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Protein & Peptide Letters

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ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

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Research Article

Concentration-mediated Folding and Unfolding of Collagen Triple Helix

Author(s): Caihong Fu, Wenhua Li, Xiuxia Sun* and Jianxi Xiao*

Volume 30, Issue 1, 2023

Published on: 19 December, 2022

Page: [85 - 91] Pages: 7

DOI: 10.2174/0929866530666221125163837

Price: $65

Abstract

Background: Collagen has been widely utilized in tissue engineering, regenerative medicine and cosmetics. Collagen of low concentrations is frequently applied to reduce the production cost, while it may result in the loss of triple helical structure and bioactivity. CD and NMR techniques have enhanced our understanding of collagen triple helix, while they require high concentrations of collagen samples.

Objective: We have systematically investigated the folding and unfolding features of collagen mimetic peptides at a broad variety of concentrations in order to decipher the role of the concentration in the triple helical stability.

Methods: Peptide FAM-G(POG)10 was synthesized by the solid phase synthesis method. Fluorescence spectra of peptide FAM-G(POG)10 at different concentrations were recorded. The unfolding and folding profiles of peptide FAM-G(POG)10 with concentrations varying from 1 nM to 100 μM were examined. The effect of concentration on the folding and unfolding capability of peptide FAMG( POG)10 was investigated.

Results: Fluorescence characterization of peptide FAM-G(POG)10 under widely varying concentrations from 1 nM to 100 μM has revealed that concentration played a critical role in the stability of collagen peptides. The two-phase pattern of the concentration-dependent folding and unfolding curves has for the first time demonstrated the presence of a critical concentration for the collagen peptide to trigger the complete folding of the triple helix and to maintain the triple helix structure. It is noteworthy that the triple helix structure of collagen peptides was very stable at μM-level concentrations from both the folding and unfolding perspectives.

Conclusion: It has significantly contributed to our understanding of collagen triple helix stability at low and ultra-low concentrations, and provided valuable and practical guidelines for the preparation of collagen-based products.

