Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T02:40:54.248Z Has data issue: false hasContentIssue false

Microscopy techniques for investigating the control of organic constituents on biomineralization

Published online by Cambridge University Press:  03 June 2015

Coit T. Hendley IV
Affiliation:
Department of Materials Science and Engineering, Cornell University, USA; [email protected]
Jinhui Tao
Affiliation:
Physical Sciences Division, Pacific Northwest National Laboratory, USA; [email protected]
Jennie A.M.R. Kunitake
Affiliation:
Department of Materials Science and Engineering, Cornell University, USA; [email protected]
James J. De Yoreo
Affiliation:
Physical Sciences Division, Pacific Northwest National Laboratory; and Department of Materials Science and Engineering and Department of Chemistry, University of Washington, USA; [email protected]
Lara A. Estroff
Affiliation:
Department of Materials Science and Engineering, Cornell University, USA; [email protected]
Get access

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.

Type
Research Article
Copyright
Copyright © Materials Research Society 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Lowenstam, H., Weiner, S., On Biomineralization (Oxford University Press, New york, 1989).CrossRefGoogle Scholar
Dove, P.M., De Yoreo, J.J., Weiner, S., Eds., Biomineralization (Mineral Society of America, Washington, DC, 2003).CrossRefGoogle Scholar
Asenath-Smith, E., Li, H., Keene, E.C., Seh, Z.W., Estroff, L.A., Adv. Funct. Mater. 22, 2891 (2012).CrossRefGoogle Scholar
Nudelman, F., Sommerdijk, N.A.J.M., Angew. Chem. Int. Ed. 51, 6582 (2012).CrossRefGoogle Scholar
Arakaki, A., Shimizu, K., Oda, M., Sakamoto, T., Nishimura, T., Kato, T., Org. Biomol. Chem. 13, 974 (2014).CrossRefGoogle Scholar
Franz, C.M., Muller, D.J., Methods Mol. Biol. 736, 97 (2011).CrossRefGoogle Scholar
De Yoreo, J.J., AIP Conf. Proc. 916, 416 (2007).CrossRefGoogle Scholar
Rashkovich, L.N., De Yoreo, J.J., Orme, C.A., Chernov, A.A., Crystallogr. Rep. 51, 1063 (2006).CrossRefGoogle Scholar
Cisneros, D.A., Hung, C., Franz, C.M., Muller, D.J., J. Struct. Biol. 154, 232 (2006).CrossRefGoogle Scholar
Chung, S., Shin, S.-H., Bertozzi, C.R., De Yoreo, J.J., Proc. Natl. Acad. Sci. U.S.A. 107, 16536 (2010).CrossRefGoogle Scholar
Narayanan, B., Gilmer, G.H., Tao, J., De Yoreo, J.J., Ciobanu, C.V., Langmuir 30, 1343 (2014).CrossRefGoogle Scholar
Habraken, W.J.E.M., Tao, J., Brylka, L.J., Friedrich, H., Bertinetti, L., Schenk, A.S., Verch, A., Dmitrovic, V., Bomans, P.H.H., Frederik, P.M., Laven, J., van der Schoot, P., Aichmayer, B., de With, G., De Yoreo, J.J., Sommerdijk, N.A.J.M., Nat. Commun. 4, 1507 (2013).CrossRefGoogle Scholar
Hamm, L.M., Giuffre, A.J., Han, N., Tao, J., Wang, D., De Yoreo, J.J., Dove, P.M., Proc. Natl. Acad. Sci. U.S.A. 111, 1304 (2014).CrossRefGoogle Scholar
Rimer, J.D., An, Z., Zhu, Z., Lee, M.H., Goldfarb, D.S., Wesson, J.A., Ward, M.D., Science 330, 337 (2010).CrossRefGoogle Scholar
