Collagen Type II—Chitosan Interactions as Dependent on Hydroxylation and Acetylation Inferred from Molecular Dynamics Simulations - Publication - Bridge of Knowledge

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Collagen Type II—Chitosan Interactions as Dependent on Hydroxylation and Acetylation Inferred from Molecular Dynamics Simulations

Abstract

Chitosan–collagen blends have been widely applied in tissue engineering, joints diseases treatment, and many other biomedical fields. Understanding the affinity between chitosan and collagen type II is particularly relevant in the context of mechanical properties modulation, which is closely associated with designing biomaterials suitable for cartilage and synovial fluid regeneration. However, many structural features influence chitosan’s affinity for collagen. One of the most important ones is the deacetylation degree (DD) in chitosan and the hydroxylation degree (HD) of proline (PRO) moieties in collagen. In this paper, combinations of both factors were analyzed using a very efficient molecular dynamics approach. It was found that DD and HD modifications significantly affect the structural features of the complex related to considered types of interactions, namely hydrogen bonds, hydrophobic, and ionic contacts. In the case of hydrogen bonds both direct and indirect (water bridges) contacts were examined. In case of the most collagen analogues, a very good correlation between binding free energy and DD was observed.

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Category:
Magazine publication
Type:
Magazine publication
Published in:
MOLECULES no. 28, edition 1,
ISSN: 1420-3049
Publication year:
2023
DOI:
Digital Object Identifier (open in new tab) 10.3390/molecules28010154
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  1. Han, L.; Grodzinsky, A.J.; Ortiz, C. Nanomechanics of the cartilage extracellular matrix. Annu. Rev. Mater. Res. 2011, 41, 133-168. [CrossRef] [PubMed] open in new tab
  2. Xu, Q.; Torres, J.E.; Hakim, M.; Babiak, P.M.; Pal, P.; Battistoni, C.M.; Nguyen, M.; Panitch, A.; Solorio, L.; Liu, J.C. Collagen- and hyaluronic acid-based hydrogels and their biomedical applications. Mater. Sci. Eng. R Reports 2021, 146, 100641. [CrossRef] [PubMed] open in new tab
  3. Mitura, S.; Sionkowska, A.; Jaiswal, A. Biopolymers for hydrogels in cosmetics: Review. J. Mater. Sci. Mater. Med. 2020, 31, 50. [CrossRef] [PubMed] open in new tab
  4. Sionkowska, A.; Gadomska, M.; Musiał, K.; Piatek, J. Hyaluronic Acid as a Component of Natural Polymer Blends for Biomedical Applications: A Review. Molecules 2020, 25, 4035. [CrossRef] [PubMed] open in new tab
  5. Mazeau, K.; Rinaudo, M. Comparative properties of hyaluronan and chitosan in aqueous environment. Polym. Sci.-Ser. C 2012, 54, 96-107. [CrossRef] open in new tab
  6. Wu, X.; Black, L.; Santacana-Laffitte, G.; Patrick, C.W. Preparation and assessment of glutaraldehyde-crosslinked collagen-chitosan hydrogels for adipose tissue engineering. J. Biomed. Mater. Res.-Part A 2007, 81, 59-65. [CrossRef] open in new tab
  7. Yan, L.P.; Wang, Y.J.; Ren, L.; Wu, G.; Caridade, S.G.; Fan, J.B.; Wang, L.Y.; Ji, P.H.; Oliveira, J.M.; Oliveira, J.T.; et al. Genipin-cross- linked collagen/chitosan biomimetic scaffolds for articular cartilage tissue engineering applications. J. Biomed. Mater. Res.-Part A 2010, 95 Pt A, 465-475. [CrossRef] open in new tab
