Abstract
This article addresses recent advances in the application of microscopy techniques to characterize crystallization processes as they relate to biomineralization and bioinspired materials synthesis. In particular, we focus on studies aimed at revealing the role organic macromolecules and functionalized surfaces play in modulating the mechanisms of nucleation and growth. In nucleation studies, we explore the use of methods such as in situ transmission electron microscopy, atomic force microscopy, and cryogenic electron microscopy to delineate formation pathways, phase stabilization, and the competing effects of free energy and kinetic barriers. In growth studies, we emphasize understanding the interactions of macromolecular constituents with growing crystals and characterization of the internal structures of the resulting composite crystals using techniques such as electron tomography, atom probe tomography, and vibrational spectromicroscopy. Examples are drawn from both biological and bioinspired synthetic systems.
Similar content being viewed by others
References
H. Lowenstam, S. Weiner, On Biomineralization ( Oxford University Press, New york, 1989 ).
P.M. Dove, J.J. De Yoreo, S. Weiner, Eds., Biomineralization ( Mineral Society of America, Washington, DC, 2003 ).
E. Asenath-Smith, H. Li, E.C. Keene, Z.W. Seh, L.A. Estroff, Adv. Funct. Mater. 22, 2891 ( 2012 ).
F. Nudelman, N.A.J.M. Sommerdijk, Angew. Chem. Int. Ed. 51, 6582 ( 2012 ).
A. Arakaki, K. Shimizu, M. Oda, T. Sakamoto, T. Nishimura, T. Kato, Org. Biomol. Chem. 13, 974 ( 2014 ).
C.M. Franz, D.J. Muller, Methods Mol. Biol. 736, 97 ( 2011 ).
J.J. De Yoreo, AIP Conf. Proc. 916, 416 ( 2007 ).
L.N. Rashkovich, J.J. De Yoreo, C.A. Orme, A.A. Chernov, Crystallogr. Rep. 51, 1063 ( 2006 ).
D.A. Cisneros, C. Hung, C.M. Franz, D.J. Muller, J. Struct. Biol. 154, 232 (2006).
S. Chung, S.-H. Shin, C.R. Bertozzi, J.J. De Yoreo, Proc. Natl. Acad. Sci. U.S.A. 107, 16536 ( 2010 ).
B. Narayanan, G.H. Gilmer, J. Tao, J.J. De Yoreo, C.V. Ciobanu, Langmuir 30, 1343 ( 2014 ).
W.J.E.M. Habraken, J. Tao, L.J. Brylka, H. Friedrich, L. Bertinetti, A.S. Schenk, A. Verch, V. Dmitrovic, P.H.H. Bomans, P.M. Frederik, J. Laven, P. van der Schoot, B. Aichmayer, G. de With, J.J. De Yoreo, N.A.J.M. Sommerdijk, Nat. Commun. 4, 1507 ( 2013 ).
L.M. Hamm, A.J. Giuffre, N. Han, J. Tao, D. Wang, J.J. De Yoreo, P.M. Dove, Proc. Natl. Acad. Sci. U.S.A. 111, 1304 ( 2014 ).
J.D. Rimer, Z. An, Z. Zhu, M.H. Lee, D.S. Goldfarb, J.A. Wesson, M.D. Ward, Science 330, 337 ( 2010 ).
C.A. Orme, A. Noy, A. Wierzbicki, M.T. McBride, M. Grantham, H.H. Teng, P.M. Dove, J.J. De Yoreo, Nature 411, 775 ( 2001 ).
K.N. Olafson, M.A. Ketchum, J.D. Rimer, P.G. Vekilov, Proc. Natl. Acad. Sci. U.S.A. 112, 4969 ( 2015 ).
J.J. De Yoreo, L.A. Zepeda-Ruiz, R.W. Friddle, S.R. Qiu, L.E. Wasylenki, A.A. Chernov, G.H. Gilmer, P.M. Dove, Cryst. Growth Des. 9, 5135 ( 2009 ).
R.W. Friddle, M.L. Weaver, S.R. Qiu, A. Wierzbicki, W.H. Casey, J.J. De Yoreo, Proc. Natl. Acad. Sci. U.S.A. 107, 11 ( 2010 ).
