Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T15:53:00.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Correlative multiscale tomography of biological materials

Published online by Cambridge University Press:  07 July 2016

Robert S. Bradley  and
Philip J. Withers
Robert S. Bradley
Affiliation:
The University of Manchester, UK; [email protected]
Philip J. Withers
Affiliation:
School of Materials, The University of Manchester, UK; [email protected]
Get access

Abstract

The intricate hierarchical microstructures typical of biological materials give rise to fascinating combinations of anisotropic mechanical properties that can surpass those of man-made materials. The linking together of three-dimensional (3D) imaging techniques has the potential to reveal these structures in unprecedented detail. However, a complete understanding can only be reached if the relationship between structure and mechanical properties can be elucidated. X-ray-computed tomography (CT) is uniquely placed to image such structures across a wide range of length scales. We review recent technical advances that are leading to improved contrast and spatial resolution. We highlight how time-lapse CT 3D studies can track the response of hierarchical microstructures to mechanical loading.

Keywords

x-ray tomographybiologicalmicrostructurescanning electron microscopy (SEM)fracture
Type
Research Article
Information
MRS Bulletin , Volume 41 , Issue 7: Advanced Tomography Techniques for Materials Applications , July 2016 , pp. 549 - 556
Copyright
Copyright © Materials Research Society 2016 