  8. Kim, I.Y.; Seo, S.J.; Moon, H.S.; Yoo, M.K.; Park, I.Y.; Kim, B.C.; Cho, C.S. Chitosan and its derivatives for tissue engineering applications. Biotechnol. Adv. 2008, 26, 1-21. [CrossRef] open in new tab
  9. Tangsadthakun, C.; Kanokpanont, S.; Sanchavanakit, N.; Banaprasert, T.; Damrongsakkul, S. Properties of Collagen/Chitosan Scaffolds for Skin Tissue Engineering. J. Met. Mater. Miner. 2017, 16, 37-44. open in new tab
  10. Zhu, C.; Fan, D.; Duan, Z.; Xue, W.; Shang, L.; Chen, F.; Luo, Y. Initial investigation of novel human-like collagen/chitosan scaffold for vascular tissue engineering. J. Biomed. Mater. Res.-Part A 2009, 89, 829-840. [CrossRef] open in new tab
  11. 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. [CrossRef] [PubMed] open in new tab
  12. Rafat, M.; Li, F.; Fagerholm, P.; Lagali, N.S.; Watsky, M.A.; Munger, R.; Matsuura, T.; Griffith, M. PEG-stabilized carbodiimide crosslinked collagen-chitosan hydrogels for corneal tissue engineering. Biomaterials 2008, 29, 3960-3972. [CrossRef] [PubMed] open in new tab
  13. Tan, W.; Krishnaraj, R.; Desai, T.A. Evaluation of nanostructured composite collagen-chitosan matrices for tissue engineering. Tissue Eng. 2001, 7, 203-210. [CrossRef] [PubMed] open in new tab
  14. Fernandes, L.L.; Resende, C.X.; Tavares, D.S.; Soares, G.A.; Castro, L.O.; Granjeiro, J.M. Cytocompatibility of chitosan and collagen-chitosan scaffolds for tissue engineering. Polimeros 2011, 21, 1-6. [CrossRef] open in new tab
  15. Ma, L.; Gao, C.; Mao, Z.; Zhou, J.; Shen, J.; Hu, X.; Han, C. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 2003, 24, 4833-4841. [CrossRef] open in new tab
  16. Chicatun, F.; Griffanti, G.; McKee, M.D.; Nazhat, S.N. Collagen/chitosan composite scaffolds for bone and cartilage tissue engineering. In Biomedical Composites; Woodhead Publishing: Sawston, UK, 2017; pp. 163-198. open in new tab
  17. Jiang, Y.; Fu, C.; Wu, S.; Liu, G.; Guo, J.; Su, Z. Determination of the deacetylation degree of chitooligosaccharides. Mar. Drugs 2017, 15, 332. [CrossRef] open in new tab
  18. Jones, M.; Kujundzic, M.; John, S.; Bismarck, A. Crab vs. Mushroom: A review of crustacean and fungal chitin in wound treatment. Mar. Drugs 2020, 18, 64. [CrossRef] open in new tab
  19. Pellis, A.; Guebitz, G.M.; Nyanhongo, G.S. Chitosan: Sources, Processing and Modification Techniques. Gels 2022, 8, 393. [CrossRef] open in new tab
  20. El Knidri, H.; El Khalfaouy, R.; Laajeb, A.; Addaou, A.; Lahsini, A. Eco-friendly extraction and characterization of chitin and chitosan from the shrimp shell waste via microwave irradiation. Process Saf. Environ. Prot. 2016, 104, 395-405. [CrossRef] open in new tab
  21. Oladzadabbasabadi, N.; Mohammadi Nafchi, A.; Ariffin, F.; Wijekoon, M.M.J.O.; Al-Hassan, A.A.; Dheyab, M.A.; Ghasemlou, M. Recent advances in extraction, modification, and application of chitosan in packaging industry. Carbohydr. Polym. 2022, 277, 118876. [CrossRef] open in new tab
  22. Rodríguez-Vázquez, M.; Vega-Ruiz, B.; Ramos-Zúñiga, R.; Saldaña-Koppel, D.A.; Quiñones-Olvera, L.F. Chitosan and Its Potential Use as a Scaffold for Tissue Engineering in Regenerative Medicine. Biomed Res. Int. 2015, 2015, 821279. [CrossRef] [PubMed] open in new tab
  23. Domalik-Pyzik, P.; Chłopek, J.; Pielichowska, K. Chitosan-Based Hydrogels: Preparation, Properties, and Applications. In Cellulose-Based Superabsorbent Hydrogels. Polymers and Polymeric Composites: A Reference Series; open in new tab