J.P.R.O. Orgel, T.C. Irving, A. Miller, T.J. Wess, Proc. Natl. Acad. Sci. U.S.A. 103, 9001 ( 2006 ).
J. Tao, K.C. Battle, H. Pan, E.A. Salter, Y.-C. Chien, A. Wierzbicki, J.J. De Yoreo, Proc. Natl. Acad. Sci. U.S.A. 112, 326 ( 2015 ).
J.J. De Yoreo, S. Chung, R.W. Friddle, Adv. Funct. Mater. 23, 2525 ( 2013 ).
S. Weiner, H.D. Wagner, Annu. Rev. Mater. Sci. 28, 271 ( 1998 ).
W.J. Landis, F.H. Silver, Cells Tissues Organs 189, 20 ( 2009 ).
Y. Wang, T. Azaïs, M. Robin, A. Vallée, C. Catania, P. Legriel, G. Pehau-Arnaudet, F. Babonneau, M.-M. Giraud-Guille, N. Nassif, Nat. Mater. 11, 724 ( 2012 ).
M.J. Olszta, X. Cheng, S.S. Jee, R. Kumar, Y.-Y. Kim, M.J. Kaufman, E.P. Douglas, L.B. Gower, Mater. Sci. Eng. Res. 58, 77 ( 2007 ).
F. Nudelman, G. de With, N.A.J.M. Sommerdijk, Soft Matter 7, 17 ( 2011 ).
B.D. Quan, E.D. Sone, Methods Enzymol. 532, 189 ( 2013 ).
E.D. Sone, S. Weiner, L. Addadi, J. Struct. Biol. 158, 428 ( 2007 ).
B.P. Pichon, P.H.H. Bomans, P.M. Frederik, N.A.J.M. Sommerdijk, J. Am. Chem. Soc. 130, 4034 ( 2008 ).
C.C.M.C. Carcouët, M.W.P. van de Put, B. Mezari, P.C.M.M. Magusin, J. Laven, P.H.H. Bomans, H. Friedrich, A.C.C. Esteves, N.A.J.M. Sommerdijk, R.A.T.M. van Benthem, G. de With, Nano Lett. 14, 1433 ( 2014 ).
C. Frandsen, B.A. Legg, L.R. Comolli, H. Zhang, B. Gilbert, E. Johnson, J.F. Banfield, CrystEngComm 16, 1451 ( 2014 ).
P.-A. Fang, J.F. Conway, H.C. Margolis, J.P. Simmer, E. Beniash, Proc. Natl. Acad. Sci. U.S.A. 108, 14097 ( 2011 ).
P.-A. Fang, H.C. Margolis, J.F. Conway, J.P. Simmer, E. Beniash, J. Struct. Biol. 183, 250 ( 2013 ).
F. Nudelman, K. Pieterse, A. George, P.H.H. Bomans, H. Friedrich, L.J. Brylka, P.A.J. Hilbers, G. de With, N.A.J.M. Sommerdijk, Nat. Mater. 9, 1004 ( 2010 ).
E.M. Pouget, P.H.H. Bomans, J.A.C.M. Goos, P.M. Frederik, G. de With, N.A.J.M. Sommerdijk Science 323, 1455 ( 2009 ).
M.J. Williamson, R.M. Tromp, P.M. Vereecken, R. Hull, F.M. Ross, Nat. Mater. 2, 532 ( 2003 ).
C.-M. Wang, H.-G. Liao, F.M. Ross, MRS Bull. 40, 46 ( 2015 ).
H. Zheng, Y.S. Meng, Y. Zhu, MRS Bull. 40, 12 ( 2015 ).
E.A. Sutter, P.W. Sutter, J. Am. Chem. Soc. 136, 16865 ( 2014 ).
D. Li, M.H. Nielsen, J.J. De Yoreo, Methods Enzymol. 532, 147 ( 2013 ).
M.H. Nielsen, D. Li, H. Zhang, S. Aloni, T.Y.-J. Han, C. Frandsen, J. Seto, J.F. Banfield, H. Cölfen, J.J. De Yoreo, Microsc. Microanal. 20, 1 ( 2014 ).
M.H. Nielsen, S. Aloni, J.J. De Yoreo, Science 345, 1158 ( 2014 ).