Orme, C.A., Noy, A., Wierzbicki, A., McBride, M.T., Grantham, M., Teng, H.H., Dove, P.M., De Yoreo, J.J., Nature 411, 775 (2001).CrossRefGoogle Scholar
Olafson, K.N., Ketchum, M.A., Rimer, J.D., Vekilov, P.G., Proc. Natl. Acad. Sci. U.S.A. 112, 4969 (2015).Google Scholar
De Yoreo, J.J., Zepeda-Ruiz, L.A., Friddle, R.W., Qiu, S.R., Wasylenki, L.E., Chernov, A.A., Gilmer, G.H., Dove, P.M., Cryst. Growth Des. 9, 5135 (2009).CrossRefGoogle Scholar
Friddle, R.W., Weaver, M.L., Qiu, S.R., Wierzbicki, A., Casey, W.H., De Yoreo, J.J., Proc. Natl. Acad. Sci. U.S.A. 107, 11 (2010).CrossRefGoogle Scholar
Orgel, J.P.R.O., Irving, T.C., Miller, A., Wess, T.J., Proc. Natl. Acad. Sci. U.S.A. 103, 9001 (2006).CrossRefGoogle Scholar
Tao, J., Battle, K.C., Pan, H., Salter, E.A., Chien, Y.-C., Wierzbicki, A., De Yoreo, J.J., Proc. Natl. Acad. Sci. U.S.A. 112, 326 (2015).CrossRefGoogle Scholar
De Yoreo, J.J., Chung, S., Friddle, R.W., Adv. Funct. Mater. 23, 2525 (2013).CrossRefGoogle Scholar
Weiner, S., Wagner, H.D., Annu. Rev. Mater. Sci. 28, 271 (1998).CrossRefGoogle Scholar
Landis, W.J., Silver, F.H., Cells Tissues Organs 189, 20 (2009).CrossRefGoogle Scholar
Wang, Y., Azaïs, T., Robin, M., Vallée, A., Catania, C., Legriel, P., Pehau-Arnaudet, G., Babonneau, F., Giraud-Guille, M.-M., Nassif, N., Nat. Mater. 11, 724 (2012).CrossRefGoogle Scholar
Olszta, M.J., Cheng, X., Jee, S.S., Kumar, R., Kim, Y.-Y., Kaufman, M.J., Douglas, E.P., Gower, L.B., Mater. Sci. Eng. Res. 58, 77 (2007).CrossRefGoogle Scholar
Nudelman, F., de With, G., Sommerdijk, N.A.J.M., Soft Matter 7, 17 (2011).CrossRefGoogle Scholar
Quan, B.D., Sone, E.D., Methods Enzymol. 532, 189 (2013).CrossRefGoogle Scholar
Sone, E.D., Weiner, S., Addadi, L., J. Struct. Biol. 158, 428 (2007).CrossRefGoogle Scholar
Pichon, B.P., Bomans, P.H.H., Frederik, P.M., Sommerdijk, N.A.J.M., J. Am. Chem. Soc. 130, 4034 (2008).CrossRefGoogle Scholar
Carcouët, C.C.M.C., van de Put, M.W.P., Mezari, B., Magusin, P.C.M.M., Laven, J., Bomans, P.H.H., Friedrich, H., Esteves, A.C.C., Sommerdijk, N.A.J.M., van Benthem, R.A.T.M., de With, G., Nano Lett. 14, 1433 (2014).CrossRefGoogle Scholar
Frandsen, C., Legg, B.A., Comolli, L.R., Zhang, H., Gilbert, B., Johnson, E., Banfield, J.F., CrystEngComm 16, 1451 (2014).CrossRefGoogle Scholar
Fang, P.-A., Conway, J.F., Margolis, H.C., Simmer, J.P., Beniash, E., Proc. Natl. Acad. Sci. U.S.A. 108, 14097 (2011).CrossRefGoogle Scholar
Fang, P.-A., Margolis, H.C., Conway, J.F., Simmer, J.P., Beniash, E., J. Struct. Biol. 183, 250 (2013).CrossRefGoogle Scholar
Nudelman, F., Pieterse, K., George, A., Bomans, P.H.H., Friedrich, H., Brylka, L.J., Hilbers, P.A.J., de With, G., Sommerdijk, N.A.J.M., Nat. Mater. 9, 1004 (2010).CrossRefGoogle Scholar
Pouget, E.M., Bomans, P.H.H., Goos, J.A.C.M., Frederik, P.M., de With, G., Sommerdijk, N.A.J.M. Science 323, 1455 (2009).CrossRefGoogle Scholar
Williamson, M.J., Tromp, R.M., Vereecken, P.M., Hull, R., Ross, F.M., Nat. Mater. 2, 532 (2003).CrossRefGoogle Scholar
