Microscopy Techniques for Investigating the Control of Organic Constituents on Biomineralization

Hendley, Coit T.; Tao, Jinhui; Kunitake, Jennie A.; De Yoreo, James J.; Estroff, Lara A.

doi:10.1557/mrs.2015.98

Title: Microscopy Techniques for Investigating the Control of Organic Constituents on Biomineralization

Journal Article · Sat Jun 06 00:00:00 EDT 2015 · MRS Bulletin

DOI:https://doi.org/10.1557/mrs.2015.98· OSTI ID:1581968

Hendley, Coit T. ^[1];

^[2]; Kunitake, Jennie A. ^[1]; De Yoreo, James J. ^[2]; Estroff, Lara A. ^[1]

Cornell University
BATTELLE (PACIFIC NW LAB)

In this paper we address recent advances in the application of microscopy techniques to characterize crystallization processes as they relate to biomineralization and bio-inspired materials synthesis. In particular, we focus on studies aimed at revealing the role that organic macromolecules and functionalized surfaces have in modulating the mechanisms of nucleation and growth. In the nucleation studies, we explore the use of methods such asin situ transmission electron microscopy (TEM),atomic force microscopy (AFM), and cryogenic electron microscopy (cryoEM)to delineate formation pathways, phase stabilization, and the competing effects of free energy and kinetic barriers. In the growth studies, an emphasis is placed on understanding the interactions of macromolecular constituents with growing crystals and how to characterize the internal structures of the resulting composite crystals using techniques such as electron tomography, atom probe tomography (APT), and vibrational spectromicroscopy. Examples are drawn from both biological and bio-inspired synthetic systems.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1581968

Report Number(s):: PNNL-SA-108196

Journal Information:: MRS Bulletin, Vol. 40, Issue 6

Country of Publication:: United States

Language:: English

References (101)