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

Fratzl, P., Weinkamer, R., Prog. Mater. Sci. 52, 1263 (2007).CrossRefGoogle Scholar
Barber, A.H., Lu, D., Pugno, N.M., J. R. Soc. Interface 12, 20141326 (2015).CrossRefGoogle Scholar
Meyers, M.A., Chen, P.-Y., Lopez, M.I., Seki, Y., Lin, A.Y.M., J. Mech. Behav. Biomed. Mater. 4, 626 (2011).CrossRefGoogle Scholar
Vincent, J.F.V., Proc. Inst. Mech. Eng. H J. Eng. Med. 223, 919 (2009).CrossRefGoogle Scholar
Chen, Q., Pugno, N.M., J. Mech. Behav. Biomed. Mater. 19, 3 (2013).CrossRefGoogle Scholar
Barthelat, F., Int. Mater. Rev. 60, 413 (2015).CrossRefGoogle Scholar
Burnett, T.L., McDonald, S.A., Gholinia, A., Geurts, R., Janus, M., Slater, T., Haigh, S.J., Ornek, C., Almuaili, F., Engelberg, D.L., Thompson, G.E., Withers, P.J., Sci. Rep. 4, 4711 (2014).CrossRefGoogle Scholar
Ntziachristos, V., Nat. Methods 7, 603 (2010).CrossRefGoogle Scholar
Socha, J.J., Westneat, M.W., Harrison, J.F., Waters, J.S., Lee, W.-K., BMC Biol. 5, 1 (2007).CrossRefGoogle Scholar
Howells, M.R., Beetz, T., Chapman, H.N., Cui, C., Holton, J.M., Jacobsen, C.J., Kirz, J., Lima, E., Marchesini, S., Miao, H., Sayre, D., Shapiro, D.A., Spence, J.C.H., Starodub, D., J. Electron. Spectrosc. Relat. Phenom. 170, 4 (2009).CrossRefGoogle Scholar
Carzaniga, R., Domart, M.-C., Collinson, L.M., Duke, E., Protoplasma 251, 449 (2014).CrossRefGoogle Scholar
Alberto, B., Paola, C., Pekka, S., Phys. Med. Biol. 58, R1 (2013).Google Scholar
Zabler, S., Cloetens, P., Guigay, J.-P., Baruchel, J., Schlenker, M., Rev. Sci. Instrum. 76, 073705 (2005).CrossRefGoogle Scholar
Weitkamp, T., Diaz, A., David, C., Pfeiffer, F., Stampanoni, M., Cloetens, P., Ziegler, E., Opt. Express 13, 6296 (2005).CrossRefGoogle Scholar
Tkachuk, A., Duewer, F., Cui, H., Feser, M., Wang, S., Yun, W., Z. Kristallogr. Cryst. Mater. 222, 650 (2007).CrossRefGoogle Scholar
Hagen, C.K., Maghsoudlou, P., Totonelli, G., Diemoz, P.C., Endrizzi, M., Rigon, L., Menk, R.-H., Arfelli, F., Dreossi, D., Brun, E., Coan, P., Bravin, A., De Coppi, P., Olivo, A., Sci. Rep. 5, 18156 (2015).CrossRefGoogle Scholar
Walton, L.A., Bradley, R.S., Withers, P.J., Newton, V.L., Watson, R.E.B., Austin, C., Sherratt, M.J., Sci. Rep. 5, 10074 (2015).CrossRefGoogle Scholar
Poologasundarampillai, G., Wang, D., Li, S., Nakamura, J., Bradley, R., Lee, P.D., Stevens, M.M., McPhail, D.S., Kasuga, T., Jones, J.R., Acta Biomater. 10, 3733 (2014).CrossRefGoogle Scholar
Pfeiffer, F., Weitkamp, T., Bunk, O., David, C., Nat. Phys. 2, 258 (2006).CrossRefGoogle Scholar
Schulz, G., Weitkamp, T., Zanette, I., Pfeiffer, F., Beckmann, F., David, C., Rutishauser, S., Reznikova, E., Müller, B., J. R. Soc. Interface 7, 1665 (2010).CrossRefGoogle Scholar
Zanette, I., Zhou, T., Burvall, A., Lundström, U., Larsson, D.H., Zdora, M., Thibault, P., Pfeiffer, F., Hertz, H.M., Phys. Rev. Lett. 112, 253903 (2014).CrossRefGoogle Scholar
Wang, H., Kashyap, Y., Sawhney, K., Sci. Rep. 6, 20476 (2016).CrossRefGoogle Scholar
Langer, M., Pacureanu, A., Suhonen, H., Grimal, Q., Cloetens, P., Peyrin, F., PLoS One 7, e35691 (2012).CrossRefGoogle Scholar
Marchesini, S., Chapman, H.N., Hau-Riege, S.P., London, R.A., Szoke, A., He, H., Howells, M.R., Padmore, H., Rosen, R., Spence, J.C.H., Weierstall, U., Opt. Express 11, 2344 (2003).CrossRefGoogle Scholar
Berenguer, F., Bean, R.J., Bozec, L., Vila-Comamala, J., Zhang, F., Kewish, C.M., Bunk, O., Rodenburg, J.M., Robinson, I.K., Biophys. J. 106, 459 (2014).CrossRefGoogle Scholar
Zanette, I., Enders, B., Dierolf, M., Thibault, P., Gradl, R., Diaz, A., Guizar-Sicairos, M., Menzel, A., Pfeiffer, F., Zaslansky, P., Sci. Rep. 5, 9210 (2015).CrossRefGoogle Scholar
Dierolf, M., Menzel, A., Thibault, P., Schneider, P., Kewish, C.M., Wepf, R., Bunk, O., Pfeiffer, F., Nature 467, 436 (2010).CrossRefGoogle Scholar
