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Research Article

Exploration of type II and III collagen binding interactions with short peptide-phenyl pyrazole conjugates via docking, molecular dynamics and laboratory experiments

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Pages 53-82 | Received 22 Jun 2022, Accepted 10 Nov 2022, Published online: 05 Dec 2022

References

  • Haleem, A. M.; Chu, C. R. Adv.Advances in Tissue Engineering Techniques for Articular Cartilage Repair, Operative Techniques in Orthopedics. Operative Techniques in Orthopaedics. 2010, 20(2), 76–89. DOI: 10.1053/j.oto.2009.10.004.
  • Loh, Q. L.; Choong, C. Three Dimensional Scaffolds for Tissue Engineering Applications: Role of Porosity and Pore Size. Tissue Engineering Part B: Reviews. 2013, 19(6), 485–502. DOI: 10.1089/ten.teb.2012.0437.
  • Howard, D.; Buttery, L. D.; Shakesheff, K. M.; Roberts, S. J. Tissue Engineering: Strategies, Stem Cells and Scaffolds. Journal of Anatomy. 2008, 213(1), 66–72. DOI: 10.1111/j.1469-7580.2008.00878.x.
  • Klimek, K.; Ginalska, G. Proteins and Peptides as Important Modifiers of the Polymer Scaffolds for Tissue Engineering Applications – A Review. Polymers. 2020, 12(4), 844. DOI: 10.3390/polym12040844.
  • Mehrabani, M. G.; Karimian, R.; Mehramouz, B.; Rahimi, M.; Kafil, H. S. Preparation of Biocompatible and Biodegradable Silk Fibroin/chitin/silver Nanoparticles 3D Scaffolds as a Bandage for Antimicrobial Wound Dressing. International Journal of Biological Macromolecules. 2018, 114, 961–971. DOI: 10.1016/j.ijbiomac.2018.03.128.
  • Fratzl, P. 2008. Collagen: Structure and Mechanics, an Introduction. Collagen; Fratzl, P., Eds., pp. 1–13. Springer: Boston, MA. DOI: 10.1007/978-0-387-73906-9_1
  • Ricard-Blum, S. The Collagen Family. Cold Spring Harb. Perspect. Biol. 2011, 3, a004978. DOI: 10.1101/cshperspect.a004978.
  • Abreu-Velez, A. M.; Howard, M. S. Collagen IV in Normal Skin and Pathological Processes. North American Journal of Medical Sciences. 2012, 4(1), 1. DOI: 10.4103/1947-2714.92892.
  • Boudko, S. P.; Engel, J.; Okuyama, K.; Mizuno, K.; Bachinger, H. P. M.; Schumacher, A. Crystal Structure of Human Type III Collagen Gly991-Gly1032 Cystine Knot-containing Peptide Shows Both 7/2 and 10/3 Triple Helical Symmetries. Journal of Biological Chemistry. 2008, 283(47), 32580–32589. DOI: 10.1074/jbc.M805394200.
  • Wu, -J.-J.; Weis, M. A.; Kim, L. S.; Eyre,; Eyre, D. R. Type III Collagen, a Fibril Network Modifier in Articular Cartilage. Journal of Biological Chemistry. 2010, 285(24), 18537–18544. DOI: 10.1074/jbc.M110.112904.
  • Liu, X.; Wu, H.; Byrne, M.; Krane, S.; Jaenisch, R. Type III Collagen Is Crucial for Collagen I Fibrillogenesis and for Normal Cardiovascular Development. Proceedings of the National Academy of Sciences. 1997, 94(5), 1852–1856. DOI: 10.1073/pnas.94.5.1852.
  • Bauer, E. A.; Uitto, J. 1982. Special Tissue Collagen. Skin. In Collagen in Health and Disease; Jayson, M. I. V., Weiss, J. B., Eds.; Edinburgh: Churchill Livingstone, 474–487.
  • Antipova, O.; Orgel, J. P. R. O. In Situ D-periodic Molecular Structure of Type II Collagen. Journal of Biological Chemistry. 2010, 285(10), 7087–7096. DOI: 10.1074/jbc.M109.060400.
  • Prockop, D. J.; Kivirikko, K. I. Collagens: Molecular Biology, Diseases and Potentials for Therapy. Annu. Rev. Biochem. 1995, 64(1), 403–434. DOI: 10.1146/annurev.bi.64.070195.002155.