Raman Spectroscopy of Biological Tissues Talari, Abdullah Chandra Sekhar; Movasaghi, Zanyar; Rehman, Shazza Applied Spectroscopy Reviews, Vol. 50, Issue 1 https://doi.org/10.1080/05704928.2014.923902	journal	August 2014
The localization of occluded matrix proteins in calcareous spicules of sea urchin larvae Seto, Jong; Zhang, Yang; Hamilton, Patricia Journal of Structural Biology, Vol. 148, Issue 1 https://doi.org/10.1016/j.jsb.2004.04.001	journal	October 2004
A Quasi-Time-Resolved CryoTEM Study of the Nucleation of CaCO 3 under Langmuir Monolayers Pichon, Benoît P.; Bomans, Paul H. H.; Frederik, Peter M. Journal of the American Chemical Society, Vol. 130, Issue 12 https://doi.org/10.1021/ja710416h	journal	March 2008
Polarization-dependent Imaging Contrast (PIC) mapping reveals nanocrystal orientation patterns in carbonate biominerals Gilbert, Pupa U. P. A. Journal of Electron Spectroscopy and Related Phenomena, Vol. 185, Issue 10 https://doi.org/10.1016/j.elspec.2012.06.001	journal	October 2012
THE MATERIAL BONE: Structure-Mechanical Function Relations Weiner, S.; Wagner, H. D. Annual Review of Materials Science, Vol. 28, Issue 1 https://doi.org/10.1146/annurev.matsci.28.1.271	journal	August 1998
Atom probe tomography Miller, M. K.; Forbes, R. G. Materials Characterization, Vol. 60, Issue 6 https://doi.org/10.1016/j.matchar.2009.02.007	journal	June 2009
Observation of materials processes in liquids by electron microscopy Wang, Chong-Min; Liao, Hong-Gang; Ross, Frances M. MRS Bulletin, Vol. 40, Issue 1 https://doi.org/10.1557/mrs.2014.283	journal	January 2015
Cryo-TEM Analysis of Collagen Fibrillar Structure Quan, Bryan D.; Sone, Eli D. Methods in Enzymology, 189-205 https://doi.org/10.1016/B978-0-12-416617-2.00009-6	book	January 2013
Correction for Woolgar et al., Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex Proceedings of the National Academy of Sciences, Vol. 112, Issue 35 https://doi.org/10.1073/pnas.1513862112	journal	July 2015
Simultaneous Raman Microspectroscopy and Fluorescence Imaging of Bone Mineralization in Living Zebrafish Larvae Bennet, M.; Akiva, A.; Faivre, D. Biophysical Journal, Vol. 106, Issue 4 https://doi.org/10.1016/j.bpj.2014.01.002	journal	February 2014
Evaluation of strengthening mechanisms in calcite single crystals from mollusk shells Kunitake, Miki E.; Mangano, Lauren M.; Peloquin, John M. Acta Biomaterialia, Vol. 9, Issue 2 https://doi.org/10.1016/j.actbio.2012.09.030	journal	February 2013
A chemical model for the cooperation of sulfates and carboxylates in calcite crystal nucleation: Relevance to biomineralization Addadi, L.; Moradian, J.; Shay, E. Proceedings of the National Academy of Sciences, Vol. 84, Issue 9 https://doi.org/10.1073/pnas.84.9.2732	journal	May 1987
Ultrastructure and Crystallography of Nanoscale Calcite Building Blocks in Rhabdosphaera clavigera Coccolith Spines van de Locht, Renée; Slater, Thomas J. A.; Verch, Andreas Crystal Growth & Design, Vol. 14, Issue 4 https://doi.org/10.1021/cg4018486	journal	March 2014
Directly Probing the Effects of Ions on Hydration Forces at Interfaces Kilpatrick, Jason I.; Loh, Siu-Hong; Jarvis, Suzanne P. Journal of the American Chemical Society, Vol. 135, Issue 7 https://doi.org/10.1021/ja310255s	journal	February 2013
Amorphous intergranular phases control the properties of rodent tooth enamel Gordon, L. M.; Cohen, M. J.; MacRenaris, K. W. Science, Vol. 347, Issue 6223 https://doi.org/10.1126/science.1258950	journal	February 2015
Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography Rigort, A.; Bauerlein, F. J. B.; Villa, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 12 https://doi.org/10.1073/pnas.1201333109	journal	March 2012
Investigations of voids in the aragonite platelets of nacre Gries, Katharina; Kröger, Roland; Kübel, Christian Acta Biomaterialia, Vol. 5, Issue 8 https://doi.org/10.1016/j.actbio.2009.04.017	journal	October 2009