Giewekemeyer, K., Hackenberg, C., Aquila, A., Wilke, R.N., Groves, M.R., Jordanova, R., Lamzin, V.S., Borchers, G., Saksl, K., Zozulya, A.V., Sprung, M., Mancuso, A.P., Biophys. J. 109, 1986 (2015).CrossRefGoogle Scholar
Shemilt, L., Verbanis, E., Schwenke, J., Estandarte, A.K., Xiong, G., Harder, R., Parmar, N., Yusuf, M., Zhang, F., Robinson, I.K., Biophys. J. 108, 706 (2015).CrossRefGoogle Scholar
Metscher, B.D., BMC Physiol. 9, 1 (2009).CrossRefGoogle Scholar
Das Neves Borges, P., Forte, A.E., Vincent, T.L., Dini, D., Marenzana, M., Osteoarthr. Cartil. 22, 1419 (2014).CrossRefGoogle Scholar
Butters, T.D., Castro, S.J., Lowe, T., Zhang, Y., Lei, M., Withers, P.J., Zhang, H., PLoS One 9, e105552 (2014).CrossRefGoogle Scholar
Aslanidi, O.V., Nikolaidou, T., Jichao, Z., Smaill, B.H., Gilbert, S.H., Holden, A.V., Lowe, T., Withers, P.J., Stephenson, R.S., Jarvis, J.C., Hancox, J.C., Boyett, M.R., Henggui, Z., IEEE Trans. Med. Imaging 32, 8 (2013).CrossRefGoogle ScholarPubMed
Shearer, T., Rawson, S., Castro, S.J., Balint, R., Bradley, R.S., Lowe, T., Vila-Comamala, J., Lee, P.D., Cartmell, S.H., Muscles Ligaments Tendons J. 4, 238 (2014).CrossRefGoogle Scholar
de Silva, J.M., Zanette, I., Noël, P.B., Cardoso, M.B., Kimm, M.A., Pfeiffer, F., Sci. Rep. 5, 14088 (2015).CrossRefGoogle Scholar
Cole, L.E., Ross, R.D., Tilley, J.M.R., Vargo-Gogola, T., Roeder, R.K., Nanomedicine 10, 321 (2015).CrossRefGoogle Scholar
De La Vega, J.C., Häfeli, U.O., Contrast Media Mol. Imaging 10, 81 (2015).CrossRefGoogle Scholar
Popovtzer, R., Agrawal, A., Kotov, N.A., Popovtzer, A., Balter, J., Carey, T.E., Kopelman, R., Nano Lett. 8, 4593 (2008).CrossRefGoogle Scholar
Hagen, C., Werner, S., Carregal-Romero, S., Malhas, A.N., Klupp, B.G., Guttmann, P., Rehbein, S., Henzler, K., Mettenleiter, T.C., Vaux, D.J., Parak, W.J., Schneider, G., Grunewald, K., Ultramicroscopy 146, 46 (2014).CrossRefGoogle Scholar
Withers, P.J., Mater. Today 10, 26 (2007).CrossRefGoogle Scholar
Bertilson, M., von Hofsten, O., Vogt, U., Holmberg, A., Christakou, A.E., Hertz, H.M., Opt. Lett. 36, 2728 (2011).CrossRefGoogle Scholar
Carlson, D.B., Gelb, J., Palshin, V., Evans, J.E., Microsc. Microanal. 19, 22 (2013).CrossRefGoogle Scholar
Uchida, M., Sun, Y., McDermott, G., Knoechel, C., Le Gros, M.A., Parkinson, D., Drubin, D.G., Larabell, C.A., Yeast 28, 227 (2011).CrossRefGoogle ScholarPubMed
Schneider, G., Guttmann, P., Heim, S., Rehbein, S., Mueller, F., Nagashima, K., Heymann, J.B., Muller, W.G., McNally, J.G., Nat. Methods 7, 985 (2010).CrossRefGoogle Scholar
Obst, M., Schmid, G., “3D Chemical Mapping: Application of Scanning Transmission (Soft) X-Ray Microscopy (STXM) in Combination with Angle-Scan Tomography in Bio-, Geo-, and Environmental Sciences,” in Electron Microscopy: Methods and Protocols, Kuo, J., Ed. (Humana Press, Totowa, NJ, 2014) pp. 757–781.CrossRefGoogle Scholar
Cosmidis, J., Benzerara, K., Nassif, N., Tyliszczak, T., Bourdelle, F., Acta Biomater. 12, 260 (2015).CrossRefGoogle Scholar
Hernández Cruz, D., Rousseau, M.-E., West, M.M., Pézolet, M., Hitchcock, A.P., Biomacromolecules 7, 836 (2006).CrossRefGoogle Scholar
Normandeau, J., Van Kessel, C., Nicholson, D., Rahusaar Routledge, B., Fawcett, A., Lim-Cole, L., Condy, C., Sylvain, N., Walker, T., Borondics, F., Can. Young Sci. J. 2014, 35 (2014).Google Scholar
Kyrieleis, A., Titarenko, V., Ibison, M., Connolley, T., Withers, P.J., J. Microsc. 241, 69 (2011).CrossRefGoogle Scholar
Patwardhan, A., Ashton, A., Brandt, R., Butcher, S., Carzaniga, R., Chiu, W., Collinson, L., Doux, P., Duke, E., Ellisman, M.H., Franken, E., Grunewald, K., Heriche, J.-K., Koster, A., Kuhlbrandt, W., Lagerstedt, I., Larabell, C., Lawson, C.L., Saibil, H.R., Sanz-Garcia, E., Subramaniam, S., Verkade, P., Swedlow, J.R., Kleywegt, G.J., