Contrasting Local and Macroscopic Effects of Collagen Hydroxylation
Abstract
:1. Introduction
2. Methods
2.1. Zero-Stress Simulations
2.2. Constant Strain Simulations
2.3. MD Parameters
3. Results and Discussion
3.1. Effect of Hydroxylation on Fibril Structure
3.2. Effect of Hydroxylation on Fibril Mechanics
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Shoulders, M.D.; Raines, R.T. Collagen Structure and Stability. Annu. Rev. Biochem. 2009, 78, 929–958. [Google Scholar] [CrossRef] [Green Version]
- Orgel, J.P.R.O.; Antonio, J.D.S.; Antipova, O. Molecular and structural mapping of collagen fibril interactions. Connect. Tissue Res. 2011, 52, 2–17. [Google Scholar] [CrossRef]
- Mienaltowski, M.J.; Birk, D.E. Structure, Physiology, and Biochemistry of Collagens. In Progress in Heritable Soft Connective Tissue Diseases; Halper, J., Ed.; Springer: Dordrecht, The Netherlands, 2014; pp. 5–29. [Google Scholar] [CrossRef]
- Cen, L.; Liu, W.; Cui, L.; Zhang, W.; Cao, Y. Collagen Tissue Engineering: Development of Novel Biomaterials and Applications. Pediatr. Res. 2008, 63, 492–496. [Google Scholar] [CrossRef]
- Parenteau-Bareil, R.; Gauvin, R.; Berthod, F. Collagen-Based Biomaterials for Tissue Engineering Applications. Materials 2010, 3, 1863–1887. [Google Scholar] [CrossRef] [Green Version]
- Chattopadhyay, S.; Raines, R.T. Review collagen-based biomaterials for wound healing. Biopolymers 2014, 101, 821–833. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Lullo, G.A.; Sweeney, S.M.; Korkko, J.; Ala-Kokko, L.; San Antonio, J.D. Mapping the Ligand-binding Sites and Disease-associated Mutations on the Most Abundant Protein in the Human, Type I Collagen. J. Biol. Chem. 2002, 277, 4223–4231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Myllyharju, J.; Kivirikko, K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 2004, 20, 33–43. [Google Scholar] [CrossRef]
- Marini, J.C.; Forlino, A.; Bächinger, H.P.; Bishop, N.J.; Byers, P.H.; Paepe, A.D.; Fassier, F.; Fratzl-Zelman, N.; Kozloff, K.M.; Krakow, D.; et al. Osteogenesis imperfecta. Nat. Rev. Dis. Prim. 2017, 3, 17052. [Google Scholar] [CrossRef]
- Chen, A.; Fertala, A.; Abboud, J.; Wang, M.; Rivlin, M.; Beredjiklian, P.K. The Molecular Basis of Genetic Collagen Disorders and Its Clinical Relevance. J. Bone Jt. Surg. 2018, 100, 976–986. [Google Scholar] [CrossRef] [PubMed]
- Arseni, L.; Lombardi, A.; Orioli, D. From Structure to Phenotype: Impact of Collagen Alterations on Human Health. Int. J. Mol. Sci. 2018, 19, 1407. [Google Scholar] [CrossRef] [Green Version]
- Hulmes, D.J.S.; Miller, A. Quasi-hexagonal molecular packing in collagen fibrils. Nature 1979, 282, 878–880. [Google Scholar] [CrossRef] [PubMed]
- Trus, B.L.; Piez, K.A. Compressed microfibril models of the native collagen fibril. Nature 1980, 286, 300–301. [Google Scholar] [CrossRef]
- Orgel, J.P.; Miller, A.; Irving, T.C.; Fischetti, R.F.; Hammersley, A.P.; Wess, T.J. The In Situ Supermolecular Structure of Type I Collagen. Structure 2001, 9, 1061–1069. [Google Scholar] [CrossRef] [Green Version]
- Orgel, J.P.R.O.; Irving, T.C.; Miller, A.; Wess, T.J. Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. USA 2006, 103, 9001–9005. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hutton, J.J.; Kaplan, A.; Udenfriend, S. Conversion of the amino acid sequence Gly-Pro-Pro in protein to Gly-Pro-Hyp by collagen proline hydroxylase. Arch. Biochem. Biophys. 1967, 121, 384–391. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Zurlo, G.; Guo, J.; Takada, M.; Wei, W.; Zhang, Q. New Insights into Protein Hydroxylation and Its Important Role in Human Diseases. Biochim. Biophys. Acta 2016, 1866, 208–220. [Google Scholar] [CrossRef] [Green Version]
- Gjaltema, R.A.F.; Bank, R.A. Molecular insights into prolyl and lysyl hydroxylation of fibrillar collagens in health and disease. Crit. Rev. Biochem. Mol. Biol. 2017, 52, 74–95. [Google Scholar] [CrossRef] [Green Version]