Wang, C.-M., Liao, H.-G., Ross, F.M., MRS Bull. 40, 46 (2015).CrossRefGoogle Scholar
Zheng, H., Meng, Y.S., Zhu, Y., MRS Bull. 40, 12 (2015).CrossRefGoogle Scholar
Sutter, E.A., Sutter, P.W., J. Am. Chem. Soc. 136, 16865 (2014).CrossRefGoogle Scholar
Li, D., Nielsen, M.H., De Yoreo, J.J., Methods Enzymol. 532, 147 (2013).CrossRefGoogle Scholar
Nielsen, M.H., Li, D., Zhang, H., Aloni, S., Han, T.Y.-J., Frandsen, C., Seto, J., Banfield, J.F., Cölfen, H., De Yoreo, J.J., Microsc. Microanal. 20, 1 (2014).CrossRefGoogle Scholar
Nielsen, M.H., Aloni, S., De Yoreo, J.J., Science 345, 1158 (2014).CrossRefGoogle Scholar
Smeets, P.J.M., Cho, K.R., Kempen, R.G.E., Sommerdijk, N.A.J.M., De Yoreo, J.J., Nat. Mater. 14, 394 (2015).CrossRefGoogle Scholar
Woehl, T.J., Evans, J.E., Arslan, I., Ristenpart, W.D., Browning, N.D., ACS Nano 6, 8599 (2012).CrossRefGoogle Scholar
Zhang, H., De Yoreo, J.J., Banfield, J.F., ACS Nano 8, 6526 (2014).CrossRefGoogle Scholar
Addadi, L., Moradian, J., Shay, E., Maroudas, N.G., Weiner, S., Proc. Natl. Acad. Sci. U.S.A. 84, 2732 (1987).CrossRefGoogle Scholar
Marsh, M.E., Protoplasma 177, 108 (1994).CrossRefGoogle Scholar
Schenk, A.S., Zlotnikov, I., Pokroy, B., Gierlinger, N., Masic, A., Zaslansky, P., Fitch, A.N., Paris, O., Metzger, T.H., Cölfen, H., Fratzl, P., Aichmayer, B., Adv. Funct. Mater. 22, 4668 (2012).CrossRefGoogle Scholar
Sousa, A.A., Leapman, R.D., Ultramicroscopy 123, 38 (2012).CrossRefGoogle Scholar
Kabalah-Amitai, L., Mayzel, B., Kauffmann, Y., Fitch, A.N., Bloch, L., Gilbert, P.U.P.A., Pokroy, B., Science 340, 454 (2013).CrossRefGoogle Scholar
Osuna-Mascaró, A., Cruz-Bustos, T., Benhamada, S., Guichard, N., Marie, B., Plasseraud, L., Corneillat, M., Alcaraz, G., Checa, A., Marin, F., Comp. Biochem. Physiol. B Biochem. Mol. Biol. 168, 76 (2014).CrossRefGoogle Scholar
Mass, T., Drake, J.L., Peters, E.C., Jiang, W., Falkowski, P.G., Proc. Natl. Acad. Sci. U.S.A. 111, 12728 (2014).CrossRefGoogle Scholar
Ameye, L., Hermann, R., Killian, C., Wilt, F., Dubois, P., J. Histochem. Cytochem. 47, 1189 (1999).CrossRefGoogle Scholar
Seto, J., Zhang, Y., Hamilton, P., Wilt, F., J. Struct. Biol. 148, 123 (2004).CrossRefGoogle Scholar
Midgley, P.A., Weyland, M., Ultramicroscopy 96, 413 (2003).CrossRefGoogle Scholar
Leary, R., Midgley, P., Thomas, J., Acc. Chem. Res. 45 (2012).CrossRefGoogle Scholar
Voyles, P.M., Grazul, J.L., Muller, D.A., Ultramicroscopy 96, 251 (2003).CrossRefGoogle Scholar
Kunitake, M.E., Mangano, L.M., Peloquin, J.M., Baker, S.P., Estroff, L.A., Acta Biomater. 9, 5353 (2013).CrossRefGoogle Scholar
Li, H., Xin, H.L., Kunitake, M.E., Keene, E.C., Muller, D.A., Estroff, L.A., Adv. Funct. Mater. 21, 2028 (2011).CrossRefGoogle Scholar
Gries, K., Kröger, R., Kübel, C., Fritz, M., Rosenauer, A., Acta Biomater. 5, 3038 (2009).CrossRefGoogle Scholar
Okumura, T., Suzuki, M., Nagasawa, H., Kogure, T., J. Cryst. Growth 381, 114 (2013).CrossRefGoogle Scholar
van de Locht, R., Slater, T.J.A., Verch, A., Young, J.R., Haigh, S.J., Kröger, R., Cryst. Growth Des. 14, 1710 (2014).CrossRefGoogle Scholar