  24. Mondal, M., Ed.; Springer: Cham, Switzerland, 2019; pp. 1665-1693.
  25. Mathaba, M.; Daramola, M.O. Effect of chitosan's degree of deacetylation on the performance of pes membrane infused with chitosan during amd treatment. Membranes 2020, 10, 52. [CrossRef] [PubMed] open in new tab
  26. Rasweefali, M.K.; Sabu, S.; Sunooj, K.V.; Sasidharan, A.; Xavier, K.A.M. Consequences of chemical deacetylation on physicochem- ical, structural and functional characteristics of chitosan extracted from deep-sea mud shrimp. Carbohydr. Polym. Technol. Appl. 2021, 2, 100032. [CrossRef] open in new tab
  27. Yuan, Y.; Chesnutt, B.M.; Haggard, W.O.; Bumgardner, J.D. Deacetylation of Chitosan: Material Characterization and in vitro Evaluation via Albumin Adsorption and Pre-Osteoblastic Cell Cultures. Materials 2011, 4, 1399-1416. [CrossRef] [PubMed] open in new tab
  28. Sionkowska, A.; Wisniewski, M.; Skopinska, J.; Kennedy, C.J.; Wess, T.J. Molecular interactions in collagen and chitosan blends. Biomaterials 2004, 25, 795-801. [CrossRef] open in new tab
  29. Hou, C.; Gao, L.; Wang, Z.; Rao, W.; Du, M.; Zhang, D. Mechanical properties, thermal stability, and solubility of sheep bone collagen-chitosan films. J. Food Process Eng. 2020, 43, e13086. [CrossRef] open in new tab
  30. Machado, A.A.S.; Martins, V.C.A.; Plepis, A.M.G. Thermal and rheological behavior of collagen: Chitosan blends. J. Therm. Anal. Calorim. 2002, 67, 491-498. [CrossRef] open in new tab
  31. Hsu, S.H.; Whu, S.W.; Tsai, C.L.; Wu, Y.H.; Chen, H.W.; Hsieh, K.H. Chitosan as scaffold materials: Effects of molecular weight and degree of deacetylation. J. Polym. Res. 2004, 11, 141-147. [CrossRef] open in new tab
  32. Varma, S.; Orgel, J.P.R.O.; Schieber, J.D. Contrasting local and macroscopic effects of collagen hydroxylation. Int. J. Mol. Sci. 2021, 22, 9068. [CrossRef] open in new tab
  33. Rosenbloom, J.; Harsch, M.; Jimenez, S. Hydroxyproline content determines the denaturation temperature of chick tendon collagen. Arch. Biochem. Biophys. 1973, 158, 478-484. [CrossRef] open in new tab
  34. Sipila, K.H.; Drushinin, K.; Rappu, P.; Jokinen, J.; Salminen, T.A.; Salo, A.M.; Käpyla, J.; Myllyharju, J.; Heino, J. Proline hydroxylation in collagen supports integrin binding by two distinct mechanisms. J. Biol. Chem. 2018, 293, 7645-7658. [CrossRef] [PubMed] open in new tab
  35. Martinou, A.; Kafetzopoulos, D.; Bouriotis, V. Chitin deacetylation by enzymatic means: Monitoring of deacetylation processes. Carbohydr. Res. 1995, 273, 235-242. [CrossRef] open in new tab
  36. Jaworska, M.M. Kinetics of enzymatic deacetylation of chitosan. Cellulose 2012, 19, 363-369. [CrossRef] open in new tab
  37. Harmsen, R.A.G.; Tuveng, T.R.; Antonsen, S.G.; Eijsink, V.G.H.; Sørlie, M. Can we make Chitosan by Enzymatic Deacetylation of Chitin? Molecules 2019, 24, 3862. [CrossRef] [PubMed] open in new tab
  38. No, H.K.; Cho, Y.I.; Kim, H.R.; Meyers, S.P. Effective Deacetylation of Chitin under Conditions of 15 psi/121 • C. J. Agric. Food Chem. 2000, 48, 2625-2627. [CrossRef] open in new tab
  39. He, X.; Li, K.; Xing, R.; Liu, S.; Hu, L.; Li, P. The production of fully deacetylated chitosan by compression method. Egypt. J. Aquat. Res. 2016, 42, 75-81. [CrossRef] open in new tab
  40. Tsaih, M.L.; Chen, R.H. The effect of reaction time and temperature during heterogenous alkali deacetylation on degree of deacetylation and molecular weight of resulting chitosan. J. Appl. Polym. Sci. 2003, 88, 2917-2923. [CrossRef] open in new tab
  41. An, B.; Kaplan, D.L.; Brodsky, B. Engineered recombinant bacterial collagen as an alternative collagen-based biomaterial for tissue engineering. Front. Chem. 2014, 2, 40. [CrossRef] open in new tab
  42. Xu, X.; Gan, Q.; Clough, R.C.; Pappu, K.M.; Howard, J.A.; Baez, J.A.; Wang, K. Hydroxylation of recombinant human collagen type I alpha 1 in transgenic maize co-expressed with a recombinant human prolyl 4-hydroxylase. BMC Biotechnol. 2011, 11, 69. [CrossRef] open in new tab
  43. Wang, T.; Lew, J.; Premkumar, J.; Poh, C.L.; Naing, M.W. Production of recombinant collagen: State of the art and challenges. Eng. Biol. 2017, 1, 18-23. [CrossRef] open in new tab
  44. Acevedo, C.A.; Diáz-Calderón, P.; López, D.; Enrione, J. Assessment of gelatin-chitosan interactions in films by a chemometrics approach. CYTA-J. Food 2015, 13, 227-234. [CrossRef] open in new tab
