10.1007/s40204-020-00141-4

Nanoscale mechanical properties of chitosan hydrogels as revealed by AFM

  • A. Ben Bouali1,
  • A. Montembault2,
  • L. David2,
  • Y. Von Boxberg3,
  • M. Viallon2,
  • B. Hamdi4,
  • F. Nothias3,
  • R. Fodil5,
  • S. Féréol*5,
  1. Univ Paris Est Creteil, INSERM, IMRB, Creteil, F-94010, FR CNRS UMR 8246, INSERM U 1130, Neuroscience Paris Seine NPS, Paris, F-75005, FR Sorbonne Universités, UPMC Paris 06, UM 119, Institut de Biologie Paris Seine IBPS, Paris, F-75005, FR LEPCMAE, USTHB, Bab Ezzouar, Alger, DZ
  2. IMP, CNRS UMR 5223, Université Claude Bernard Lyon 1, Université de Lyon, Villeurbanne, FR
  3. CNRS UMR 8246, INSERM U 1130, Neuroscience Paris Seine NPS, Paris, F-75005, FR Sorbonne Universités, UPMC Paris 06, UM 119, Institut de Biologie Paris Seine IBPS, Paris, F-75005, FR
  4. LEPCMAE, USTHB, Bab Ezzouar, Alger, DZ LCVRM, ENSSMAL, Cheraga, Alger, DZ
  5. Univ Paris Est Creteil, INSERM, IMRB, Creteil, F-94010, FR CNRS UMR 8246, INSERM U 1130, Neuroscience Paris Seine NPS, Paris, F-75005, FR Sorbonne Universités, UPMC Paris 06, UM 119, Institut de Biologie Paris Seine IBPS, Paris, F-75005, FR

Published in Issue 2020-11-06

How to Cite

Ben Bouali, A., Montembault, A., David, L., Von Boxberg, Y., Viallon, M., Hamdi, B., Nothias, F., Fodil, R., & Féréol, S. (2020). Nanoscale mechanical properties of chitosan hydrogels as revealed by AFM. Progress in Biomaterials, 9(4 (December 2020). https://doi.org/10.1007/s40204-020-00141-4
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Abstract

Abstract In the context of tissue engineering, chitosan hydrogels are attractive biomaterials because they represent a family of natural polymers exhibiting several suitable features (cytocompatibility, bioresorbability, wound healing, bacteriostatic and fungistatic properties, structural similarity with glycosaminoglycans), and tunable mechanical properties. Optimizing the design of these biomaterials requires fine knowledge of its physical characteristics prior to assessment of the cell–biomaterial interactions. In this work, using atomic force microscopy (AFM), we report a characterization of mechanical and topographical properties at the submicron range of chitosan hydrogels, depending on physico-chemical parameters such as their polymer concentration (1.5%, 2.5% and 3.5%), their degree of acetylation (4% and 38.5%), and the conditions of the gelation process. Well-known polyacrylamide gels were used to validate the methodology approach for the determination and analysis of elastic modulus (i.e., Young’s modulus) distribution at the gel surface. We present elastic modulus distribution and topographical and stiffness maps for different chitosan hydrogels. For each chitosan hydrogel formulation, AFM analyses reveal a specific asymmetric elastic modulus distribution that constitutes a useful hallmark for chitosan hydrogel characterization. Our results regarding the local mechanical properties and the topography of chitosan hydrogels initiate new possibilities for an interpretation of the behavior of cells in contact with such soft materials .

Keywords

  • Atomic force microscopy,
  • Chitosan hydrogel gelation,
  • Young’s modulus distribution