Li, H., Xin, H.L., Muller, D.A., Estroff, L.A., Science 326, 1244 (2009).CrossRefGoogle Scholar
Kim, Y.-Y., Ganesan, K., Yang, P., Kulak, A.N., Borukhin, S., Pechook, S., Ribeiro, L., Kröger, R., Eichhorn, S.J., Armes, S.P., Pokroy, B., Meldrum, F.C., Nat. Mater. 10, 890 (2011).CrossRefGoogle Scholar
Seidman, D.N., Annu. Rev. Mater. Res. 37, 127 (2007).CrossRefGoogle Scholar
Miller, M.K., Forbes, R.G., Mater. Charact. 60, 461 (2009).CrossRefGoogle Scholar
Kelly, T.F., Nishikawa, O., Panitz, J.A., Prosa, T.J., MRS Bull. 34, 744 (2009).CrossRefGoogle Scholar
Marquis, E.A., Bachhav, M., Chen, Y., Dong, Y., Gordon, L.M., McFarland, A., Curr. Opin. Solid State Mater. Sci. 17, 217 (2013).CrossRefGoogle Scholar
Gordon, L.M., Joester, D., Nature 469, 194 (2011).CrossRefGoogle Scholar
Gordon, L., Tran, L., Joester, D., ACS Nano 6, 10667 (2012).CrossRefGoogle Scholar
Gordon, L.M., Cohen, M.J., MacRenaris, K.W., Pasteris, J.D., Seda, T., Joester, D., Science 347, 746 (2015).CrossRefGoogle Scholar
Tamura, N., Gilbert, P.U.P.A., Methods Enzymol. 532, 501 (2013).CrossRefGoogle Scholar
Gilow, C., Zolotoyabko, E., Paris, O., Fratzl, P., Aichmayer, B., Cryst. Growth Des. 11, 2054 (2011).CrossRefGoogle Scholar
Beniash, E., Metzler, R.A., Lam, R.S.K., Gilbert, P.U.P.A., J. Struct. Biol. 166, 133 (2009).CrossRefGoogle Scholar
Weiner, S., Mahamid, J., Politi, Y., Ma, Y., Addadi, L., Front. Mater. Sci. China. 3, 104 (2009).CrossRefGoogle Scholar
Levi-Kalisman, Y., Raz, S., Weiner, S., Addadi, L., Sagi, I., J. Chem. Soc. Dalton Trans. 21, 3977 (2000).CrossRefGoogle Scholar
Mahamid, J., Aichmayer, B., Shimoni, E., Ziblat, R., Li, C., Siegel, S., Paris, O., Fratzl, P., Weiner, S., Addadi, L., Proc. Natl. Acad. Sci. U.S.A. 107, 6316 (2010).CrossRefGoogle Scholar
Gilbert, P.U.P.A., J. Electron Spectrosc. Relat. Phenom. 185, 395 (2012).CrossRefGoogle Scholar
Ma, Y., Aichmayer, B., Paris, O., Fratzl, P., Meibom, A., Metzler, R.A., Politi, Y., Addadi, L., Gilbert, P.U.P.A., Weiner, S., Proc. Natl. Acad. Sci. U.S.A. 106, 6048 (2009).CrossRefGoogle Scholar
Weiner, S., Addadi, L., Annu. Rev. Mater. Res. 41, 21 (2011).CrossRefGoogle Scholar
Gong, Y.U.T., Killian, C.E., Olson, I.C., Appathurai, N.P., Amasino, A.L., Martin, M.C., Holt, L.J., Wilt, F.H., Gilbert, P.U.P.A., Proc. Natl. Acad. Sci. U.S.A. 109, 6088 (2012).CrossRefGoogle Scholar
Metzler, R.A., Tribello, G.A., Parrinello, M., Gilbert, P.U.P.A., J. Am. Chem. Soc. 132, 11585 (2010).CrossRefGoogle Scholar
Metzler, R.A., Evans, J.S., Killian, C.E., Zhou, D., Churchill, T.H., Appathurai, N.P., Coppersmith, S.N., Gilbert, P.U.P.A., J. Am. Chem. Soc. 132, 6329 (2010).CrossRefGoogle Scholar
Lam, R.S.K., Metzler, R.A., Gilbert, P.U.P.A., Beniash, E., ACS Chem. Biol. 7, 476 (2012).CrossRefGoogle Scholar
Gamsjaeger, S., Mendelsohn, R., Boskey, A.L., Gourion-Arsiquaud, S., Klaushofer, K., Paschalis, E.P., Curr. Osteoporos. Rep. 12, 454 (2014).CrossRefGoogle Scholar