  45. Ledward, D.A. Gelation of gelatin. In Functional Properties of Food Macromolecules;
  46. Mitchell, J.R., Ledward, D.A., Eds.; Elsevier Applied Science: London, UK, 1986; pp. 171-201.
  47. Gómez-Estaca, J.; Gómez-Guillén, M.C.; Fernández-Martín, F.; Montero, P. Effects of gelatin origin, bovine-hide and tuna-skin, on the properties of compound gelatin-chitosan films. Food Hydrocoll. 2011, 25, 1461-1469. [CrossRef] open in new tab
  48. Pietrucha, K. Changes in denaturation and rheological properties of collagen-hyaluronic acid scaffolds as a result of temperature dependencies. Int. J. Biol. Macromol. 2005, 36, 299-304. [CrossRef] [PubMed] open in new tab
  49. Taravel, M.N.; Domard, A. Collagen and its interaction with chitosan. II. Influence of the physicochemical characteristics of collagen. Biomaterials 1995, 16, 865-871. [CrossRef] open in new tab
  50. Martínez, A.; Blanco, M.D.; Davidenko, N.; Cameron, R.E. Tailoring chitosan/collagen scaffolds for tissue engineering: Effect of composition and different crosslinking agents on scaffold properties. Carbohydr. Polym. 2015, 132, 606-619. [CrossRef] [PubMed] open in new tab
  51. Zakhem, E.; Bitar, K. Development of Chitosan Scaffolds with Enhanced Mechanical Properties for Intestinal Tissue Engineering Applications. J. Funct. Biomater. 2015, 6, 999-1011. [CrossRef] open in new tab
  52. Han, C.M.; Zhang, L.P.; Sun, J.Z.; Shi, H.F.; Zhou, J.; Gao, C.Y. Application of collagen-chitosan/fibrin glue asymmetric scaffolds in skin tissue engineering. J. Zhejiang Univ. Sci. B 2010, 11, 524-530. [CrossRef] open in new tab
  53. Carvalho, D.N.; Lopez-Cebral, R.; Sousa, R.O.; Alves, A.L.; Reys, L.L.; Silva, S.S.; Oliveira, J.M.; Reis, R.L.; Silva, T.H. Marine collagen-chitosan-fucoidan cryogels as cell-laden biocomposites envisaging tissue engineering. Biomed. Mater. 2020, 15, 055030. [CrossRef] open in new tab
  54. Moon, H.; Choy, S.; Park, Y.; Jung, Y.M.; Koo, J.M.; Hwang, D.S. Different Molecular Interaction between Collagen and α-or β-Chitin in Mechanically Improved Electrospun Composite. Mar. Drugs 2019, 17, 318. [CrossRef] open in new tab
  55. Krieger, E.; Dunbrack, R.L.; Hooft, R.W.W.; Krieger, B. Assignment of protonation states in proteins and ligands: Combining pK a prediction with hydrogen bonding network optimization. Methods Mol. Biol. 2012, 819, 405-421. [CrossRef] open in new tab
  56. Indrani, D.J.; Lukitowati, F.; Yulizar, Y. Preparation of Chitosan/Collagen Blend Membranes for Wound Dressing: A Study on FTIR Spectroscopy and Mechanical Properties. IOP Conf. Ser. Mater. Sci. Eng. 2017, 202, 012020. [CrossRef] open in new tab
  57. Staroszczyk, H.; Sztuka, K.; Wolska, J.; Wojtasz-Pajak, A.; Kołodziejska, I. Interactions of fish gelatin and chitosan in uncrosslinked and crosslinked with EDC films: FT-IR study. Spectrochim. Acta-Part A Mol. Biomol. Spectrosc. 2014, 117, 707-712. [CrossRef] [PubMed] open in new tab
  58. Langrock, T.; Hoffmann, R. Analysis of Hydroxyproline in Collagen Hydrolysates. In Amino Acid Analysis. Methods in Molecular Biology; open in new tab