References

  1. Abidine et al. (2015) Physical properties of polyacrylamide gels probed by AFM and rheology https://doi.org/10.1209/0295-5075/109/38003
  2. Adibnia and Hill (2016) Universal aspects of hydrogel gelation kinetics, percolation and viscoelasticity from PA-hydrogel rheology https://doi.org/10.1122/1.4948428
  3. Alcaraz et al. (2003) Microrheology of human lung epithelial cells measured by atomic force microscopy (pp. 2071-2079) https://doi.org/10.1016/S0006-3495(03)75014-0
  4. Aussel et al. (2017) Chitosan-based hydrogels for developing a small-diameter vascular graft: in vitro and in vivo evaluation https://doi.org/10.1088/1748-605X/aa78d0
  5. Becerra et al. (2017) Tuning the hydrophilic/hydrophobic balance to control the structure of chitosan films and their protein release behavior (pp. 1070-1083) https://doi.org/10.1208/s12249-016-0678-9
  6. Bilodeau (1992) Regular pyramid punch problem (pp. 519-523) https://doi.org/10.1115/1.2893754
  7. Chedly et al. (2017) Physical chitosan microhydrogels as scaffolds for spinal cord injury restoration and axon regeneration (pp. 91-107) https://doi.org/10.1016/j.biomaterials.2017.05.024
  8. Crini et al. (2007) Presses Univ
  9. Denisin and Pruitt (2016) Tuning the range of polyacrylamide gel stiffness for mechanobiology applications (pp. 21893-21902) https://doi.org/10.1021/acsami.5b09344
  10. Dokukin and Sokolov (2015) High-resolution high-speed dynamic mechanical spectroscopy of cells and other soft materials with the help of atomic force microscopy https://doi.org/10.1038/srep12630
  11. Elosegui-Artola et al. (2014) Rigidity sensing and adaptation through regulation of integrin types (pp. 631-637) https://doi.org/10.1038/nmat3960
  12. Enache et al. (2018) Kinetics of chitosan coagulation from aqueous solutions https://doi.org/10.1002/app.46062
  13. Fereol and Fodil (2017) Effect of cholesterol depletion on the viscoelastic properties of alveolar epithelial cells assessed by atomic force microscopy in large deformation (pp. 57-72) https://doi.org/10.3166/rcma.2017.00004
  14. Fereol et al. (2009) Prestress and adhesion site dynamics control cell sensitivity to extracellular stiffness (pp. 2009-2022) https://doi.org/10.1016/j.bpj.2008.10.072
  15. Féréol et al. (2006) Sensitivity of alveolar macrophages to substrate mechanical and adhesive properties (pp. 321-340) https://doi.org/10.1002/cm.20130
  16. Fiamingo et al. (2016) Chitosan hydrogels for the regeneration of infarcted myocardium: preparation, physicochemical characterization, and biological evaluation (pp. 1662-1672) https://doi.org/10.1021/acs.biomac.6b00075
  17. Glass et al. (2014) Tissue-engineered cartilage with inducible and tunable immunomodulatory properties https://doi.org/10.1016/j.biomaterials.2014.03.073
  18. Gross and Kress (2017) Simultaneous measurement of the Young's modulus and the Poisson ratio of thin elastic layers (pp. 1048-1055) https://doi.org/10.1039/C6SM02470J
  19. Gutiérrez (2017) Chitosan applications for the food industry https://doi.org/10.1002/9781119364849.ch8
  20. Hirai and Nakajima (1991) Determination of degree of deacetylation of chitosan by 1H NMR spectroscopy (pp. 87-94) https://doi.org/10.1007/BF00299352
  21. Hutter (1993) Characterization of atomic-force microscope tips (pp. 1868-1873) https://doi.org/10.1063/1.1143970
  22. Kim et al. (2008) Chitosan and its derivatives for tissue engineering applications (pp. 1-21) https://doi.org/10.1016/j.biotechadv.2007.07.009
  23. Kumar (2018) Future biomaterials for enhanced cell–substrate communication in spinal cord injury intervention https://doi.org/10.4155/fsoa-2017-0130
  24. Ladoux and Nicolas (2012) Physically based principles of cell adhesion mechanosensitivity in tissues https://doi.org/10.1088/0034-4885/75/11/116601
  25. Lamarque et al. (2005) Physicochemical behavior of homogeneous series of acetylated chitosans in aqueous solution: role of various structural parameters (pp. 131-142) https://doi.org/10.1021/bm0496357
  26. Lee (2018) Injectable hydrogels delivering therapeutic agents for disease treatment and tissue engineering https://doi.org/10.1186/s40824-018-0138-6
  27. Li et al. (2012) Engineering neural stem cell fates with hydrogel design for central nervous system regeneration (pp. 1105-1129) https://doi.org/10.1016/j.progpolymsci.2012.02.004
