The role of confined collagen geometry in decreasing nucleation energy barriers to intrafibrillar mineralization

Kim, Doyoon; Lee, Byeongdu; Thomopoulos, Stavros; Jun, Young-Shin

doi:10.1038/s41467-018-03041-1

Title: The role of confined collagen geometry in decreasing nucleation energy barriers to intrafibrillar mineralization

Journal Article · Tue Mar 06 00:00:00 EST 2018 · Nature Communications

DOI:https://doi.org/10.1038/s41467-018-03041-1· OSTI ID:1427508

^[1];

^[2]; Thomopoulos, Stavros ^[3];

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Washington Univ., St. Louis, MO (United States). Dept. of Energy, Environmental & Chemical Engineering
Argonne National Lab. (ANL), Argonne, IL (United States). X-ray Science Division
Columbia Univ., New York, NY (United States). Dept. of Orthopedic Surgery

Mineralization of collagen is critical for the mechanical functions of bones and teeth. Calcium phosphate nucleation in collagenous structures follows distinctly different patterns in highly confined gap regions (nanoscale confinement) than in less confined extrafibrillar spaces (microscale confinement). Although the mechanism(s) driving these differences are still largely unknown, differences in the free energy for nucleation may explain these two mineralization behaviors. Here, we report on experimentally obtained nucleation energy barriers to intra- and extrafibrillar mineralization, using in situ X-ray scattering observations and classical nucleation theory. Polyaspartic acid, an extrafibrillar nucleation inhibitor, increases interfacial energies between nuclei and mineralization fluids. In contrast, the confined gap spaces inside collagen fibrils lower the energy barrier by reducing the reactive surface area of nuclei, decreasing the surface energy penalty. The confined gap geometry, therefore, guides the two-dimensional morphology and structure of bioapatite and changes the nucleation pathway by reducing the total energy barrier.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357; DMR-1608545; DMR-1608554

OSTI ID:: 1427508

Journal Information:: Nature Communications, Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 68 works

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References (64)