Observing growth steps of collagen self-assembly by time-lapse high-resolution atomic force microscopy Cisneros, David A.; Hung, Carlos; Franz, Clemens M. Journal of Structural Biology, Vol. 154, Issue 3 https://doi.org/10.1016/j.jsb.2006.02.006	journal	June 2006
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
Dynamic microscopy of nanoscale cluster growth at the solid–liquid interface Williamson, M. J.; Tromp, R. M.; Vereecken, P. M. Nature Materials, Vol. 2, Issue 8 https://doi.org/10.1038/nmat944	journal	July 2003
Subnanometer atomic force microscopy of peptide-mineral interactions links clustering and competition to acceleration and catastrophe Friddle, R. W.; Weaver, M. L.; Qiu, S. R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0908205107	journal	December 2009
Recent Advances in the Application of Electron Tomography to Materials Chemistry Leary, Rowan; Midgley, Paul A.; Thomas, John Meurig Accounts of Chemical Research, Vol. 45, Issue 10 https://doi.org/10.1021/ar3001102	journal	August 2012
Video imaging of walking myosin V by high-speed atomic force microscopy Kodera, Noriyuki; Yamamoto, Daisuke; Ishikawa, Ryoki Nature, Vol. 468, Issue 7320 https://doi.org/10.1038/nature09450	journal	October 2010
Self-assembly of amorphous calcium carbonate microlens arrays Lee, Kyubock; Wagermaier, Wolfgang; Masic, Admir Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1720	journal	January 2012
Microstructural control of calcite via incorporation of intracrystalline organic molecules in shells Okumura, Taiga; Suzuki, Michio; Nagasawa, Hiromichi Journal of Crystal Growth, Vol. 381 https://doi.org/10.1016/j.jcrysgro.2013.07.020	journal	October 2013
The grinding tip of the sea urchin tooth exhibits exquisite control over calcite crystal orientation and Mg distribution Ma, Y.; Aichmayer, B.; Paris, O. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0810300106	journal	March 2009
Nanostructure of Biogenic Calcite Crystals: A View by Small-Angle X-Ray Scattering Gilow, Christoph; Zolotoyabko, Emil; Paris, Oskar Crystal Growth & Design, Vol. 11, Issue 6 https://doi.org/10.1021/cg200136t	journal	June 2011
Energetic basis for the molecular-scale organization of bone Tao, Jinhui; Battle, Keith C.; Pan, Haihua Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1404481112	journal	December 2014
Biomineralization-inspired synthesis of functional organic/inorganic hybrid materials: organic molecular control of self-organization of hybrids Arakaki, Atsushi; Shimizu, Katsuhiko; Oda, Mayumi Organic & Biomolecular Chemistry, Vol. 13, Issue 4 https://doi.org/10.1039/C4OB01796J	journal	January 2015
Biomineralization as an Inspiration for Materials Chemistry Nudelman, Fabio; Sommerdijk, Nico A. J. M. Angewandte Chemie International Edition, Vol. 51, Issue 27 https://doi.org/10.1002/anie.201106715	journal	May 2012
In situ atomic force microscopy of layer-by-layer crystal growth and key growth concepts Rashkovich, L. N.; De Yoreo, J. J.; Orme, C. A. Crystallography Reports, Vol. 51, Issue 6 https://doi.org/10.1134/S1063774506060174	journal	December 2006
Hierarchical Calcite Crystals with Occlusions of a Simple Polyelectrolyte Mimic Complex Biomineral Structures Schenk, Anna S.; Zlotnikov, Igor; Pokroy, Boaz Advanced Functional Materials, Vol. 22, Issue 22 https://doi.org/10.1002/adfm.201201158	journal	July 2012
Biomineralization of limpet teeth: A cryo-TEM study of the organic matrix and the onset of mineral deposition Sone, Eli D.; Weiner, Steve; Addadi, Lia Journal of Structural Biology, Vol. 158, Issue 3 https://doi.org/10.1016/j.jsb.2007.01.001	journal	June 2007
