linked fish gelatins Polymer 2006, 47 (18) 6379-6386 10.1016/j.polymer.2006.07.004
10. Zhang, X.; Do, M. D.; Casey, P.; Sulistio, A.; Qiao, G. G.; Lundin, L.; Lillford, P.; Kosaraju, S. Chemical cross-linking gelatin with natural phenolic compounds as studied by high-resolution NMR spectroscopy Biomacromolecules 2010, 11 (4) 1125-1132 10.1021/bm1001284
11. Kosaraju, S. L.; Puvanenthiran, A.; Lillford, P. Naturally crosslinked gelatin gels with modified material properties Food Res. Int. 2010, 43 (10) 2385-2389 10.1016/j.foodres.2010.09.008
12. Hellio-Serughetti, D.; Djabourov, M. Gelatin hydrogels cross-linked with bis (vinylsulfonyl) methane (BVSM): 1. The chemical networks Langmuir 2006, 22 (20) 8509-8515 10.1021/la060375j
13. Kirchmajer, D. M.; Watson, C. A.; Ranson, M.; in het Panhuis, M. Gelapin, a degradable genipin cross-linked gelatin hydrogel RSC Adv. 2013, 3 (4) 1073-1081 10.1039/C2RA22859A
14. Bigi, A.; Cojazzi, G.; Panzavolta, S.; Roveri, N.; Rubini, K. Stabilization of gelatin films by crosslinking with genipin Biomaterials 2002, 23 (24) 4827-4832 10.1016/S0142-9612(02)00235-1
15. Liang, H. C.; Chang, W. H.; Liang, H. F.; Lee, M. H.; Sung, H. W. Crosslinking structures of gelatin hydrogels crosslinked with genipin or a water-soluble carbodiimide J. Appl. Polym. Sci. 2004, 91 (6) 4017-4026 10.1002/app.13563
16. Bode, F.; da Silva, M. A.; Smith, P.; Lorenz, C. D.; McCullen, S.; Stevens, M. M.; Dreiss, C. A. Hybrid gelation processes in enzymatically gelled gelatin: impact on nanostructure, macroscopic properties and cellular response Soft Matter 2013, 9 (29) 6986-6999 10.1039/C3SM00125C
17. Bode, F.; da Silva, M. A.; Drake, A. F.; Ross-Murphy, S. B.; Dreiss, C. A. Enzymatically cross-linked tilapia gelatin hydrogels: physical, chemical, and hybrid networks Biomacromolecules 2011, 12 (10) 3741-3752 10.1021/bm2009894
18. Kaieda, S.; Plivelic, T. S.; Halle, B. Structure and kinetics of chemically cross-linked protein gels from small-angle X-ray scattering Phys. Chem. Chem. Phys. 2014, 16 (9) 4002-4011 10.1039/c3cp54219j
19. Groot, R. D.; Bot, A.; Agterof, W. G. Molecular theory of strain hardening of a polymer gel: application to gelatin J. Chem. Phys. 1996, 104 (22) 9202-9219 10.1063/1.471611
20. Joly-Duhamel, C.; Hellio, D.; Ajdari, A.; Djabourov, M. All gelatin networks: 2. The master curve for elasticity Langmuir 2002, 18 (19) 7158-7166 10.1021/la020190m
21. Groot, R. D.; Bot, A.; Agterof, W. G. Molecular theory of the yield behavior of a polymer gel: application to gelatin J. Chem. Phys. 1996, 104 (22) 9220-9233 10.1063/1.471612
22. Jensen, M. H.; Morris, E. J.; Gallant, C. M.; Morgan, K. G.; Weitz, D. A.; Moore, J. R. Mechanism of Calponin Stabilization of Cross-Linked Actin Networks Biophys. J. 2014, 106 (4) 793-800 10.1016/j.bpj.2013.12.042
23. Lieleg, O.; Claessens, M. M.; Bausch, A. R. Structure and dynamics of cross-linked actin networks Soft Matter 2010, 6 (2) 218-225 10.1039/B912163N