  • Scott, J. E.; Haigh, M. Identification of Specific Binding Sites for Keratan Sulfate Proteoglycans and Chondroitin-dermatan Sulfate Proteoglycans on Collagen Fibrils in Cornea by the Use of Cupromeronic Blue in Critical-electrolyte-concentration Techniques. Biochemical Journal. 1988, 253(2), 607–610. DOI: 10.1042/bj2530607.
  • Eyre, D. Articular Cartilage and Changes in Arthritis: Collagen of Articular Cartilage. Arthritis Res. Therapy. 2001, 4(30). DOI: 10.1186/ar380.
  • Lian, C.; Wang, X.; Qiu, X.; Wu, Z.; Gao, B.; Liu, L.; Liang, G.; Zhou, H.; Yang, X.; Peng, Y., et al. Collagen Type II Suppresses Articular Chondrocyte Hypertrophy and Osteoarthritis Progression by Promoting Integrin β1-SMAD1 Interaction. Bone Research. 2019, 7(1), 8. DOI: 10.1038/s41413-019-0046-y.
  • Chaipinyo, K.; Oakes, B. W.; Van Damme, M.-P. The Use of Debrided Human Articular Cartilage for Autologous Chondrocyte Implantation: Maintenance of Chondrocyte Differentiation and Proliferation in Type I Collagen Gels. Journal of Orthopaedic Research. 2004, 22(2), 446–455. DOI: 10.1016/j.orthres.2003.07.001.
  • Takahashi, T.; Ogasawara, T.; Asawa, Y.; Mori, Y.; Uchinuma, E.; Takato, T.; Hoshi, K. Chondrocyte Phenotypes during Proliferation Culture. Tissue Engineering. 2007, 13(7), 1583–1592. DOI: 10.1089/ten.2006.0322.
  • Tamaddon, M.; Burrows, M.; Ferreira, S. A.; Dazzi, F.; Apperley, J. F.; Bradshaw, A.; Brand, D. D.; Czernuska, J.; Gentleman, E. Monomeric, Porous Type II Collagen Scaffolds Promote Chondrogenic Differentiation of Human Bone Marrow Mesenchymal Stem Cells. In Vitro. Scientific Reports. 2017, 7(1), 43519. DOI: 10.1038/srep43519.
  • Dai, W.; Kawazoe, N.; Lin, X.; Dong, J.; Chen, G. The Influence of Structural Design of PLGA/ Collagen Hybrid Scaffolds in Cartilage Tissue Engineering. Biomaterials. 2010, 31(8), 2141–2152. DOI: 10.1016/j.biomaterials.2009.11.070.
  • Haapranta, A.-M.; Jarvinen, E.; Cengiz, I. F.; Ella, V.; Kokkonen, H. T.; Kiviranta, I.; Kellomaki, M. Preparation and Characterization of collagen/PLA, chitosan/PLA and collagen/chitosan/PLA Hybrid Scaffolds for Cartilage Tissue Engineering. Journal of Materials Science. Materials in Medicine. 2014, 25(4), 1129–1136. DOI: 10.1007/s10856-013-5129-5.
  • Kontturi, L.-S.; Jarvinen, E.; Muhonen, V.; Collin, E. C.; Pandit, A. S.; Kviranta, I.; Yliperttula, M.; Urtti, A. An Injectable, in Situ Forming Type II Collagen/ Hyaluronic Acid Hydrogel Vehicle for Chondrocyte Delivery in Cartilage Tissue Engineering. Drug Delivery and Translational Research. 2014, 4(2), 149–158. DOI: 10.1007/s13346-013-0188-1.
  • Bragdon, B.; Thinakaran, S.; Moseychuk, O.; King, D.; Young, K.; Litchfield, D. W.; Petersen, N. O.; Nohe, A. Casein Kinase 2 Beta-subunit Is a Regulator of Bone Morphogenic Protein 2 Signaling Biophys. J. 2010, 99, 897–904. DOI: 10.1016/j.bpj.2010.04.070.
  • Akkiraju, H.; Bonor, J.; Nohe, A. CK2.1, A Novel Peptide Induces Articular Cartilage Formation in Vivo. Journal of Orthopaedic Research. 2017, 35(4), 876–885. DOI: 10.1002/jor.23342.
  • Han, -Q.-Q.; Yu, M.-J.; Ge, S.-H.; Guo, H.-M.; Zhang, J.; Zhao, B.-X.; Yang, P.-S. Osteopromotive Activity of a Novel Pyrazole Carboxamide Derivative. Future Medicinal Chemistry. 2013, 5(2), 125–134. DOI: 10.4155/fmc.12.209.