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[1]
Piez, K.A.; Miller, A. The structure of collagen fibrils. J. Supramol. Struct., 1974, 2(2-4), 121-137.
[http://dx.doi.org/10.1002/jss.400020207] [PMID: 4437176]
[2]
Montes, G.; Bezerra, M.; Junqueira, L. Collagen distribution in tissues. In: Ultrastructure of the Connective Tissue Matrix. Electron Microscopy in Biology and Medicine Springer: Boston, MA,, 1984, 3, 65-68.
[http://dx.doi.org/10.1007/978-1-4613-2831-5_3]
[3]
Shoulders, M.D.; Raines, R.T. Collagen structure and stability. Annu. Rev. Biochem., 2009, 78(1), 929-958.
[http://dx.doi.org/10.1146/annurev.biochem.77.032207.120833] [PMID: 19344236]
[4]
Brodsky, B.; Persikov, A.V. Molecular structure of the collagen triple helix. Adv. Protein Chem., 2005, 70, 301-339.
[http://dx.doi.org/10.1016/S0065-3233(05)70009-7] [PMID: 15837519]
[5]
Baum, J.; Brodsky, B. Folding of peptide models of collagen and misfolding in disease. Curr. Opin. Struct. Biol., 1999, 9(1), 122-128.
[http://dx.doi.org/10.1016/S0959-440X(99)80016-5] [PMID: 10047579]
[6]
Koide, T. Designed triple-helical peptides as tools for collagen biochemistry and matrix engineering. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2007, 362(1484), 1281-1291.
[http://dx.doi.org/10.1098/rstb.2007.2115] [PMID: 17581806]
[7]
Li, G.Y.; Fukunaga, S.; Takenouchi, K.; Nakamura, F. Comparative study of the physiological properties of collagen, gelatin and collagen hydrolysate as cosmetic materials. Int. J. Cosmet. Sci., 2005, 27(2), 101-106.
[http://dx.doi.org/10.1111/j.1467-2494.2004.00251.x] [PMID: 18492159]
[8]
Brodsky, B.; Thiagarajan, G.; Madhan, B.; Kar, K. Triple-helical peptides: An approach to collagen conformation, stability, and self-association. Biopolymers, 2008, 89(5), 345-353.
[http://dx.doi.org/10.1002/bip.20958] [PMID: 18275087]
[9]
Kuivaniemi, H.; Tromp, G.; Prockop, D.J. Mutations in fibrillar collagens (types I, II, III, and XI), fibril-associated collagen (type IX), and network-forming collagen (type X) cause a spectrum of diseases of bone, cartilage, and blood vessels. Hum. Mutat., 1997, 9(4), 300-315.
[http://dx.doi.org/10.1002/(SICI)1098-1004(1997)9:4<300::AIDHUMU2>3.0.CO;2-9] [PMID: 9101290]
[10]
Malfait, F.; Symoens, S.; Vanderhaeghen, Y.; Naeyaert, J.; Goemans, N.; Holmberg, E.; Petersen, M.; Coucke, P.; Depaepe, A. EDS/OI caused by collagen type I mutations. Matrix Biol., 2006, 25, S66-S67.
[http://dx.doi.org/10.1016/j.matbio.2006.08.183]
[11]
Magalhaes, O.A.; Rohenkohl, H.C.; de Souza, L.T.; Schuler-Faccini, L.; Félix, T.M.; Collagen, I. Collagen I defect corneal profiles in osteogenesis imperfecta. Cornea, 2018, 37(12), 1561-1565.
[http://dx.doi.org/10.1097/ICO.0000000000001764] [PMID: 30272615]
[12]
Xiao, J.; Madhan, B.; Li, Y.; Brodsky, B.; Baum, J. Osteogenesis imperfecta model peptides: Incorporation of residues replacing Gly within a triple helix achieved by renucleation and local flexibility. Biophys. J., 2011, 101(2), 449-458.
[http://dx.doi.org/10.1016/j.bpj.2011.06.017] [PMID: 21767498]
[13]
Jenkins, C.L.; Raines, R.T. Insights on the conformational stability of collagen. Nat. Prod. Rep., 2002, 19(1), 49-59.
[http://dx.doi.org/10.1039/a903001h] [PMID: 11902439]
[14]
Baum, J.; Brodsky, B. Triple-helix folding and its role in collagen diseases. 1998, 12(8), A-1328.
[15]
Abou Neel, E.A.; Bozec, L.; Knowles, J.C.; Syed, O.; Mudera, V.; Day, R.; Hyun, J.K. Collagen-Emerging collagen based therapies hit the patient. Adv. Drug Deliv. Rev., 2013, 65(4), 429-456.
[http://dx.doi.org/10.1016/j.addr.2012.08.010] [PMID: 22960357]
[16]
Meyer, M. Processing of collagen based biomaterials and the resulting materials properties. Biomed. Eng. Online, 2019, 18(1), 24.
[http://dx.doi.org/10.1186/s12938-019-0647-0] [PMID: 30885217]
[17]
Sapudom, J.; Rubner, S.; Martin, S.; Kurth, T.; Riedel, S.; Mierke, C.T.; Pompe, T. The phenotype of cancer cell invasion controlled by fibril diameter and pore size of 3D collagen networks. Biomaterials, 2015, 52, 367-375.
[http://dx.doi.org/10.1016/j.biomaterials.2015.02.022] [PMID: 25818443]
[18]
Ramshaw, J. Applications of collagen in medical devices. Biomed. Eng., 2012, 13, S1016237201000042.
[http://dx.doi.org/10.4015/S1016237201000042]
[19]
Socrates, R.; Nagarajan, S.; Bechelany, M.; Kalkura, N. Collagen based biomaterials for tissue engineering applications. Materials, 2010, 3(3), 1863-1887.