Small molecule-mediated control of hydroxyapatite growth: Free energy calculations benchmarked to density functional theory Xu, Zhijun; Yang, Yang; Wang, Ziqiu Journal of Computational Chemistry, Vol. 35, Issue 1 https://doi.org/10.1002/jcc.23474	journal	October 2013
The nanometre-scale physiology of bone: steric modelling and scanning transmission electron microscopy of collagen–mineral structure Alexander, Benjamin; Daulton, Tyrone L.; Genin, Guy M. Journal of The Royal Society Interface, Vol. 9, Issue 73 https://doi.org/10.1098/rsif.2011.0880	journal	February 2012
Crystallization by particle attachment in synthetic, biogenic, and geologic environments De Yoreo, J. J.; Gilbert, P. U. P. A.; Sommerdijk, N. A. J. M. Science, Vol. 349, Issue 6247 https://doi.org/10.1126/science.aaa6760	journal	July 2015
Control of Vertebrate Skeletal Mineralization by Polyphosphates Omelon, Sidney; Georgiou, John; Henneman, Zachary J. PLoS ONE, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pone.0005634	journal	May 2009
Mineralization of Collagen May Occur on Fibril Surfaces: Evidence from Conventional and High-Voltage Electron Microscopy and Three-Dimensional Imaging Landis, William J.; Hodgens, Karen J.; Song, Min Ja Journal of Structural Biology, Vol. 117, Issue 1 https://doi.org/10.1006/jsbi.1996.0066	journal	July 1996
Osmotic pressure induced tensile forces in tendon collagen Masic, Admir; Bertinetti, Luca; Schuetz, Roman Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6942	journal	January 2015
In Situ Evaluation of Calcium Phosphate Nucleation Kinetics and Pathways during Intra- and Extrafibrillar Mineralization of Collagen Matrices Kim, Doyoon; Lee, Byeongdu; Thomopoulos, Stavros Crystal Growth & Design, Vol. 16, Issue 9 https://doi.org/10.1021/acs.cgd.6b00864	journal	August 2016
Pre-nucleation clusters as solute precursors in crystallisation Gebauer, Denis; Kellermeier, Matthias; Gale, Julian D. Chem. Soc. Rev., Vol. 43, Issue 7 https://doi.org/10.1039/C3CS60451A	journal	January 2014
Prenucleation clusters and non-classical nucleation Gebauer, Denis; Cölfen, Helmut Nano Today, Vol. 6, Issue 6 https://doi.org/10.1016/j.nantod.2011.10.005	journal	December 2011
The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors Nudelman, Fabio; Pieterse, Koen; George, Anne Nature Materials, Vol. 9, Issue 12 https://doi.org/10.1038/nmat2875	journal	October 2010
The Calcification of Elastin in vitro Koutsopoulos, S.; Paschalakis, P. C.; Dalas, E. Langmuir, Vol. 10, Issue 7 https://doi.org/10.1021/la00019a066	journal	July 1994
The relationship between particle size and solubility Buckton, Graham; Beezer, Anthony E. International Journal of Pharmaceutics, Vol. 82, Issue 3 https://doi.org/10.1016/0378-5173(92)90184-4	journal	May 1992
Patterning a surface so as to speed nucleation from solution Hedges, Lester O.; Whitelam, Stephen Soft Matter, Vol. 8, Issue 33 https://doi.org/10.1039/c2sm26038g	journal	January 2012
Noncollagenous matrix proteins and their role in mineralization Boskey, Adele L. Bone and Mineral, Vol. 6, Issue 2 https://doi.org/10.1016/0169-6009(89)90044-5	journal	May 1989
Refinement of collagen–mineral interaction: A possible role for osteocalcin in apatite crystal nucleation, growth and development Chen, Ling; Jacquet, Robin; Lowder, Elizabeth Bone, Vol. 71 https://doi.org/10.1016/j.bone.2014.09.021	journal	February 2015
Irena : tool suite for modeling and analysis of small-angle scattering Ilavsky, Jan; Jemian, Peter R. Journal of Applied Crystallography, Vol. 42, Issue 2 https://doi.org/10.1107/S0021889809002222	journal	February 2009
Mineralization of Bones and Teeth Boskey, A. L. Elements, Vol. 3, Issue 6 https://doi.org/10.2113/GSELEMENTS.3.6.385	journal	December 2007
Interfacial Energies for Heterogeneous Nucleation of Calcium Carbonate on Mica and Quartz Li, Qingyun; Fernandez-Martinez, Alejandro; Lee, Byeongdu Environmental Science & Technology, Vol. 48, Issue 10 https://doi.org/10.1021/es405141j	journal	May 2014
In vitro apatite induction by osteopontin: Interfacial energy for hydroxyapatite nucleation on osteopontin Ito, Shuichi; Saito, Takashi; Amano, Kaori Journal of Biomedical Materials Research, Vol. 69A, Issue 1 https://doi.org/10.1002/jbm.a.20066	journal	January 2004
A solid-state NMR investigation of the structure of nanocrystalline hydroxyapatite Jäger, Christian; Welzel, Thea; Meyer-Zaika, Wolfgang Magnetic Resonance in Chemistry, Vol. 44, Issue 6 https://doi.org/10.1002/mrc.1774	journal	January 2006
Mineral and Organic Matrix Interaction in Normally Calcifying Tendon Visualized in Three Dimensions by High-Voltage Electron Microscopic Tomography and Graphic Image Reconstruction Landis, W. J.; Song, M. J.; Leith, A. Journal of Structural Biology, Vol. 110, Issue 1 https://doi.org/10.1006/jsbi.1993.1003	journal	January 1993
