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Structural insights into charge pair interactions in triple helical collagen-like proteins.

Fallas JA, Dong J, Tao YJ, Hartgerink JD
J Biol Chem 287 8039-47 (2012)
Related entries: 3t4f, 6vzx

Cited: 36 times
EuropePMC logo PMID: 22179819

Abstract

The collagen triple helix is the most abundant protein fold in humans. Despite its deceptively simple structure, very little is understood about its folding and fibrillization energy landscape. In this work, using a combination of x-ray crystallography and nuclear magnetic resonance spectroscopy, we carry out a detailed study of stabilizing pair-wise interactions between the positively charged lysine and the negatively charged amino acids aspartate and glutamate. We find important differences in the side chain conformation of amino acids in the crystalline and solution state. Structures from x-ray crystallography may have similarities to the densely packed triple helices of collagen fibers whereas solution NMR structures reveal the simpler interactions of isolated triple helices. In solution, two distinct types of contacts are observed: axial and lateral. Such register-specific interactions are crucial for the understanding of the registration process of collagens and the overall stability of proteins in this family. However, in the crystalline state, there is a significant rearrangement of the side chain conformation allowing for packing interactions between adjacent helices, which suggests that charged amino acids may play a dual role in collagen stabilization and folding, first at the level of triple helical assembly and second during fibril formation.

Articles - 3u29 mentioned but not cited (3)

  1. Structural insights into charge pair interactions in triple helical collagen-like proteins. Fallas JA, Dong J, Tao YJ, Hartgerink JD. J Biol Chem 287 8039-8047 (2012)
  2. Peptide tessellation yields micrometre-scale collagen triple helices. Tanrikulu IC, Forticaux A, Jin S, Raines RT. Nat Chem 8 1008-1014 (2016)
  3. The role of cross-chain ionic interactions for the stability of collagen model peptides. Keshwani N, Banerjee S, Brodsky B, Makhatadze GI. Biophys J 105 1681-1688 (2013)


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  1. Nanomaterials design and tests for neural tissue engineering. Saracino GA, Cigognini D, Silva D, Caprini A, Gelain F. Chem Soc Rev 42 225-262 (2013)
  2. Self-assemble peptide biomaterials and their biomedical applications. Chen J, Zou X. Bioact Mater 4 120-131 (2019)
  3. Rational design of fiber forming supramolecular structures. Kumar VA, Wang BK, Kanahara SM. Exp Biol Med (Maywood) 241 899-908 (2016)
  4. Pairwise interactions in collagen and the design of heterotrimeric helices. Jalan AA, Hartgerink JD. Curr Opin Chem Biol 17 960-967 (2013)
  5. Glycoproteins functionalized natural and synthetic polymers for prospective biomedical applications: A review. Tabasum S, Noreen A, Kanwal A, Zuber M, Anjum MN, Zia KM. Int J Biol Macromol 98 748-776 (2017)