  • Locarno, S.; Eleta-Lopez, A.; Lupo, M. G.; Gelmi, M. L.; Clerici, F.; Bittner, A. M. Electrospinning of Pyrazole-isothiazole Derivatives: Nanofibers from Small Molecules. RSC Advances. 2019, 9(36), 20565–20572. DOI: 10.1039/c9ra02486g.
  • Zhao, Z.; Dai, X.; Li, C.; Wang, X.; Tian, J.; Feng, Y.; Xie, J.; Ma, C.; Nie, Z.; Fan, P., et al. Pyrazolone Structural Motif in Medicinal Chemistry: Retrospect and Prospect. European Journal of Medicinal Chemistry. 2020, 186, 111893. DOI: 10.1016/j.ejmech.2019.111893.
  • Kzumikava, T.; Sato, B.; Kitagawa, H. Chondroitin Sulfate Is Indispensable for Pluripotency and Differentiation of Mouse Embryonic Stem Cells. Scientific Reports. 2014, 4, 3701. DOI: 10.1038/srep03701.
  • Yang, X.; Zhu, Y.; Ye, S.; Zhang, R.; Lu, L. Structure of Triple-helix Region of Human Collagen Type II (To Be Published). https://www.rcsb.org/structure/6jec, Sep 2022
  • Hua, C.; Zhu, Y.; Xu, W.; Ye, S.; Zhang, R.; Lu, L.; Jiang, S. Characterization by High-resolution Crystal Structure Analysis of a Triple-helix Region of Human Collagen Type III with Potent Cell Adhesion Activity Biochem. Biochemical and Biophysical Research Communications. 2019, 508(4), 1018. DOI: 10.1016/j.bbrc.2018.12.018.
  • Trott, O.; Olson, A. J. Autodock Vina: Improving the Speed and Accuracy of Docking with a New Scoring Function, Efficient Optimization, and Multithreading. Journal of Computational Chemistry. 2010, 31(2), 455–461. https://onlinelibrary.wiley.com/doi/10.1002/jcc.21334, Sep 2022
  • The PyMOL Molecular Graphics System., Version 2.0, Schrodinger LLC
  • Adasme, M. F.; Linnemann, K. L.; Bolz, S. N.; Kaiser, F.; Salentin, S.; Haupt, V. J.; Schroeder, M. PLIP 2021: Expanding the Scope of the Protein-ligand Interaction Profiler to DNA and Rna. Nucleic Acids Research. 2021, 49(W1), W530–W534. DOI: 10.1093/nar/gkab294.
  • Shaw Research, D. E., Schrödinger Release 2020-3: Desmond Molecular Dynamics System; New York, NY, 2020
  • Harder, E.; Damm, W.; Maple, J.; Wu, C.; Reboul, M.; Xiang, J.; Wang, L.; Lupyan, D.; Dahlgren, M. K.; Knight, J. L., et al. OPLS3: A Force Field Providing Broad Coverage of Drug-like Small Molecules and Proteins. Journal of Chemical Theory and Computation. 2016, 12(1), 281–296. DOI: 10.1021/acs.jctc.5b00864.
  • Martinez, R. A.; Birgin, E. G.; Martinez, J. M.; Martínez, J. M. Packmol: A Package for Building Initial Configurations for Molecular Dynamics Simulations. Journal of Computational Chemistry. 2009, 30(13), 2157–2164. DOI: 10.1002/jcc.21224.
  • Genheden, S.; Ryde, U. The MM/PBSA and MM/GBSA Methods to Estimate Ligand-binding Affinities. Expert Opinion on Drug Discovery. 2015, 10(5), 1–13. DOI: 10.1517/17460441.2015.1032936.
  • Homola, J. Present and Future of Surface Plasmon Resonance Biosensors. Analytical and Bioanalytical Chemistry. 2003, 377(3), 528–539. DOI: 10.1007/s00216-003-2101-0.
  • Richard, B. M. S. Chapter 1: Introduction to Surface Plasmon Resonance. Handb. Surf. Plasmon Reson. 2017, 2, 1–26. DOI: 10.1039/9781788010283-00001.