Theoretical analysis of calcium phosphate precipitation in simulated body fluid Lu, Xiong; Leng, Yang Biomaterials, Vol. 26, Issue 10 https://doi.org/10.1016/j.biomaterials.2004.05.034	journal	April 2005
Nanogeochemistry: Nanostructures, emergent properties and their control on geochemical reactions and mass transfers Wang, Yifeng Chemical Geology, Vol. 378-379 https://doi.org/10.1016/j.chemgeo.2014.04.007	journal	June 2014
Bone structure and formation: A new perspective Olszta, Matthew J.; Cheng, Xingguo; Jee, Sang Soo Materials Science and Engineering: R: Reports, Vol. 58, Issue 3-5 https://doi.org/10.1016/j.mser.2007.05.001	journal	November 2007
Water-driven structure transformation in nanoparticles at room temperature Zhang, Hengzhong; Gilbert, Benjamin; Huang, Feng Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01845	journal	August 2003
Molecular mechanisms for intrafibrillar collagen mineralization in skeletal tissues Xu, Zhijun; Yang, Yang; Zhao, Weilong Biomaterials, Vol. 39 https://doi.org/10.1016/j.biomaterials.2014.10.048	journal	January 2015
The role of poly(aspartic acid) in the precipitation of calcium phosphate in confinement Cantaert, Bram; Beniash, Elia; Meldrum, Fiona C. Journal of Materials Chemistry B, Vol. 1, Issue 48 https://doi.org/10.1039/c3tb21296c	journal	January 2013
Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate Habraken, Wouter J. E. M.; Tao, Jinhui; Brylka, Laura J. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2490	journal	February 2013
Manipulating Crystal Growth and Polymorphism by Confinement in Nanoscale Crystallization Chambers Hamilton, Benjamin D.; Ha, Jeong-Myeong; Hillmyer, Marc A. Accounts of Chemical Research, Vol. 45, Issue 3 https://doi.org/10.1021/ar200147v	journal	October 2011
Principles of Crystal Nucleation and Growth De Yoreo, J. J. Reviews in Mineralogy and Geochemistry, Vol. 54, Issue 1 https://doi.org/10.2113/0540057	journal	January 2003
In situ Investigations of Carbonate Nucleation on Mineral and Organic Surfaces De Yoreo, J. J.; Waychunas, G. A.; Jun, Y. -S. Reviews in Mineralogy and Geochemistry, Vol. 77, Issue 1 https://doi.org/10.2138/rmg.2013.77.7	journal	January 2013
Synthetic amorphous calcium phosphate and its relation to bone mineral structure Posner, Aaron S.; Betts, Foster Accounts of Chemical Research, Vol. 8, Issue 8 https://doi.org/10.1021/ar50092a003	journal	August 1975
The role of prenucleation clusters in surface-induced calcium phosphate crystallization Dey, Archan; Bomans, Paul H. H.; Müller, Frank A. Nature Materials, Vol. 9, Issue 12 https://doi.org/10.1038/nmat2900	journal	November 2010
Effects of Coupled Chemo-Mechanical Processes on the Evolution of Pore-Size Distributions in Geological Media Emmanuel, Simon; Anovitz, Lawrence M.; Day-Stirrat, Ruarri J. Reviews in Mineralogy and Geochemistry, Vol. 80, Issue 1 https://doi.org/10.2138/rmg.2015.03	journal	January 2015
Now You See Them Meldrum, Fiona C.; Sear, Richard P. Science, Vol. 322, Issue 5909 https://doi.org/10.1126/science.1167221	journal	December 2008
Development of bone-like composites via the polymer-induced liquid-precursor (PILP) process. Part 1: Influence of polymer molecular weight Jee, Sang-Soo; Thula, Taili T.; Gower, Laurie B. Acta Biomaterialia, Vol. 6, Issue 9 https://doi.org/10.1016/j.actbio.2010.03.036	journal	September 2010
Crystal Size, Morphology, and Growth Mechanism in Bio-Inspired Apatite Nanocrystals Delgado-López, José Manuel; Frison, Ruggero; Cervellino, Antonio Advanced Functional Materials, Vol. 24, Issue 8 https://doi.org/10.1002/adfm.201302075	journal	September 2013
Simple and accurate methods for quantifying deformation, disruption, and development in biological tissues Boyle, John J.; Kume, Maiko; Wyczalkowski, Matthew A. Journal of The Royal Society Interface, Vol. 11, Issue 100 https://doi.org/10.1098/rsif.2014.0685	journal	November 2014
The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite Wang, Yan; Azaïs, Thierry; Robin, Marc Nature Materials, Vol. 11, Issue 8 https://doi.org/10.1038/nmat3362	journal	July 2012
The mineralization of collagen in vitro Koutsoukos, P. G.; Nancollas, G. H. Colloids and Surfaces, Vol. 28 https://doi.org/10.1016/0166-6622(87)80176-2	journal	January 1987
Glassy Carbon as an Absolute Intensity Calibration Standard for Small-Angle Scattering Zhang, Fan; Ilavsky, Jan; Long, Gabrielle G. Metallurgical and Materials Transactions A, Vol. 41, Issue 5 https://doi.org/10.1007/s11661-009-9950-x	journal	August 2009
Solubility of Ca5{P04)3OH in the System Ca{OH)2-H3P04-H20 at 5, 15, 25, and 37 °C McDowell, H.; Gregory, T. M.; Brown, W. E. Journal of Research of the National Bureau of Standards Section A: Physics and Chemistry, Vol. 81A, Issue 1 https://doi.org/10.6028/jres.081A.017	journal	April 1977