Crystal Growth of Calcium Carbonate in Hydrogels as a Model of Biomineralization Asenath-Smith, Emily; Li, Hanying; Keene, Ellen C. Advanced Functional Materials, Vol. 22, Issue 14 https://doi.org/10.1002/adfm.201200300	journal	May 2012
Phase transitions in biogenic amorphous calcium carbonate Gong, Y. U. T.; Killian, C. E.; Olson, I. C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1118085109	journal	April 2012
Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth Gordon, Lyle M.; Joester, Derk Nature, Vol. 469, Issue 7329 https://doi.org/10.1038/nature09686	journal	January 2011
Calcite Prisms from Mollusk Shells (Atrina Rigida): Swiss-cheese-like Organic-Inorganic Single-crystal Composites Li, Hanying; Xin, Huolin L.; Kunitake, Miki E. Advanced Functional Materials, Vol. 21, Issue 11 https://doi.org/10.1002/adfm.201002709	journal	April 2011
Multiscale Contribution of Bone Tissue Material Property Heterogeneity to Trabecular Bone Mechanical Behavior Lloyd, Ashley A.; Wang, Zhen Xiang; Donnelly, Eve Journal of Biomechanical Engineering, Vol. 137, Issue 1 https://doi.org/10.1115/1.4029046	journal	January 2015
In Situ Atomic Force Microscopy as a Tool for Investigating Interactions and Assembly Dynamics in Biomolecular and Biomineral Systems De Yoreo, James J.; Chung, Sungwook; Friddle, Raymond W. Advanced Functional Materials, Vol. 23, Issue 20 https://doi.org/10.1002/adfm.201203424	journal	April 2013
X-Ray absorption spectroscopy studies on the structure of a biogenic “amorphous” calcium carbonate phase † Levi-Kalisman, Yael; Raz, Sefi; Weiner, Steve Journal of the Chemical Society, Dalton Transactions, Issue 21 https://doi.org/10.1039/b003242p	journal	January 2000
CryoTEM study of effects of phosphorylation on the hierarchical assembly of porcine amelogenin and its regulation of mineralization in vitro Fang, Ping-An; Margolis, Henry C.; Conway, James F. Journal of Structural Biology, Vol. 183, Issue 2 https://doi.org/10.1016/j.jsb.2013.05.011	journal	August 2013
Calcium carbonate nucleation driven by ion binding in a biomimetic matrix revealed by in situ electron microscopy Smeets, Paul J. M.; Cho, Kang Rae; Kempen, Ralph G. E. Nature Materials, Vol. 14, Issue 4 https://doi.org/10.1038/nmat4193	journal	January 2015
Crystal Growth Inhibitors for the Prevention of L-Cystine Kidney Stones Through Molecular Design Rimer, J. D.; An, Z.; Zhu, Z. Science, Vol. 330, Issue 6002 https://doi.org/10.1126/science.1191968	journal	October 2010
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
Rethinking Classical Crystal Growth Models through Molecular Scale Insights: Consequences of Kink-Limited Kinetics De Yoreo, J. J.; Zepeda-Ruiz, L. A.; Friddle, R. W. Crystal Growth & Design, Vol. 9, Issue 12 https://doi.org/10.1021/cg900543g	journal	December 2009
Cryo-electron tomography: 3-dimensional imaging of soft matter Nudelman, Fabio; de With, Gijsbertus; Sommerdijk, Nico A. J. M. Soft Matter, Vol. 7, Issue 1 https://doi.org/10.1039/C0SM00441C	journal	January 2011
Mineral Deposition in the Extracellular Matrices of Vertebrate Tissues: Identification of Possible Apatite Nucleation Sites on Type I Collagen Landis, William J.; Silver, Frederick H. Cells Tissues Organs, Vol. 189, Issue 1-4 https://doi.org/10.1159/000151454	journal	August 2008
Self-catalyzed growth of S layers via an amorphous-to-crystalline transition limited by folding kinetics Chung, S.; Shin, S. -H.; Bertozzi, C. R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 38 https://doi.org/10.1073/pnas.1008280107	journal	September 2010
Biomolecular Modification of Inorganic Crystal Growth De Yoreo, James J. PERSPECTIVES ON INORGANIC, ORGANIC, AND BIOLOGICAL CRYSTAL GROWTH: FROM FUNDAMENTALS TO APPLICATIONS: Basedon the lectures presented at the 13th International Summer School on Crystal Growth, AIP Conference Proceedings https://doi.org/10.1063/1.2751927	conference	January 2007