  • Martinez-Perdiguero, J.; Retolaza, A.; Bujanda, L.; Merino, S. Surface Plasmon Resonance Immunoassay for the Detection of the TNFα Biomarker in Human Serum. Talanta. 2014, 119, 492–497. DOI: 10.1016/j.talanta.2013.11.063.
  • Stoddart, M. WST-8 Analysis of Cell Viability during Osteogenesis of Human Mesenchymal Stem Cells. Methods Mol. Biol. 2011, 740, 21–25. DOI: 10.1007/978-1-61779-108-6_4.
  • Rastelli, G.; Del Rio, A.; Degliesposti, G.; Sgobba, M. Fast and accurate predictions of binding free energies using MM-PBSA and MM-GBSA. J. Comput. Chem. 2010, 31, 797–810.
  • Michel, G.; Pojasek, K.; Li, Y.; Sulea, T.; Linhardt, R. J.; Raman, R.; Prabhakar, V.; Sasisekharan, R.; Cygler, M. The Structure of Chondroitin B Lyase Complexed with Glycosaminoglycan Oligosaccharides Unravels a Calcium-dependent Catalytic Machinery. Journal of Biological Chemistry. 2004, 279(31), 32882–32896. DOI: 10.1074/jbc.M403421200.
  • Wieczorek, A.; Rezaei, N.; Chan, C. K.; Bromme, D.; Bromme, D.; Merschrod, E. F.; Forde, N. R.; Forde, N. R. Development and Characterization of a Eukaryotic Expression System for Human Type II Procollagen. BMC Biotechnol. 2015, 15(1), 112. DOI: 10.1186/s12896-015-0228-7.
  • Kamiyama, T.; Miura, T.; Takeuchi, H. His-Trp cation-π Interaction and Its Structural Role in a α-helical Dimer of HIV-1 Vpr Protein. Biophys. Chem. 2013, 173–174, 8–14. Doi:10.1016/j.bpc.2013.01.004.
  • Costa, R. D.; Orti, E.; Blink, H.; Graber, S.; Housecroft, C.; Constable, E. C. Intramolecular π-stacking in a Phenylpyrazole Based Iridium Complex and Its Use in Light Emitting Electrochemical Cells. Journal of the American Chemical Society. 2010, 132(17), 5978–5980. DOI: 10.1021/ja1010674.
  • Dyson, H. J.; Wright, P. E.; Scheraga, H. The Role of Hydrophobic Interactions in Initiation and Propagation of Protein Folding. Proceedings of the National Academy of Sciences. 2006, 103(35), 13057–13061. DOI: 10.1073/pnas.0605504103.
  • Poole, A. R.; Kobayashi, M.; Yasuda, T.; Laverty, S.; Mwale, F.; Kojima, T.; Sakai, T.; Wahl, C.; El-Maadawy, S.; Webb, G., et al. Type II Collagen Degradation and Its Regulation in Articular Cartilage in Osteoarthritis. Annals of the Rheumatic Diseases. 2002, 61(Supplement 2), ii78–ii81. DOI: 10.1136/ard.61.suppl_2.ii78.
  • Zondlo, N. J. Aromatic-proline Interactions: Electronically Tunable CH/π Interactions. Accounts of Chemical Research. 2013, 46(4), 1039–1049. DOI: 10.1021/ar300087y.
  • Bruckner, P.; Bachinger, H. P.; Timpl, R.; Engel, J. Three Conformationally Distinct Domains in the Amino-terminal Segment of Type III Procollagen and Its Rapid Triple Helix Leads to and Comes from Coil Transition. European Journal of Biochemistry. 1978, 90(3), 595–603. DOI: 10.1111/j.1432-1033.1978.tb12640.x.
  • Tatara, Y.; Kakizaki, I.; Suto, S.; Ishioka, H.; Negishi, M.; Endo, M. Chondroitin Sulfate Cluster of Epiphycan from Salmon Nasal Cartilage Defines Binding Specificity to Collagens. Glycobiology. 2015, 25(5), 557–569. DOI: 10.1093/glycob/cwu186.
  • Makwana, K. M.; Mahalakshmi, R. Implications of Aromatic-aromatic Interactions: From Protein Structures to Peptide Models. Protein Science. 2015, 24(12), 1920–1933. DOI: 10.1002/pro.2814.
  • Lee, J.; Ju, M.; Cho, O. H.; Kim, Y.; Nam, K. T. Tyrosine-rich Peptides as a Platform for Assembly and Material Synthesis. Advanced Science. 2019, 6(4), 1801255. DOI: 10.1002/advs.201801255.