  59. Alterman, M., Ed.; Humana: New York, NY, USA, 2019; Volume 2030, pp. 47-56.
  60. The MathWorks Inc. MATLAB; The MathWorks Inc.: Natick, MA, USA, 2022. open in new tab
  61. Pokidysheva, E.; Boudko, S.; Vranka, J.; Zientek, K.; Maddox, K.; Moser, M.; Fässler, R.; Ware, J.; Bächinger, H.P. Biological role of prolyl 3-hydroxylation in type IV collagen. Proc. Natl. Acad. Sci. USA 2014, 111, 161-166. [CrossRef] [PubMed] open in new tab
  62. Rappu, P.; Salo, A.M.; Myllyharju, J.; Heino, J. Role of prolyl hydroxylation in the molecular interactions of collagens. Essays Biochem. 2019, 63, 325-335. [CrossRef] open in new tab
  63. Kivirikko, K.I.; Myllylä, R.; Pihlajaniemi, T. Hydroxylation of proline and lysine residues in collagens and other animal and plant proteins. In Post-Translational Modifications of Proteins; open in new tab
  64. Harding, J.J., Crabbe, M.J.C., Eds.; CRC Press: Boca Raton, FL, USA, 1991; pp. 1-51. ISBN 9780849341717.
  65. Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010, 31, 455-461. [CrossRef] open in new tab
  66. Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M.C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; et al. A Point-Charge Force Field for Molecular Mechanics Simulations of Proteins Based on Condensed-Phase Quantum Mechanical Calculations. J. Comput. Chem. 2003, 24, 1999-2012. [CrossRef] open in new tab
  67. Kirschner, K.N.; Yongye, A.B.; Tschampel, S.M.; González-Outeiriño, J.; Daniels, C.R.; Foley, B.L.; Woods, R.J. GLYCAM06: A generalizable biomolecular force field. carbohydrates. J. Comput. Chem. 2008, 29, 622-655. [CrossRef] open in new tab
  68. Kulke, M.; Geist, N.; Friedrichs, W.; Langel, W. Molecular dynamics simulations on networks of heparin and collagen. Proteins Struct. Funct. Bioinform. 2017, 85, 1119-1130. [CrossRef] open in new tab
  69. Roy, A.; Gauld, J.W. Molecular Dynamics Investigation on the Effects of Protonation and Lysyl Hydroxylation on Sulfilimine Cross-links in Collagen IV. ACS Omega 2022, 7, 39680-39689. [CrossRef] open in new tab
  70. Cole, C.C.; Misiura, M.; Hulgan, S.A.H.; Peterson, C.M.; Williams, J.W.; Kolomeisky, A.B.; Hartgerink, J.D. Cation−π Interactions and Their Role in Assembling Collagen Triple Helices. Biomacromolecules 2022, 23, 4645-4654. [CrossRef] open in new tab
  71. Krieger, E.; Vriend, G. YASARA View-Molecular graphics for all devices-From smartphones to workstations. Bioinformatics 2014, 30, 2981-2982. [CrossRef] [PubMed] open in new tab
  72. Essmann, U.; Perera, L.; Berkowitz, M.L.; Darden, T.; Lee, H.; Pedersen, L.G. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103, 8577-8593. [CrossRef] open in new tab
  73. Holst, M.; Baker, N.; Wang, F. Adaptive multilevel finite element solution of the Poisson-Boltzmann equation I. Algorithms and examples. J. Comput. Chem. 2000, 21, 1319-1342. [CrossRef] open in new tab
  74. Baker, N.; Holst, M.; Wang, F. Adaptive multilevel finite element solution of the Poisson-Boltzmann equation II. Refinement at solvent-accessible surfaces in biomolecular systems. J. Comput. Chem. 2000, 21, 1343-1352. [CrossRef] open in new tab
  75. Syme, N.R.; Dennis, C.; Bronowska, A.; Paesen, G.C.; Homans, S.W. Comparison of entropic contributions to binding in a "hydrophilic" versus "hydrophobic" ligand-protein interaction. J. Am. Chem. Soc. 2010, 132, 8682-8689. [CrossRef] [PubMed] open in new tab
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