P.J.M. Smeets, K.R. Cho, R.G.E. Kempen, N.A.J.M. Sommerdijk, J.J. De Yoreo, Nat. Mater. 14, 394 ( 2015 ).
T.J. Woehl, J.E. Evans, I. Arslan, W.D. Ristenpart, N.D. Browning, ACS Nano 6, 8599 ( 2012 ).
H. Zhang, J.J. De Yoreo, J.F. Banfield, ACS Nano 8, 6526 ( 2014 ).
L. Addadi, J. Moradian, E. Shay, N.G. Maroudas, S. Weiner, Proc. Natl. Acad. Sci. U.S.A. 84, 2732 ( 1987 ).
M.E. Marsh, Protoplasma 177, 108 ( 1994 ).
A.S. Schenk, I. Zlotnikov, B. Pokroy, N. Gierlinger, A. Masic, P. Zaslansky, A.N. Fitch, O. Paris, T.H. Metzger, H. Cölfen, P. Fratzl, B. Aichmayer, Adv. Funct. Mater. 22, 4668 ( 2012 ).
A.A. Sousa, R.D. Leapman, Ultramicroscopy 123, 38 ( 2012 ).
L. Kabalah-Amitai, B. Mayzel, Y. Kauffmann, A.N. Fitch, L. Bloch, P.U.P.A. Gilbert, B. Pokroy, Science 340, 454 ( 2013 ).
A. Osuna-Mascaró, T. Cruz-Bustos, S. Benhamada, N. Guichard, B. Marie, L. Plasseraud, M. Corneillat, G. Alcaraz, A. Checa, F. Marin, Comp. Biochem. Physiol. B Biochem. Mol. Biol. 168, 76 ( 2014 ).
T. Mass, J.L. Drake, E.C. Peters, W. Jiang, P.G. Falkowski, Proc. Natl. Acad. Sci. U.S.A. 111, 12728 ( 2014 ).
L. Ameye, R. Hermann, C. Killian, F. Wilt, P. Dubois, J. Histochem. Cytochem. 47, 1189 ( 1999 ).
J. Seto, Y. Zhang, P. Hamilton, F. Wilt, J. Struct. Biol. 148, 123 ( 2004 ).
P.A. Midgley, M. Weyland, Ultramicroscopy 96, 413 ( 2003 ).
R. Leary, P. Midgley, J. Thomas, Acc. Chem. Res. 45 ( 2012 ).
P.M. Voyles, J.L. Grazul, D.A. Muller, Ultramicroscopy 96, 251 ( 2003 ).
M.E. Kunitake, L.M. Mangano, J.M. Peloquin, S.P. Baker, L.A. Estroff, Acta Biomater. 9, 5353 ( 2013 ).
H. Li, H.L. Xin, M.E. Kunitake, E.C. Keene, D.A. Muller, L.A. Estroff, Adv. Funct. Mater. 21, 2028 ( 2011 ).
K. Gries, R. Kröger, C. Kübel, M. Fritz, A. Rosenauer, A cta Biomater. 5, 3038 ( 2009 ).
T. Okumura, M. Suzuki, H. Nagasawa, T. Kogure, J. Cryst. Growth 381, 114 ( 2013 ).
R. van de Locht, T.J.A. Slater, A. Verch, J.R. Young, S.J. Haigh, R. Kröger, Cryst. Growth Des. 14, 1710 ( 2014 ).
H. Li, H.L. Xin, D.A. Muller, L.A. Estroff, Science 326, 1244 ( 2009 ).
Y.-Y. Kim, K. Ganesan, P. Yang, A.N. Kulak, S. Borukhin, S. Pechook, L. Ribeiro, R. Kröger, S.J. Eichhorn, S.P. Armes, B. Pokroy, F.C. Meldrum, Nat. Mater. 10, 890 ( 2011 ).
D.N. Seidman, Annu. Rev. Mater. Res. 37, 127 ( 2007 ).
M.K. Miller, R.G. Forbes, Mater. Charact. 60, 461 ( 2009 ).
T.F. Kelly, O. Nishikawa, J.A. Panitz, T.J. Prosa, MRS Bull. 34, 744 ( 2009 ).