[20]
Wallace, D.; Rosenblatt, J. Collagen gel systems for sustained delivery and tissue engineering. Adv. Drug Deliv. Rev., 2003, 55(12), 1631-1649.
[http://dx.doi.org/10.1016/j.addr.2003.08.004] [PMID: 14623405]
[21]
Avila Rodríguez, M.I.; Rodríguez Barroso, L.G.; Sánchez, M.L. Collagen: A review on its sources and potential cosmetic applications. J. Cosmet. Dermatol., 2018, 17(1), 20-26.
[http://dx.doi.org/10.1111/jocd.12450] [PMID: 29144022]
[22]
Sorushanova, A.; Delgado, L.M.; Wu, Z.; Shologu, N.; Kshirsagar, A.; Raghunath, R.; Mullen, A.; Bayon, Y.; Pandit, A.; Raghunath, M.; Zeugolis, D. The collagen suprafamily: From biosynthesis to advanced biomaterial development. Adv. Mater., 2019, 31(1)e1801651
[http://dx.doi.org/10.1002/adma.201801651]
[23]
Beck, K.; Chan, V.C.; Shenoy, N.; Kirkpatrick, A.; Ramshaw, J.A.M.; Brodsky, B. Destabilization of osteogenesis imperfecta collagen-like model peptides correlates with the identity of the residue replacing glycine. Proc. Natl. Acad. Sci. USA, 2000, 97(8), 4273-4278.
[http://dx.doi.org/10.1073/pnas.070050097] [PMID: 10725403]
[24]
Bhatnagar, R.; Gough, C. Circular dichroism of collagen and related polypeptides. In: Circular Dichroism and the Conformational Analysis of Biomolecules; Springer: Boston, MA, 1996.
[http://dx.doi.org/10.1007/978-1-4757-2508-7_6]
[25]
Toniolo, C.; Formaggio, F.; Woody, R. Electronic circular dichroism of peptides. In: Comprehensive Chiroptical Spectroscopy; Wiley Online, 2012; pp. 499-544.
[http://dx.doi.org/10.1002/9781118120392.ch15]
[26]
Lisitza, N.; Huang, X.; Hatabu, H.; Patz, S. Exploring collagen self-assembly by NMR. Phys. Chem. Chem. Phys., 2010, 12(42), 14169-14171.
[http://dx.doi.org/10.1039/c0cp00651c] [PMID: 20877840]
[27]
Madhan, B.; Xiao, J.; Thiagarajan, G.; Baum, J.; Brodsky, B. NMR monitoring of chain-specific stability in heterotrimeric collagen peptides. J. Am. Chem. Soc., 2008, 130(41), 13520-13521.
[http://dx.doi.org/10.1021/ja805496v]
[28]
Buevich, A.V.; Dai, Q.H.; Liu, X.; Brodsky, B.; Baum, J. Site-specific NMR monitoring of cis-trans isomerization in the folding of the proline-rich collagen triple helix. Biochemistry, 2000, 39(15), 4299-4308.
[http://dx.doi.org/10.1021/bi992584r] [PMID: 10757978]
[29]
Baum, J.; Brodsky, B. Real-time NMR investigations of triple-helix folding and collagen folding diseases. Fold. Des., 1997, 2(4), R53-R60.
[http://dx.doi.org/10.1016/S1359-0278(97)00028-X] [PMID: 9269560]
[30]
Zhang, Z-B.; Wang, J-J.; Chen, H-J.; Xiong, Q-Q.; Liu, L-R.; Zhang, Q-Q. Study of collagen mimetic peptide’s triple-helix structure and its thermostability by circular dichroism. Spectroscop. Spectral. Anal., 2014, 34(4), 1050-1055.
[http://dx.doi.org/10.3964/j.issn.1000-0593(2014)04-1050-06]
[31]
Nashchekina, Y.A.; Yudintceva, N.M.; Nikonov, P.O.; Ivanova, E.A.; Smagina, L.V.; Voronkina, I.V. Effect of concentration of collagen gel on functional activity of bone marrow mesenchymal stromal cells. Bull. Exp. Biol. Med., 2017, 163(1), 123-128.
[http://dx.doi.org/10.1007/s10517-017-3751-9] [PMID: 28580492]
[32]
Fang, M.; Goldstein, E.L.; Matich, E.K.; Orr, B.G.; Banaszak Holl, M.M.; Type, I. Type I collagen self-assembly: The roles of substrate and concentration. Langmuir, 2013, 29(7), 2330-2338.
[http://dx.doi.org/10.1021/la3048104] [PMID: 23339654]
[33]
Peng, Y.; Glattauer, V.; Werkmeister, J.A.; Ramshaw, J.A.M. Evaluation for collagen products for cosmetic application. Int. J. Cosmet. Sci., 2004, 26(6), 313.
[http://dx.doi.org/10.1111/j.1467-2494.2004.00245_2.x] [PMID: 15386024]
[34]
Samad, N.; Sikarwar, A. Collagen: New dimension in cosmetic and healthcare. Int. J. Biochem. Res. Rev., 2016, 14(3), 1-8.
[http://dx.doi.org/10.9734/IJBCRR/2016/27271]
[35]
Sun, X.; Fan, J.; Li, X.; Zhang, S.; Liu, X.; Xiao, J. Colorimetric and fluorometric monitoring of the helix composition of collagen-like peptides at the nM level. Chem. Commun., 2016, 52(15), 3107-3110.
[http://dx.doi.org/10.1039/C5CC09565D] [PMID: 26692232]
[36]
Sun, X.X.; Fan, J.; Hou, Y.N.; Liang, S.; Zhang, Y.P.; Xiao, J.X. Fluorescence characterization of the thermal stability of collagen mimic peptides. Chin. Chem. Lett., 2017, 28(5), 963-967.
[http://dx.doi.org/10.1016/j.cclet.2016.11.029]

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