  • Fang, J. F.; Xuan, Y. M.; Li, Q. Preparation of Polystyrene Spheres in Different Particle Sizes and Assembly of the PS Colloidal Crystals. Science China Technological Sciences. 2010, 53(11), 3088. DOI: 10.1007/s11431-010-4110-5.
  • Yang, K.; Sun, J.; Wei, D.; Yuan, L.; Yang, J.; Guo, L.; Fan, H.; Zhang, X. Photo-crosslinked Mono-component Type II Collagen Hydrogel as a Matrix to Induce Chondrogenic Differentiation of Bone Marrow Mesenchymal Stem Cells. J. Mater. Chem. 2017, 5, 8707–8718. DOI: 10.1039/C7TB02348K.
  • Cao, H.; S-y, X. Purification and Characterization of Type II Collagen from Chick Sternal Cartilage. Food Chemistry. 2008, 108(2), 439–445. DOI: 10.1016/j.foodchem.2007.
  • Rieppo, L.; Saarakkala, S.; Narhi, T.; Heliminen, H. J.; Jurvelin, J. S.; Rieppo, J. Application of Second Derivative Spectroscopy for Increasing Molecular Specificity of Fourier Transform Infrared Spectroscopic Imaging of Articular Cartilage. Osteoarthritis and Cartilage. 2012, 20(5), 451–459. DOI: 10.1016/j.joca.2012.01.010.
  • Belbachir, K.; Noreen, R.; Gouspillou, G.; Petibois, C. Collagen Types Analysis and Differentiation by FTIR Spectroscopy. Analytical and Bioanalytical Chemistry. 2009, 395(3), 829–837. DOI: 10.1007/s00216-009-3019-y.
  • Liu, Y. L.; Kim, H.-J. Fourier Transform Infrared Spectroscopy (FT-IR) and Simple Algorithm Analysis for Rapid and Non-destructive Assessment of Developmental Cotton Fibers. Sensors. 2017, 17(7), 1469. DOI: 10.3390/s17071469.
  • Suhail, M.; Wu, P.-C.; Minhas, M. U. Development and Characterization of pH-sensitive Chondroitin Sulfate-co-poly(acrylic Acid) Hydrogels for Controlled Release of Diclofenac Sodium. Journal of Saudi Chemical Society. 2021, 25(4), 101212. DOI: 10.1016/j.jscs.2021.101212.
  • Lai, J.-Y.; Wang, P.-R.; Luo, L.-J.; Chen, S.-T. Stabilization of Collagen Nanofibers with L-Lysine Improves the Ability of Carbodiimide Cross-linked Amniotic Membranes to Preserve Limbal Epithelial Progenitor Cells. International Journal of Nanomedicine. 2014, 9, 5117–5130. DOI: 10.2147/IJN.S69689.
  • Persikov, A. V.; Ramshaw, J. A. M.; Kirkpatrick, A.; Brodsky, B. Electrostatic Interactions Involving Lysine Make Major Contributions to Collagen Triple-helix Stability. Biochemistry. 2005, 44(5), 1414–1422. DOI: 10.1021/bi048216r.
  • Galus, A.; Mallet, J.-M.; Lembo, D.; Cagno, V.; Djabourov, M.; Lortat-Jacob, H.; Bouchemal, K. Hexagonal-shaped Chondroitin Sulfate Self-assemblies Have Exalted anti-HSV Activity. Carbohydrate Polymers. 2016, 136, 113–120. DOI: 10.1016/j.carbpol.2015.08.054.
  • Innocenti, M. New Insights into the Formation and Function of Lamellipodia and Ruffles in Mesenchymal Cell Migration. Cell Adhesion & Migration. 2018, 12(5), 401–416. DOI: 10.1080/19336918.2018.1448352.
  • Taubenberger, A. V.; Baum, B.; Matthews, H. K. The Mechanics of Mitotic Cell Rounding. Frontiers in Cell and Developmental Biology. 2020, 8, 687. DOI: 10.3389/fcell.2020.00687.
  • Tan, T.; Malik-Garbi, M.; Abu-Shah, E.; Li, J.; Sharma, A.; Mackintosh, F. C.; Keren, K.; Schmidt, C. F.; Fakhri, N. Self-Organized Stress Patterns Drive State Transitions in Actin Cortices. Sci. Adv. 2018, 4(6), eaar2847. DOI: 10.1126/sciadv.aar2847.

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