E.A. Marquis, M. Bachhav, Y. Chen, Y. Dong, L.M. Gordon, A. McFarland, Curr. Opin. Solid State Mater. Sci. 17, 217 ( 2013 ).
L.M. Gordon, D. Joester, Nature 469, 194 ( 2011 ).
L. Gordon, L. Tran, D. Joester, ACS Nano 6, 10667 ( 2012 ).
L.M. Gordon, M.J. Cohen, K.W. MacRenaris, J.D. Pasteris, T. Seda, D. Joester, Science 347, 746 ( 2015 ).
N. Tamura, P.U.P.A. Gilbert, Methods Enzymol. 532, 501 ( 2013 ).
C. Gilow, E. Zolotoyabko, O. Paris, P. Fratzl, B. Aichmayer, Cryst. Growth Des. 11, 2054 ( 2011 ).
E. Beniash, R.A. Metzler, R.S.K. Lam, P.U.P.A. Gilbert, J. Struct. Biol. 166, 133 ( 2009 ).
S. Weiner, J. Mahamid, Y. Politi, Y. Ma, L. Addadi, Front. Mater. Sci. China. 3, 104 ( 2009 ).
Y. Levi-Kalisman, S. Raz, S. Weiner, L. Addadi, I. Sagi, J. Chem. Soc. Dalton Trans. 21, 3977 ( 2000 ).
J. Mahamid, B. Aichmayer, E. Shimoni, R. Ziblat, C. Li, S. Siegel, O. Paris, P. Fratzl, S. Weiner, L. Addadi, Proc. Natl. Acad. Sci. U.S.A. 107, 6316 ( 2010 ).
P.U.P.A. Gilbert, J. Electron Spectrosc. Relat. Phenom. 185, 395 ( 2012 ).
Y. Ma, B. Aichmayer, O. Paris, P. Fratzl, A. Meibom, R.A. Metzler, Y. Politi, L. Addadi, P.U.P.A. Gilbert, S. Weiner, Proc. Natl. Acad. Sci. U.S.A. 106, 6048 ( 2009 ).
S. Weiner, L. Addadi, Annu. Rev. Mater. Res. 41, 21 ( 2011 ).
Y.U.T. Gong, C.E. Killian, I.C. Olson, N.P. Appathurai, A.L. Amasino, M.C. Martin, L.J. Holt, F.H. Wilt, P.U.P.A. Gilbert, Proc. Natl. Acad. Sci. U.S.A. 109, 6088 ( 2012).
R.A. Metzler, G.A. Tribello, M. Parrinello, P.U.P.A. Gilbert, J. Am. Chem. Soc. 132, 11585 ( 2010 ).
R.A. Metzler, J.S. Evans, C.E. Killian, D. Zhou, T.H. Churchill, N.P. Appathurai, S.N. Coppersmith, P.U.P.A. Gilbert, J. Am. Chem. Soc. 132, 6329 ( 2010 ).
R.S.K. Lam, R.A. Metzler, P.U.P.A. Gilbert, E. Beniash, ACS Chem. Biol. 7, 476 ( 2012).
S. Gamsjaeger, R. Mendelsohn, A.L. Boskey, S. Gourion-Arsiquaud, K. Klaushofer, E.P. Paschalis, Curr. Osteoporos. Rep. 12, 454 ( 2014 ).
A.C.S. Talari, Z. Movasaghi, S. Rehman, I.U.R. Rehman, Appl. Spectrosc. Rev. 50, 46 ( 2014 ).
J.C. Weaver, G.W. Milliron, A. Miserez, K. Evans-Lutterodt, S. Herrera, I. Gallana, W.J. Mershon, B. Swanson, P. Zavattieri, E. DiMasi, D. Kisailus, Science 336, 1275 ( 2012).
S. Amini, A. Masic, L. Bertinetti, J.S. Teguh, J.S. Herrin, X. Zhu, H. Su, A. Miserez, Nat. Commun. 5, 3187 ( 2014 ).
K. Lee, W. Wagermaier, A. Masic, K.P. Kommareddy, M. Bennet, I. Manjubala, S.-W. Lee, S.B. Park, H. Cölfen, P. Fratzl, Nat. Commun. 3, 725 ( 2012 ).