24. Gilbert, E. P.; Schulz, J. C.; Noakes, T. J. 'Quokka'-the small-angle neutron scattering instrument at OPAL Phys. B 2006, 385, 1180-1182 10.1016/j.physb.2006.05.385
25. Joly-Duhamel, C.; Hellio, D.; Djabourov, M. All gelatin networks: 1. Biodiversity and physical chemistry Langmuir 2002, 18 (19) 7208-7217 10.1021/la020189n
26. Ronsin, O.; Caroli, C.; Baumberger, T. Interplay between Shear Loading and Structural Aging in a Physical Gelatin Gel Phys. Rev. Lett. 2009, 103 (13) 138302 10.1103/PhysRevLett.103.138302
27. Farris, S.; Song, J.; Huang, Q. Alternative Reaction Mechanism for the Cross-Linking of Gelatin with Glutaraldehyde J. Agric. Food Chem. 2010, 58 (2) 998-1003 10.1021/jf9031603
28. Mohtar, N. F.; Perera, C. O.; Hemar, Y. Chemical modification of New Zealand hoki (Macruronus novaezelandiae) skin gelatin and its properties Food Chem. 2014, 155 (0) 64-73 10.1016/j.foodchem.2014.01.043
29. Moura, M. J.; Figueiredo, M. M.; Gil, M. H. Rheological Study of Genipin Cross-Linked Chitosan Hydrogels Biomacromolecules 2007, 8 (12) 3823-3829 10.1021/bm700762w
30. Hyun, K.; Wilhelm, M.; Klein, C. O.; Cho, K. S.; Nam, J. G.; Ahn, K. H.; Lee, S. J.; Ewoldt, R. H.; McKinley, G. H. A review of nonlinear oscillatory shear tests: Analysis and application of large amplitude oscillatory shear (LAOS) Prog. Polym. Sci. 2011, 36 (12) 1697-1753 10.1016/j.progpolymsci.2011.02.002
31. Yoshimura, A.; Prud'homme, R. K. Wall slip corrections for Couette and parallel disk viscometers J. Rheol. 1988, 32 (1) 53-67 10.1122/1.549963
32. Wen, Q.; Basu, A.; Janmey, P. A.; Yodh, A. G. Non-affine deformations in polymer hydrogels Soft Matter 2012, 8 (31) 8039-8049 10.1039/c2sm25364j
33. Motte, S.; Kaufman, L. J. Strain stiffening in collagen I networks Biopolymers 2013, 99 (1) 35-46 10.1002/bip.22133
34. Vader, D.; Kabla, A.; Weitz, D.; Mahadevan, L. Strain-induced alignment in collagen gels PLoS One 2009, 4 (6) e5902 10.1371/journal.pone.0005902
35. Sun, W.-x.; Huang, L.-z.; Yang, Y.-r.; Liu, X.-x.; Tong, Z. Large amplitude oscillatory shear studies on the strain-stiffening behavior of gelatin gels Chin. J. Polym. Sci. 2015, 33 (1) 70-83 10.1007/s10118-015-1559-5
36. Haut, R. C.; Little, R. W. A constitutive equation for collagen fibers J. Biomech. 1972, 5 (5) 423-430 10.1016/0021-9290(72)90001-2
37. Pioletti, D. P.; Rakotomanana, L.; Benvenuti, J.-F.; Leyvraz, P.-F. Viscoelastic constitutive law in large deformations: application to human knee ligaments and tendons J. Biomech. 1998, 31 (8) 753-757 10.1016/S0021-9290(98)00077-3
38. Broedersz, C. P.; Kasza, K. E.; Jawerth, L. M.; Münster, S.; Weitz, D. A.; MacKintosh, F. C. Measurement of nonlinear rheology of cross-linked biopolymer gels Soft Matter 2010, 6 (17) 4120-4127 10.1039/c0sm00285b
39. Blatz, P.; Sharda, S. C.; Tschoegl, N. Strain energy function for rubberlike materials based on a generalized measure of strain J. Rheol. (Melville, NY, U. S.) 1974, 18 (1) 145-161 10.1122/1.549353