Frontiers of in situ electron microscopy Zheng, Haimei; Meng, Ying Shirley; Zhu, Yimei MRS Bulletin, Vol. 40, Issue 1 https://doi.org/10.1557/mrs.2014.305	journal	January 2015
A Unified Description of Attachment-Based Crystal Growth Zhang, Hengzhong; De Yoreo, James J.; Banfield, Jillian F. ACS Nano, Vol. 8, Issue 7 https://doi.org/10.1021/nn503145w	journal	June 2014
Polyanion-mediated mineralization ? assembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition Marsh, Mary E. Protoplasma, Vol. 177, Issue 3-4 https://doi.org/10.1007/BF01378985	journal	September 1994
An artificial biomineral formed by incorporation of copolymer micelles in calcite crystals Kim, Yi-Yeoun; Ganesan, Kathirvel; Yang, Pengcheng Nature Materials, Vol. 10, Issue 11 https://doi.org/10.1038/nmat3103	journal	September 2011
Prospects for Nanobiology with Atom-Probe Tomography Kelly, Thomas F.; Nishikawa, Osamu; Panitz, J. A. MRS Bulletin, Vol. 34, Issue 10 https://doi.org/10.1557/mrs2009.249	journal	October 2009
Three-Dimensional Atom-Probe Tomography: Advances and Applications Seidman, David N. Annual Review of Materials Research, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.matsci.37.052506.084200	journal	August 2007
Ultrastructural Localization of Proteins Involved in Sea Urchin Biomineralization Ameye, Laurent; Hermann, René; Killian, Christopher Journal of Histochemistry & Cytochemistry, Vol. 47, Issue 9 https://doi.org/10.1177/002215549904700911	journal	September 1999
Aggregation-induced growth and transformation of β-FeOOH nanorods to micron-sized α-Fe ₂ O ₃ spindles Frandsen, Cathrine; Legg, Benjamin A.; Comolli, Luis R. CrystEngComm, Vol. 16, Issue 8 https://doi.org/10.1039/C3CE40983J	journal	January 2014
Development and application of STEM for the biological sciences Sousa, Alioscka A.; Leapman, Richard D. Ultramicroscopy, Vol. 123 https://doi.org/10.1016/j.ultramic.2012.04.005	journal	December 2012
High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin Shibata, Mikihiro; Yamashita, Hayato; Uchihashi, Takayuki Nature Nanotechnology, Vol. 5, Issue 3 https://doi.org/10.1038/nnano.2010.7	journal	February 2010
The Initial Stages of Template-Controlled CaCO₃ Formation Revealed by Cryo-TEM Pouget, E. M.; Bomans, P. H. H.; Goos, J. A. C. M. Science, Vol. 323, Issue 5920, p. 1455-1458 https://doi.org/10.1126/science.1169434	journal	March 2009
Studying Collagen Self-Assembly by Time-Lapse High-Resolution Atomic Force Microscopy Franz, Clemens M.; Muller, Daniel J. Atomic Force Microscopy in Biomedical Research, 97–107 https://doi.org/10.1007/978-1-61779-105-5_7	book	January 2011
Nucleation and Growth of Monodisperse Silica Nanoparticles Carcouët, Camille C. M. C.; van de Put, Marcel W. P.; Mezari, Brahim Nano Letters, Vol. 14, Issue 3 https://doi.org/10.1021/nl404550d	journal	February 2014
Investigating Processes of Nanocrystal Formation and Transformation via Liquid Cell TEM Nielsen, Michael H.; Li, Dongsheng; Zhang, Hengzhong Microscopy and Microanalysis, Vol. 20, Issue 2 https://doi.org/10.1017/S1431927614000294	journal	March 2014
Crystallization Pathways in Biomineralization Weiner, Steve; Addadi, Lia Annual Review of Materials Research, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-matsci-062910-095803	journal	August 2011
Anisotropy of Chemical Bonds in Collagen Molecules Studied by X-ray Absorption Near-Edge Structure (XANES) Spectroscopy Lam, Raymond S. K.; Metzler, Rebecca A.; Gilbert, Pupa U. P. A. ACS Chemical Biology, Vol. 7, Issue 3 https://doi.org/10.1021/cb200260d	journal	December 2011
Current-induced transition from particle-by-particle to concurrent intercalation in phase-separating battery electrodes Li, Yiyang; El Gabaly, Farid; Ferguson, Todd R. Nature Materials, Vol. 13, Issue 12 https://doi.org/10.1038/nmat4084	journal	September 2014