S.H.K. Eder, A.M. Gigler, M. Hanzlik, M. Winklhofer, PLoS One 9, e107356 ( 2014 ).
S. Omelon, J. Georgiou, F. Variola, M.N. Dean, Acta Biomater. 10, 3899 ( 2014 ).
A.A. Lloyd, Z.X. Wang, E. Donnelly, J. Biomech. Eng. 137, 010801 ( 2015 ).
A. Masic, L. Bertinetti, R. Schuetz, L. Galvis, N. Timofeeva, J.W.C. Dunlop, J. Seto, M.A. Hartmann, P. Fratzl, Biomacromolecules 12, 3989 ( 2011 ).
M. Bennet, A. Akiva, D. Faivre, G. Malkinson, K. Yaniv, S. Abdelilah-Seyfried, P. Fratzl, A. Masic, Biophys. J. 106, L17 ( 2014 ).
A. Akiva, G. Malkinson, A. Masic, M. Kerschnitzki, M. Bennet, P. Fratzl, L. Addadi, S. Weiner, K. Yaniv, Bone 75, 192 ( 2015 ).
T. Ando, N. Kodera, Y. Naito, T. Kinoshita, K. Furuta, Y.Y. Toyoshima, ChemPhysChem 4, 1196 ( 2003 ).
M. Shibata, H. Yamashita, T. Uchihashi, H. Kandori, T. Ando, Nat. Nanotechnol. 5, 208 ( 2010 ).
N. Kodera, D. Yamamoto, R. Ishikawa, T. Ando, Nature 468, 72 ( 2010 ).
T. Fukuma, S.P. Jarvis, Rev. Sci. Instrum. 77, 043701 ( 2006 ).
J.I. Kilpatrick, S.-H. Loh, S.P. Jarvis, J. Am. Chem. Soc. 135, 2628 ( 2013 ).
T. Fukuma, M.J. Higgins, S.P. Jarvis, Biophys. J. 92, 3603 ( 2007 ).
M. Obst, G. Schmid, in Electron Microscopy: Methods and Protocols, Methods in Molecular Biology, J. Kuo, Ed. ( Springer, New York, 2014 ), vol. 1117.
J. Cosmidis, K. Benzerara, N. Nassif, T. Tyliszczak, F. Bourdelle, Acta Biomater. 12, 260 ( 2015 ).
Y. Li, F. El Gabaly, T.R. Ferguson, R.B. Smith, N.C. Bartelt, J.D. Sugar, K.R. Fenton, D.A. Cogswell, A.L.D. Kilcoyne, T. Tyliszczak, M.Z. Bazant, W.C. Chueh, Nat. Mater. 13, 1149 ( 2014 ).
N. Vidavsky, S. Addadi, J. Mahamid, E. Shimoni, D. Ben-Ezra, M. Shpigel, S. Weiner, L. Addadi, Proc. Natl. Acad. Sci. U.S.A. 111, 39 ( 2014 ).
I. Solomonov, D. Talmi-Frank, Y. Milstein, S. Addadi, A. Aloshin, I. Sagi, Sci. Rep. 4, 5987 ( 2014 ).
A. Rigort, F.J.B. Bäuerlein, E. Villa, M. Eibauer, T. Laugks, W. Baumeister, J.M. Plitzko, Proc. Natl. Acad. Sci. U.S.A. 109, 4449 ( 2012 ).
Acknowledgements
The authors acknowledge support from the National Science Foundation (DMR 1210304) and the National Institutes of Health (CA173083). J.J.D.Y. and J.T. acknowledge support from the US Department of Energy, Office of Basic Energy Sciences, Division of Materials Science and Engineering J.J.D.Y also acknowledges support from the Laboratory Directed Research and Development Initiative on Materials Synthesis and Simulation across Scales at the Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for the US Department of Energy under Contract DE-AC05–76RL01830.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hendley, C.T., Tao, J., Kunitake, J.A.M.R. et al. Microscopy techniques for investigating the control of organic constituents on biomineralization. MRS Bulletin 40, 480–489 (2015). https://doi.org/10.1557/mrs.2015.98
Published:
Issue Date:
DOI: https://doi.org/10.1557/mrs.2015.98