40. Forte, A. E.; D'Amico, F.; Charalambides, M. N.; Dini, D.; Williams, J. G. Modelling and experimental characterisation of the rate dependent fracture properties of gelatin gels Food Hydrocolloids 2015, 46, 180-190 10.1016/j.foodhyd.2014.12.028
41. van Vliet, T.; Walstra, P. Large deformation and fracture behaviour of gels Faraday Discuss. 1995, 101, 359-370 10.1039/fd9950100359
42. Ross-Murphy, S. B.; Morris, V. J.; Morris, E. R. Molecular Viscoelasticity of Xanthan Polysaccharide Faraday Symp. Chem. Soc. 1983, 18, 115-129 10.1039/FS9831800115
43. McEvoy, H.; Ross-Murphy, S.; Clark, A. Large deformation and ultimate properties of biopolymer gels: 1. Single biopolymer component systems Polymer 1985, 26 (10) 1483-1492 10.1016/0032-3861(85)90081-3
44. Hammouda, B.; Ho, D. L.; Kline, S. Insight into clustering in poly (ethylene oxide) solutions Macromolecules 2004, 37 (18) 6932-6937 10.1021/ma049623d
45. Saffer, E. M.; Lackey, M. A.; Griffin, D. M.; Kishore, S.; Tew, G. N.; Bhatia, S. R. SANS study of highly resilient poly (ethylene glycol) hydrogels Soft Matter 2014, 10 (12) 1905-1916 10.1039/c3sm52395k
46. Karino, T.; Shibayama, M.; Okumura, Y.; Ito, K. SANS study on pulley effect of slide-ring gel Phys. B 2006, 385, 807-809 10.1016/j.physb.2006.06.095
47. Di Lorenzo, F.; Seiffert, S. Nanostructural heterogeneity in polymer networks and gels Polym. Chem. 2015, 6, 5515-5528 10.1039/C4PY01677G
48. Bastide, J.; Leibler, L. Large-scale heterogeneities in randomly cross-linked networks Macromolecules 1988, 21 (8) 2647-2649 10.1021/ma00186a058
49. Helminger, M.; Wu, B.; Kollmann, T.; Benke, D.; Schwahn, D.; Pipich, V.; Faivre, D.; Zahn, D.; Cölfen, H. Synthesis and Characterization of Gelatin-Based Magnetic Hydrogels Adv. Funct. Mater. 2014, 24 (21) 3187-3196 10.1002/adfm.201303547
50. Zhang, J.; Daubert, C. R.; Allen Foegeding, E. A proposed strain-hardening mechanism for alginate gels J. Food Eng. 2007, 80 (1) 157-165 10.1016/j.jfoodeng.2006.04.057
51. Onck, P.; Koeman, T.; Van Dillen, T.; Van der Giessen, E. Alternative explanation of stiffening in cross-linked semiflexible networks Phys. Rev. Lett. 2005, 95 (17) 178102 10.1103/PhysRevLett.95.178102
52. Gardel, M.; Shin, J.; MacKintosh, F.; Mahadevan, L.; Matsudaira, P.; Weitz, D. Elastic behavior of cross-linked and bundled actin networks Science 2004, 304 (5675) 1301-1305 10.1126/science.1095087
53. Piechocka, I. K.; Bacabac, R. G.; Potters, M.; MacKintosh, F. C.; Koenderink, G. H. Structural hierarchy governs fibrin gel mechanics Biophys. J. 2010, 98 (10) 2281-2289 10.1016/j.bpj.2010.01.040
54. Carrillo, J. M. Y.; MacKintosh, F. C.; Dobrynin, A. V. Nonlinear Elasticity: From Single Chain to Networks and Gels Macromolecules 2013, 46 (9) 3679-3692 10.1021/ma400478f
55. Hule, R. A.; Nagarkar, R. P.; Hammouda, B.; Schneider, J. P.; Pochan, D. J. Dependence of Self-Assembled Peptide Hydrogel Network Structure on Local Fibril Nanostructure Macromolecules 2009, 42 (18) 7137-7145 10.1021/ma9003242