Small Angle X-ray Scattering for Nanoparticle Research Li, Tao; Senesi, Andrew J.; Lee, Byeongdu Chemical Reviews, Vol. 116, Issue 18 https://doi.org/10.1021/acs.chemrev.5b00690	journal	April 2016
Microfibrillar structure of type I collagen in situ Orgel, J. P. R. O.; Irving, T. C.; Miller, A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 24 https://doi.org/10.1073/pnas.0502718103	journal	June 2006
The use of physiological solutions or media in calcium phosphate synthesis and processing Tas, A. Cuneyt Acta Biomaterialia, Vol. 10, Issue 5 https://doi.org/10.1016/j.actbio.2013.12.047	journal	May 2014
Bone mineralization pathways during the rapid growth of embryonic chicken long bones Kerschnitzki, Michael; Akiva, Anat; Ben Shoham, Adi Journal of Structural Biology, Vol. 195, Issue 1 https://doi.org/10.1016/j.jsb.2016.04.011	journal	July 2016
One-to-One Correspondence Growth Mechanism of Gourd-like SiO _x Nanotubes Na, Han Gil; Choi, Sun-Woo; Park, Suyoung Crystal Growth & Design, Vol. 16, Issue 6 https://doi.org/10.1021/acs.cgd.5b01473	journal	April 2016
Particle size distributions from small-angle scattering using global scattering functions Beaucage, G.; Kammler, H. K.; Pratsinis, S. E. Journal of Applied Crystallography, Vol. 37, Issue 4 https://doi.org/10.1107/S0021889804008969	journal	July 2004
Effect of Chelation Chemistry of Sodium Polyaspartate on the Dissolution of Calcite Wu, You-Ting; Grant, Christine Langmuir, Vol. 18, Issue 18 https://doi.org/10.1021/la011839a	journal	September 2002
An X-ray radial distribution study of amorphous calcium phosphate Betts, F.; Posner, A. S. Materials Research Bulletin, Vol. 9, Issue 3 https://doi.org/10.1016/0025-5408(74)90087-7	journal	March 1974
Nanoscale Confinement Controls the Crystallization of Calcium Phosphate: Relevance to Bone Formation Cantaert, Bram; Beniash, Elia; Meldrum, Fiona C. Chemistry - A European Journal, Vol. 19, Issue 44 https://doi.org/10.1002/chem.201302835	journal	September 2013
Effect of Nanoscale Confinement on the Crystallization of Potassium Ferrocyanide Anduix-Canto, Clara; Kim, Yi-Yeoun; Wang, Yun-Wei Crystal Growth & Design, Vol. 16, Issue 9 https://doi.org/10.1021/acs.cgd.6b00894	journal	August 2016
Heterogeneous Nucleation and Growth of Nanoparticles at Environmental Interfaces Jun, Young-Shin; Kim, Doyoon; Neil, Chelsea W. Accounts of Chemical Research, Vol. 49, Issue 9 https://doi.org/10.1021/acs.accounts.6b00208	journal	August 2016
Crystallization in pores Scherer, George W. Cement and Concrete Research, Vol. 29, Issue 8 https://doi.org/10.1016/S0008-8846(99)00002-2	journal	August 1999
Mapping amorphous calcium phosphate transformation into crystalline mineral from the cell to the bone in zebrafish fin rays Mahamid, J.; Aichmayer, B.; Shimoni, E. Proceedings of the National Academy of Sciences, Vol. 107, Issue 14 https://doi.org/10.1073/pnas.0914218107	journal	March 2010
Association of Calcium and Phosphate Ions with Collagen in the Mineralization of Vertebrate Tissues Landis, William J.; Jacquet, Robin Calcified Tissue International, Vol. 93, Issue 4 https://doi.org/10.1007/s00223-013-9725-7	journal	March 2013
Mechanism of apatite formation on CaOSiO2P2O5 glasses in a simulated body fluid Ohtsuki, Chikara; Kokubo, Tadashi; Yamamuro, Takao Journal of Non-Crystalline Solids, Vol. 143 https://doi.org/10.1016/S0022-3093(05)80556-3	journal	January 1992
Molecular mechanics of mineralized collagen fibrils in bone Nair, Arun K.; Gautieri, Alfonso; Chang, Shu-Wei Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2720	journal	April 2013
Failure to detect an amorphous calcium-phosphate solid phase in bone mineral: A radial distribution function study Grynpas, Marc D.; Bonar, Laurence C.; Glimcher, Melvin J. Calcified Tissue International, Vol. 36, Issue 1 https://doi.org/10.1007/bf02405333	journal	December 1984
Growth units and nucleation: The case of calcium phosphates Boistelle, Roland; Lopez-Valero, Isabel Journal of Crystal Growth, Vol. 102, Issue 3 https://doi.org/10.1016/0022-0248(90)90420-p	journal	May 1990
Crystallization under nanoscale confinement Jiang, Qi; Ward, Michael D. Chem. Soc. Rev., Vol. 43, Issue 7 https://doi.org/10.1039/c3cs60234f	journal	January 2014
Heterogeneous Nucleation in and out of Pores Page, Amanda J.; Sear, Richard P. Physical Review Letters, Vol. 97, Issue 6 https://doi.org/10.1103/physrevlett.97.065701	journal	August 2006
Small-angle scattering in materials science - a short review of applications in alloys, ceramics and composite materials Fratzl, Peter Journal of Applied Crystallography, Vol. 36, Issue 3 https://doi.org/10.1107/s0021889803000335	journal	April 2003
Bone and Tooth Mineralization: Why Apatite? Pasteris, J. D.; Wopenka, B.; Valsami-Jones, E. Elements, Vol. 4, Issue 2 https://doi.org/10.2113/gselements.4.2.97	journal	April 2008

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