  28. López-Velázquez (2019) Gelatin–chitosan—PVA hydrogels and their application in agriculture (pp. 3495-3504) https://doi.org/10.1002/jctb.5961
  29. Mathworks (2020).
  30. https://it.mathworks.com/help/stats/fitdist.html
  31. Meco and Lampe (2018) Microscale architecture in biomaterial scaffolds for spatial control of neural cell behavior https://doi.org/10.3389/fmats.2018.00002
  32. Medtronic (2017) Chitosan as a biomaterial.
  33. https://www.medtronic.com/se-sv/healthcare-professionals/products/ear-nose-throat/bio-packing/bio-nasal-packing/novashield.html
  34. . Accessed 2017.
  35. Mohammadzadeh Pakdel and Peighambardoust (2018) Review on recent progress in chitosan-based hydrogels for wastewater treatment application (pp. 264-279) https://doi.org/10.1016/j.carbpol.2018.08.070
  36. Montembault et al. (2005) Rheometric study of the gelation of chitosan in aqueous solution without cross-linking agent (pp. 653-662) https://doi.org/10.1021/bm049593m
  37. Montembault et al. (2005) Rheometric study of the gelation of chitosan in a hydroalcoholic medium (pp. 1633-1643) https://doi.org/10.1016/j.biomaterials.2004.06.029
  38. Montembault et al. (2006) A material decoy of biological media based on chitosan physical hydrogels: application to cartilage tissue engineering (pp. 551-564) https://doi.org/10.1016/j.biochi.2006.03.002
  39. Notbohm et al. (2012) Analysis of nanoindentation of soft materials with an atomic force microscope (pp. 229-237) https://doi.org/10.1557/jmr.2011.252
  40. Novak and Koh (2013) Phenotypic transitions of macrophages orchestrate tissue repair (pp. 1352-1363) https://doi.org/10.1016/j.ajpath.2013.06.034
  41. Oyen (2014) Mechanical characterisation of hydrogel materials (pp. 44-59) https://doi.org/10.1179/1743280413Y.0000000022
  42. Perrard et al. (2016) Complete human and rat ex vivo spermatogenesis from fresh or frozen testicular tissue https://doi.org/10.1095/biolreprod.116.142802
  43. Piner et al. (1999) Improved Imaging of soft materials with modified AFM tips (pp. 5457-5460) https://doi.org/10.1021/la990408d
  44. Popa-Nita et al. (2009) Structure of natural polyelectrolyte solutions: role of the hydrophilic/hydrophobic interaction balance (pp. 6460-6468) https://doi.org/10.1021/la900061n
  45. Popa-Nita et al. (2010) Continuum of structural organization from chitosan solutions to derived physical forms (pp. 6-12) https://doi.org/10.1021/bm9012138
  46. Rami et al. (2014) Physicochemical modulation of chitosan-based hydrogels induces different biological responses: interest for tissue engineering (pp. 3666-3676) https://doi.org/10.1002/jbm.a.35035
  47. Reuss (1929) Berechnung der Fließgrenze von Mischkristallen auf Grund der Plastizitätsbedingung für Einkristalle (pp. 49-58) https://doi.org/10.1002/zamm.19290090104
  48. Schatz et al. (2003) Typical physicochemical behaviors of chitosan in aqueous solution (pp. 641-648) https://doi.org/10.1021/bm025724c
  49. Schillers (2017) Standardized nanomechanical atomic force microscopy procedure (SNAP) for measuring soft and biological samples https://doi.org/10.1038/s41598-017-05383-0
  50. Sereni et al. (2017) Dynamic structuration of physical chitosan (pp. 12697-12707) https://doi.org/10.1021/acs.langmuir.7b02997
  51. Skoog et al. (2018) Biological responses to immobilized microscale and nanoscale surface topographies (pp. 33-55) https://doi.org/10.1016/j.pharmthera.2017.07.009
  52. Sridharan et al. (2019) Material stiffness influences the polarization state, function and migration mode of macrophages (pp. 47-59) https://doi.org/10.1016/j.actbio.2019.02.048
  53. Vachoud et al. (1997) Formation and characterisation of a physical chitin gel (pp. 169-177) https://doi.org/10.1016/S0008-6215(97)00126-2
  54. Vasconcelos et al. (2013) Macrophage polarization following chitosan implantation (pp. 9952-9959) https://doi.org/10.1016/j.biomaterials.2013.09.012
  55. Yang (2011) Chitin-based materials in tissue engineering: applications in soft tissue and epithelial organ (pp. 1936-1963) https://doi.org/10.3390/ijms12031936
  56. Zhou and Groth (2018) Host responses to biomaterials and anti-inflammatory design-a brief review https://doi.org/10.1002/mabi.201800112