56. Hule, R. A.; Nagarkar, R. P.; Altunbas, A.; Ramay, H. R.; Branco, M. C.; Schneider, J. P.; Pochan, D. J. Correlations between structure, material properties and bioproperties in self-assembled [small beta]-hairpin peptide hydrogels Faraday Discuss. 2008, 139 (0) 251-264 10.1039/b717616c
57. Pezron, I.; Djabourov, M.; Leblond, J. Conformation of gelatin chains in aqueous solutions: 1. A light and small-angle neutron scattering study Polymer 1991, 32 (17) 3201-3210 10.1016/0032-3861(91)90143-7
58. Mohanty, B.; Aswal, V. K.; Kohlbrecher, J.; Bohidar, H. B. Length scale hierarchy in sol, gel, and coacervate phases of gelatin J. Polym. Sci., Part B: Polym. Phys. 2006, 44 (12) 1653-1667 10.1002/polb.20783
59. Hule, R. A.; Nagarkar, R. P.; Altunbas, A.; Ramay, H. R.; Branco, M. C.; Schneider, J. P.; Pochan, D. J. Correlations between structure, material properties and bioproperties in self-assembled β-hairpin peptide hydrogels Faraday Discuss. 2008, 139, 251-264 10.1039/b717616c
60. Gelade, E. T.; Goderis, B.; de Koster, C. G.; Meijerink, N.; van Benthem, R. A.; Fokkens, R.; Nibbering, N. M.; Mortensen, K. Molecular structure characterization of hyperbranched polyesteramides Macromolecules 2001, 34 (11) 3552-3558 10.1021/ma001266t
61. da Silva, M. A.; Bode, F.; Grillo, I.; Dreiss, C. c. A. Exploring the Kinetics of Gelation and Final Architecture of Enzymatically Cross-Linked Chitosan/Gelatin Gels Biomacromolecules 2015, 16 (4) 1401-1409 10.1021/acs.biomac.5b00205
62. Daoud, M.; Cotton, J. P.; Farnoux, B.; Jannink, G.; Sarma, G.; Benoit, H.; Duplessix, C.; Picot, C.; de Gennes, P. G. Solutions of Flexible Polymers. Neutron Experiments and Interpretation Macromolecules 1975, 8 (6) 804-818 10.1021/ma60048a024
63. Schmidt, P. W. Small-angle scattering studies of disordered, porous and fractal systems J. Appl. Crystallogr. 1991, 24 (5) 414-435 10.1107/S0021889891003400
64. Santinath Singh, S.; Aswal, V.; Bohidar, H. Internal structures of agar-gelatin co-hydrogels by light scattering, small-angle neutron scattering and rheology Eur. Phys. J. E: Soft Matter Biol. Phys. 2011, 34 (6) 62 10.1140/epje/i2011-11062-3
65. Chaieb, S. Elasto-plasticity in wrinkled polymerized lipid membranes Sci. Rep. 2014, 4, 3699 10.1038/srep03699
66. Manley, S.; Cipelletti, L.; Trappe, V.; Bailey, A. E.; Christianson, R. J.; Gasser, U.; Prasad, V.; Segre, P. N.; Doherty, M. P.; Sankaran, S.; Jankovsky, A. L.; Shiley, B.; Bowen, J.; Eggers, J.; Kurta, C.; Lorik, T.; Weitz, D. A. Limits to Gelation in Colloidal Aggregation Phys. Rev. Lett. 2004, 93 (10) 108302 10.1103/PhysRevLett.93.108302
67. Pezron, I.; Herning, T.; Djabourov, M.; Leblond, J. In Physical Networks-Polymers and Gels; Burchard, W.; Ross-Murphy, S. B., Eds.; Elsevier: London, 1990; p 231.
68. Hammouda, B. Probing nanoscale structures-The SANS toolbox; 2010.
69. Bruîlet, A.; Lairez, D.; Lapp, A.; Cotton, J. P. Improvement of data treatment in small-angle neutron scattering J. Appl. Crystallogr. 2007, 40 (1) 165-177 10.1107/S0021889806051442