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  1. Collagen-like peptides and peptide-polymer conjugates in the design of assembled materials. Luo T, Kiick KL. Eur Polym J 49 2998-3009 (2013)
  2. Noncovalent Modulation of the Inverse Temperature Transition and Self-Assembly of Elastin-b-Collagen-like Peptide Bioconjugates. Luo T, Kiick KL. J Am Chem Soc 137 15362-15365 (2015)
  3. Anti-citrullinated protein antibodies cause arthritis by cross-reactivity to joint cartilage. Ge C, Tong D, Liang B, Lönnblom E, Schneider N, Hagert C, Viljanen J, Ayoglu B, Stawikowska R, Nilsson P, Fields GB, Skogh T, Kastbom A, Kihlberg J, Burkhardt H, Dobritzsch D, Holmdahl R. JCI Insight 2 93688 (2017)
  4. Computational design of self-assembling register-specific collagen heterotrimers. Fallas JA, Hartgerink JD. Nat Commun 3 1087 (2012)
  5. Collagen- and hyaluronic acid-based hydrogels and their biomedical applications. Xu Q, Torres JE, Hakim M, Babiak PM, Pal P, Battistoni CM, Nguyen M, Panitch A, Solorio L, Liu JC. Mater Sci Eng R Rep 146 100641 (2021)
  6. Thermoresponsive Elastin-b-Collagen-Like Peptide Bioconjugate Nanovesicles for Targeted Drug Delivery to Collagen-Containing Matrices. Luo T, David MA, Dunshee LC, Scott RA, Urello MA, Price C, Kiick KL. Biomacromolecules 18 2539-2551 (2017)
  7. How electrostatic networks modulate specificity and stability of collagen. Zheng H, Lu C, Lan J, Fan S, Nanda V, Xu F. Proc Natl Acad Sci U S A 115 6207-6212 (2018)
  8. Thermoresponsive self-assembly of nanostructures from a collagen-like peptide-containing diblock copolymer. Luo T, He L, Theato P, Kiick KL. Macromol Biosci 15 111-123 (2015)
  9. Empirical estimation of local dielectric constants: Toward atomistic design of collagen mimetic peptides. Pike DH, Nanda V. Biopolymers 104 360-370 (2015)
  10. Temperature-controlled electrospray ionization mass spectrometry as a tool to study collagen homo- and heterotrimers. Köhler M, Marchand A, Hentzen NB, Egli J, Begley AI, Wennemers H, Zenobi R. Chem Sci 10 9829-9835 (2019)
  11. Design of net-charged abc-type collagen heterotrimers. Parmar AS, Zahid S, Belure SV, Young R, Hasan N, Nanda V. J Struct Biol 185 163-167 (2014)
  12. The role of collagen charge clusters in the modulation of matrix metalloproteinase activity. Lauer JL, Bhowmick M, Tokmina-Roszyk D, Lin Y, Van Doren SR, Fields GB. J Biol Chem 289 1981-1992 (2014)
  13. Enzymatic Phosphorylation of Ser in a Type I Collagen Peptide. Qiu Y, Poppleton E, Mekkat A, Yu H, Banerjee S, Wiley SE, Dixon JE, Kaplan DL, Lin YS, Brodsky B. Biophys J 115 2327-2335 (2018)
  14. Sequence recombination improves target specificity in a redesigned collagen peptide abc-type heterotrimer. Giddu S, Xu F, Nanda V. Proteins 81 386-393 (2013)
  15. ColGen: An end-to-end deep learning model to predict thermal stability of de novo collagen sequences. Yu CH, Khare E, Narayan OP, Parker R, Kaplan DL, Buehler MJ. J Mech Behav Biomed Mater 125 104921 (2022)
  16. Stabilization of collagen-model, triple-helical peptides for in vitro and in vivo applications. Bhowmick M, Fields GB. Methods Mol Biol 1081 167-194 (2013)
  17. Control of Collagen Stability and Heterotrimer Specificity through Repulsive Electrostatic Interactions. Parmar AS, Joshi M, Nosker PL, Hasan NF, Nanda V. Biomolecules 3 986-996 (2013)
  18. Discovering design principles of collagen molecular stability using a genetic algorithm, deep learning, and experimental validation. Khare E, Yu CH, Gonzalez Obeso C, Milazzo M, Kaplan DL, Buehler MJ. Proc Natl Acad Sci U S A 119 e2209524119 (2022)
  19. Mechanistic Insights into the Structural Stability of Collagen-Containing Biomaterials Such as Bones and Cartilage. Tiwari N, Wi S, Mentink-Vigier F, Sinha N. J Phys Chem B 125 4757-4766 (2021)
  20. Case Reports A novel COL1A1 variant in a family with clinical features of hypermobile Ehlers-Danlos syndrome that proved to be a COL1-related overlap disorder. Foy M, De Mazancourt P, Métay C, Carlier R, Allamand V, Gartioux C, Gillas F, Miri N, Jobic V, Mekki A, Richard P, Michot C, Benistan K. Clin Case Rep 9 e04128 (2021)
  21. Caloric restriction overcomes pre-diabetes and hypertension induced by a high fat diet and renal artery stenosis. de Souza Nunes Faria MS, Pimentel VE, Helaehil JV, Bertolo MC, Santos NTH, da Silva-Neto PV, Thomazini BF, de Oliveira CA, do Amaral MEC. Mol Biol Rep 49 5883-5895 (2022)
  22. Structure of collagen adsorbed on a model implant surface resolved by polarization modulation infrared reflection-absorption spectroscopy. Brand I, Habecker F, Ahlers M, Klüner T. Spectrochim Acta A Mol Biomol Spectrosc 138 216-224 (2015)
  23. Composition-dependent energetic contribution of complex salt bridges to collagen stability. Sun T, Qiang S, Lu C, Xu F. Biophys J 120 3429-3436 (2021)
  24. Incorporation of 'click' chemistry glycomimetics dramatically alters triple-helix stability in an adiponectin model peptide. Lutteroth KR, Harris PWR, Wright TH, Kaur H, Sparrow K, Yang SH, Cooper GJS, Brimble MA. Org Biomol Chem 15 5602-5608 (2017)
  25. Sequence position and side chain length dependence of charge pair interactions in collagen triple helices. Wei F, Fallas JA, Hartgerink JD. Macromol Rapid Commun 33 1445-1452 (2012)
  26. Dissecting MMP P10' and P11' subsite sequence preferences, utilizing a positional scanning, combinatorial triple-helical peptide library. Tokmina-Roszyk M, Fields GB. J Biol Chem 293 16661-16676 (2018)
  27. Selective covalent capture of collagen triple helices with a minimal protecting group strategy. Yu LT, Hartgerink JD. Chem Sci 13 2789-2796 (2022)
  28. Stability of collagen heterotrimer with same charge pattern and different charged residue identities. Huang Y, Lan J, Wu C, Zhang R, Zheng H, Fan S, Xu F. Biophys J 122 2686-2695 (2023)


Related citations provided by authors (1)

  1. Covalent Capture of Collagen Triple Helices Using Lysine-Aspartate and Lysine-Glutamate Pairs.. Hulgan SAH, Jalan AA, Li IC, Walker DR, Miller MD, Kosgei AJ, Xu W, Phillips GN, Hartgerink JD Biomacromolecules 21 3772-3781 (2020)

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