- Chapman, J.A.; Hulmes, D.J.S. Electron microscopy of the collagen fibril. In Ultrastructure of the Connective Tissue Matrix; Ruggeri, A., Motta, P.M., Eds.; Springer: Boston, MA, USA, 1984; pp. 1–33. [Google Scholar] [CrossRef]
- Hulmes, D.J.; Miller, A.; White, S.W.; Doyle, B.B. Interpretation of the meridional X-ray diffraction pattern from collagen fibres in terms of the known amino acid sequence. J. Mol. Biol. 1977, 110, 643–666. [Google Scholar] [CrossRef]
- Bretscher, L.E.; Jenkins, C.L.; Taylor, K.M.; DeRider, M.L.; Raines, R.T. Conformational Stability of Collagen Relies on a Stereoelectronic Effect. J. Am. Chem. Soc. 2001, 123, 777–778. [Google Scholar] [CrossRef]
- Improta, R.; Berisio, R.; Vitagliano, L. Contribution of dipole-dipole interactions to the stability of the collagen triple helix. Protein Sci. 2008, 17, 955–961. [Google Scholar] [CrossRef] [Green Version]
- Shoulders, M.D.; Raines, R.T. Interstrand Dipole-Dipole Interactions Can Stabilize the Collagen Triple Helix. J. Biol. Chem. 2011, 286, 22905–22912. [Google Scholar] [CrossRef] [Green Version]
- Rahman, S.; Wineman-Fisher, V.; Al-Hamdani, Y.; Tkatchenko, A.; Varma, S. Predictive QM/MM modeling of the effect of lysine methylation on protein-protein binding. J. Mol. Biol. 2021, 433, 166745. [Google Scholar] [CrossRef] [PubMed]
- Varma, S.; Botlani, M.; Hammond, J.R.; Scott, H.L.; Orgel, J.P.R.O.; Schieber, J.D. Effect of intrinsic and extrinsic factors on the simulated D-band length of type I collagen. Proteins Struct. Funct. Bioinform. 2015, 83, 1800–1812. [Google Scholar] [CrossRef] [PubMed]
- Varma, S.; Orgel, J.P.R.O.; Schieber, J.D. Nanomechanics of Type I Collagen. Biophys. J. 2016, 111, 50–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melander, W.; Horvath, C. Salt effects on hydrophobic interactions in precipitation and chromatography of proteins: An interpretation of the lyotropic series. Arch. Biochem. Biophys. 1977, 183, 200–215. [Google Scholar] [CrossRef]
- Olsen, D.R.; Leigh, S.D.; Chang, R.; McMullin, H.; Ong, W.; Tai, E.; Chisholm, G.; Birk, D.E.; Berg, R.A.; Hitzeman, R.A.; et al. Production of Human Type I Collagen in Yeast Reveals Unexpected New Insights into the Molecular Assembly of Collagen Trimers. J. Biol. Chem. 2001, 276, 24038–24043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perret, S.; Merle, C.; Bernocco, S.; Berland, P.; Garrone, R.; Hulmes, D.J.S.; Theisen, M.; Ruggiero, F. Unhydroxylated Triple Helical Collagen I Produced in Transgenic Plants Provides New Clues on the Role of Hydroxyproline in Collagen Folding and Fibril Formation. J. Biol. Chem. 2001, 276, 43693–43698. [Google Scholar] [CrossRef] [Green Version]
- Zheng, H.; Lu, C.; Lan, J.; Fan, S.; Nanda, V.; Xu, F. How electrostatic networks modulate specificity and stability of collagen. Proc. Natl. Acad. Sci. USA 2018, 115, 6207–6212. [Google Scholar] [CrossRef] [Green Version]
- Ravikumar, K.M.; Hwang, W. Role of Hydration Force in the Self-Assembly of Collagens and Amyloid Steric Zipper Filaments. J. Am. Chem. Soc. 2011, 133, 11766–11773. [Google Scholar] [CrossRef] [Green Version]
- Collier, T.A.; Nash, A.; Birch, H.L.; de Leeuw, N.H. Preferential sites for intramolecular glucosepane cross-link formation in type I collagen: A thermodynamic study. Matrix Biol. 2015, 48, 78–88. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.; Hoop, C.L.; Case, D.A.; Baum, J. Cryptic binding sites become accessible through surface reconstruction of the type I collagen fibril. Sci. Rep. 2018, 8, 16646. [Google Scholar] [CrossRef] [PubMed]
- Collier, T.A.; Nash, A.; Birch, H.L.; de Leeuw, N.H. Relative orientation of collagen molecules within a fibril: A homology model for homo sapiens type I collagen. J. Biomol. Struct. Dyn. 2019, 37, 537–549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dutta, P.; Botlani, M.; Varma, S. Water Dynamics at Protein–Protein Interfaces: Molecular Dynamics Study of Virus–Host Receptor Complexes. J. Phys. Chem. B 2014, 118, 14795–14807. [Google Scholar] [CrossRef]