Design, Fabrication, and Applications of In Situ Fluid Cell TEM Li, Dongsheng; Nielsen, Michael H.; De Yoreo, James J. Methods in Enzymology, 147-164 https://doi.org/10.1016/B978-0-12-416617-2.00007-2	book	January 2013
Vibrational Spectroscopic Imaging for the Evaluation of Matrix and Mineral Chemistry Gamsjaeger, S.; Mendelsohn, R.; Boskey, A. L. Current Osteoporosis Reports, Vol. 12, Issue 4 https://doi.org/10.1007/s11914-014-0238-8	journal	September 2014
Introduction of correlative light and airSEMTM microscopy imaging for tissue research under ambient conditions Solomonov, Inna; Talmi-Frank, Dalit; Milstein, Yonat Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep05987	journal	August 2014
The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer Weaver, J. C.; Milliron, G. W.; Miserez, A. Science, Vol. 336, Issue 6086 https://doi.org/10.1126/science.1218764	journal	June 2012
A High-speed Atomic Force Microscope for Studying Biological Macromolecules in Action Ando, Toshio; Kodera, Noriyuki; Naito, Yasuyuki ChemPhysChem, Vol. 4, Issue 11 https://doi.org/10.1002/cphc.200300795	journal	November 2003
Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages Amini, Shahrouz; Masic, Admir; Bertinetti, Luca Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4187	journal	January 2014
Hierarchical self-assembly of amelogenin and the regulation of biomineralization at the nanoscale Fang, P. -A.; Conway, J. F.; Margolis, H. C. Proceedings of the National Academy of Sciences, Vol. 108, Issue 34 https://doi.org/10.1073/pnas.1106228108	journal	August 2011
Initial stages of calcium uptake and mineral deposition in sea urchin embryos Vidavsky, N.; Addadi, S.; Mahamid, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1312833110	journal	December 2013
Overview of the amorphous precursor phase strategy in biomineralization Weiner, Steve; Mahamid, Julia; Politi, Yael Frontiers of Materials Science in China, Vol. 3, Issue 2 https://doi.org/10.1007/s11706-009-0036-x	journal	March 2009
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
Characterization of Ca-phosphate biological materials by scanning transmission X-ray microscopy (STXM) at the Ca L2,3-, P L2,3- and C K-edges Cosmidis, Julie; Benzerara, Karim; Nassif, Nadine Acta Biomaterialia, Vol. 12 https://doi.org/10.1016/j.actbio.2014.10.003	journal	January 2015
Transient amorphous calcium phosphate in forming enamel Beniash, Elia; Metzler, Rebecca A.; Lam, Raymond S. K. Journal of Structural Biology, Vol. 166, Issue 2 https://doi.org/10.1016/j.jsb.2009.02.001	journal	May 2009
The shell organic matrix of the crossed lamellar queen conch shell (Strombus gigas) Osuna-Mascaró, Antonio; Cruz-Bustos, Teresa; Benhamada, Sana Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 168 https://doi.org/10.1016/j.cbpb.2013.11.009	journal	February 2014
Observations of Multiscale, Stress-Induced Changes of Collagen Orientation in Tendon by Polarized Raman Spectroscopy Masic, Admir; Bertinetti, Luca; Schuetz, Roman Biomacromolecules, Vol. 12, Issue 11 https://doi.org/10.1021/bm201008b	journal	November 2011
Formation of chiral morphologies through selective binding of amino acids to calcite surface steps Orme, C. A.; Noy, A.; Wierzbicki, A. Nature, Vol. 411, Issue 6839 https://doi.org/10.1038/35081034	journal	June 2001
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
Vaterite Crystals Contain Two Interspersed Crystal Structures Kabalah-Amitai, L.; Mayzel, B.; Kauffmann, Y. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1232139	journal	April 2013
In situ TEM imaging of CaCO3 nucleation reveals coexistence of direct and indirect pathways Nielsen, M. H.; Aloni, S.; De Yoreo, J. J. Science, Vol. 345, Issue 6201 https://doi.org/10.1126/science.1254051	journal	September 2014