Talari, A.C.S., Movasaghi, Z., Rehman, S., Rehman, I.U.R., Appl. Spectrosc. Rev. 50, 46 (2014).CrossRefGoogle Scholar
Weaver, J.C., Milliron, G.W., Miserez, A., Evans-Lutterodt, K., Herrera, S., Gallana, I., Mershon, W.J., Swanson, B., Zavattieri, P., DiMasi, E., Kisailus, D., Science 336, 1275 (2012).CrossRefGoogle Scholar
Amini, S., Masic, A., Bertinetti, L., Teguh, J.S., Herrin, J.S., Zhu, X., Su, H., Miserez, A., Nat. Commun. 5, 3187 (2014).CrossRefGoogle Scholar
Lee, K., Wagermaier, W., Masic, A., Kommareddy, K.P., Bennet, M., Manjubala, I., Lee, S.-W., Park, S.B., Cölfen, H., Fratzl, P., Nat. Commun. 3, 725 (2012).CrossRefGoogle Scholar
Eder, S.H.K., Gigler, A.M., Hanzlik, M., Winklhofer, M., PLoS One 9, e107356 (2014).CrossRefGoogle Scholar
Omelon, S., Georgiou, J., Variola, F., Dean, M.N., Acta Biomater. 10, 3899 (2014).CrossRefGoogle Scholar
Lloyd, A.A., Wang, Z.X., Donnelly, E., J. Biomech. Eng. 137, 010801 (2015).CrossRefGoogle Scholar
Masic, A., Bertinetti, L., Schuetz, R., Galvis, L., Timofeeva, N., Dunlop, J.W.C., Seto, J., Hartmann, M.A., Fratzl, P., Biomacromolecules 12, 3989 (2011).CrossRefGoogle Scholar
Bennet, M., Akiva, A., Faivre, D., Malkinson, G., Yaniv, K., Abdelilah-Seyfried, S., Fratzl, P., Masic, A., Biophys. J. 106, L17 (2014).CrossRefGoogle Scholar
Akiva, A., Malkinson, G., Masic, A., Kerschnitzki, M., Bennet, M., Fratzl, P., Addadi, L., Weiner, S., Yaniv, K., Bone 75, 192 (2015).CrossRefGoogle ScholarPubMed
Ando, T., Kodera, N., Naito, Y., Kinoshita, T., Furuta, K., Toyoshima, Y.Y., ChemPhysChem 4, 1196 (2003).CrossRefGoogle Scholar
Shibata, M., Yamashita, H., Uchihashi, T., Kandori, H., Ando, T., Nat. Nanotechnol. 5, 208 (2010).CrossRefGoogle Scholar
Kodera, N., Yamamoto, D., Ishikawa, R., Ando, T., Nature 468, 72 (2010).CrossRefGoogle Scholar
Fukuma, T., Jarvis, S.P., Rev. Sci. Instrum. 77, 043701 (2006).Google Scholar
Kilpatrick, J.I., Loh, S.-H., Jarvis, S.P., J. Am. Chem. Soc. 135, 2628 (2013).CrossRefGoogle Scholar
Fukuma, T., Higgins, M.J., Jarvis, S.P., Biophys. J. 92, 3603 (2007).CrossRefGoogle Scholar
Obst, M., Schmid, G., in Electron Microscopy: Methods and Protocols, Methods in Molecular Biology, Kuo, J., Ed. (Springer, New York, 2014), vol. 1117.Google Scholar
Cosmidis, J., Benzerara, K., Nassif, N., Tyliszczak, T., Bourdelle, F., Acta Biomater. 12, 260 (2015).CrossRefGoogle Scholar
Li, Y., El Gabaly, F., Ferguson, T.R., Smith, R.B., Bartelt, N.C., Sugar, J.D., Fenton, K.R., Cogswell, D.A., Kilcoyne, A.L.D., Tyliszczak, T., Bazant, M.Z., Chueh, W.C., Nat. Mater. 13, 1149 (2014).CrossRefGoogle Scholar
Vidavsky, N., Addadi, S., Mahamid, J., Shimoni, E., Ben-Ezra, D., Shpigel, M., Weiner, S., Addadi, L., Proc. Natl. Acad. Sci. U.S.A. 111, 39 (2014).CrossRefGoogle Scholar
Solomonov, I., Talmi-Frank, D., Milstein, Y., Addadi, S., Aloshin, A., Sagi, I., Sci. Rep. 4, 5987 (2014).CrossRefGoogle Scholar
Rigort, A., Bäuerlein, F.J.B., Villa, E., Eibauer, M., Laugks, T., Baumeister, W., Plitzko, J.M., Proc. Natl. Acad. Sci. U.S.A. 109, 4449 (2012).CrossRefGoogle Scholar