- Berendsen, H.J.C.; Grigera, J.R.; Straatsma, T.P. The missing term in effective pair potentials. J. Phys. Chem. 1987, 91, 6269–6271. [Google Scholar] [CrossRef]
- Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins Struct. Funct. Bioinform. 2006, 65, 712–725. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lindorff-Larsen, K.; Piana, S.; Palmo, K.; Maragakis, P.; Klepeis, J.; Dror, R.; Shaw, D. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins Struct. Funct. Bioinform. 2010, 78, 1950–1958. [Google Scholar] [CrossRef] [Green Version]
- Park, S.; Radmer, R.J.; Klein, T.E.; Pande, V.S. A new set of molecular mechanics parameters for hydroxyproline and its use in molecular dynamics simulations of collagen-like peptides. J. Comput. Chem. 2005, 26, 1612–1616. [Google Scholar] [CrossRef]
- Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N-log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089–10092. [Google Scholar] [CrossRef] [Green Version]
- Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 2007, 126, 014101. [Google Scholar] [CrossRef] [Green Version]
- Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 1981, 52, 7128. [Google Scholar] [CrossRef]
- Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J. Chem. Theory Comput. 2008, 4, 435–447. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arunan, E.; Desiraju, G.R.; Klein, R.A.; Sadlej, J.; Scheiner, S.; Alkorta, I.; Clary, D.C.; Crabtree, R.H.; Dannenberg, J.J.; Hobza, P.; et al. Defining the hydrogen bond: An account (IUPAC Technical Report). Pure Appl. Chem. 2011, 83, 1619–1636. [Google Scholar] [CrossRef]
- Luzar, A.; Chandler, D. Hydrogen-bond kinetics in liquid water. Nature 1996, 379, 55–57. [Google Scholar] [CrossRef]
- Sun, Y.L.; Luo, Z.P.; Fertala, A.; An, K.N. Direct quantification of the flexibility of type I collagen monomer. Biochem. Biophys. Res. Commun. 2002, 295, 382–386. [Google Scholar] [CrossRef]
- Lovelady, H.H.; Shashidhara, S.; Matthews, W.G. Solvent specific persistence length of molecular type I collagen. Biopolymers 2014, 101, 329–335. [Google Scholar] [CrossRef]
- Rezaei, N.; Lyons, A.; Forde, N.R. Environmentally Controlled Curvature of Single Collagen Proteins. Biophys. J. 2018, 115, 1457–1469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chhum, P.; Yu, H.; An, B.; Doyon, B.R.; Lin, Y.S.; Brodsky, B. Consequences of Glycine Mutations in the Fibronectin-binding Sequence of Collagen. J. Biol. Chem. 2016, 291, 27073–27086. [Google Scholar] [CrossRef] [Green Version]
- Qiu, Y.; Mekkat, A.; Yu, H.; Yigit, S.; Hamaia, S.; Farndale, R.W.; Kaplan, D.L.; Lin, Y.S.; Brodsky, B. Collagen Gly missense mutations: Effect of residue identity on collagen structure and integrin binding. J. Struct. Biol. 2018, 203, 255–262. [Google Scholar] [CrossRef] [PubMed]
Hydroxylation | Fibril D-Band Length (nm) | Fibril Gap-Fraction (%) | Monomer End-to-End Distance (nm) | Monomer Width (nm) | Inter-Monomer H-Bonds (1/V |
---|---|---|---|---|---|
Yes | 66.21 ± 0.03 | 58.2 ± 0.1 | 290.0 ± 0.1 | 0.70 ± 0.001 | 351.4 ± 1.4 |
No | 66.54 ± 0.02 | 58.9 ± 0.1 | 290.6 ± 0.1 | 0.70 ± 0.001 | 269.3 ± 0.9 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
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. https://doi.org/10.3390/ijms22169068
Varma S, Orgel JPRO, Schieber JD. Contrasting Local and Macroscopic Effects of Collagen Hydroxylation. International Journal of Molecular Sciences. 2021; 22(16):9068. https://doi.org/10.3390/ijms22169068
Chicago/Turabian StyleVarma, Sameer, Joseph P. R. O. Orgel, and Jay D. Schieber. 2021. "Contrasting Local and Macroscopic Effects of Collagen Hydroxylation" International Journal of Molecular Sciences 22, no. 16: 9068. https://doi.org/10.3390/ijms22169068