On the pathway of mineral deposition in larval zebrafish caudal fin bone Akiva, Anat; Malkinson, Guy; Masic, Admir Bone, Vol. 75 https://doi.org/10.1016/j.bone.2015.02.020	journal	June 2015
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
Nacre Protein Fragment Templates Lamellar Aragonite Growth Metzler, Rebecca A.; Evans, John Spencer; Killian, Christopher E. Journal of the American Chemical Society, Vol. 132, Issue 18 https://doi.org/10.1021/ja909735y	journal	May 2010
On the current role of atom probe tomography in materials characterization and materials science Marquis, Emmanuelle A.; Bachhav, Mukesh; Chen, Yimeng Current Opinion in Solid State and Materials Science, Vol. 17, Issue 5 https://doi.org/10.1016/j.cossms.2013.09.003	journal	October 2013
Visualizing the 3D Internal Structure of Calcite Single Crystals Grown in Agarose Hydrogels Li, Hanying; Xin, Huolin L.; Muller, David A. Science, Vol. 326, Issue 5957 https://doi.org/10.1126/science.1178583	journal	November 2009
Determination of Redox Reaction Rates and Orders by In Situ Liquid Cell Electron Microscopy of Pd and Au Solution Growth Sutter, Eli A.; Sutter, Peter W. Journal of the American Chemical Society, Vol. 136, Issue 48 https://doi.org/10.1021/ja508279v	journal	November 2014
Sub-Micrometer-Scale Mapping of Magnetite Crystals and Sulfur Globules in Magnetotactic Bacteria Using Confocal Raman Micro-Spectrometry Eder, Stephan H. K.; Gigler, Alexander M.; Hanzlik, Marianne PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0107356	journal	September 2014
Self-Assembly of Collagen on Flat Surfaces: The Interplay of Collagen–Collagen and Collagen–Substrate Interactions Narayanan, Badri; Gilmer, George H.; Tao, Jinhui Langmuir, Vol. 30, Issue 5 https://doi.org/10.1021/la4043364	journal	January 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
Colocation and role of polyphosphates and alkaline phosphatase in apatite biomineralization of elasmobranch tesserae Omelon, Sidney; Georgiou, John; Variola, Fabio Acta Biomaterialia, Vol. 10, Issue 9 https://doi.org/10.1016/j.actbio.2014.06.008	journal	September 2014
Reconciling disparate views of template-directed nucleation through measurement of calcite nucleation kinetics and binding energies Hamm, L. M.; Giuffre, A. J.; Han, N. Proceedings of the National Academy of Sciences, Vol. 111, Issue 4 https://doi.org/10.1073/pnas.1312369111	journal	January 2014
Atom Probe Tomography of Apatites and Bone-Type Mineralized Tissues Gordon, Lyle M.; Tran, Lawrence; Joester, Derk ACS Nano, Vol. 6, Issue 12 https://doi.org/10.1021/nn3049957	journal	November 2012
Immunolocalization of skeletal matrix proteins in tissue and mineral of the coral Stylophora pistillata Mass, T.; Drake, J. L.; Peters, E. C. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1408621111	journal	August 2014
Direct in Situ Determination of the Mechanisms Controlling Nanoparticle Nucleation and Growth Woehl, Taylor J.; Evans, James E.; Arslan, Ilke ACS Nano, Vol. 6, Issue 10 https://doi.org/10.1021/nn303371y	journal	September 2012
Direct Imaging of Individual Intrinsic Hydration Layers on Lipid Bilayers at Ångstrom Resolution Fukuma, Takeshi; Higgins, Michael J.; Jarvis, Suzanne P. Biophysical Journal, Vol. 92, Issue 10 https://doi.org/10.1529/biophysj.106.100651	journal	May 2007
3D electron microscopy in the physical sciences: the development of Z-contrast and EFTEM tomography Midgley, P. A.; Weyland, M. Ultramicroscopy, Vol. 96, Issue 3-4 https://doi.org/10.1016/S0304-3991(03)00105-0	journal	September 2003
Asprich Peptides Are Occluded in Calcite and Permanently Disorder Biomineral Crystals Metzler, Rebecca A.; Tribello, Gareth A.; Parrinello, Michele Journal of the American Chemical Society, Vol. 132, Issue 33 https://doi.org/10.1021/ja103089r	journal	August 2010

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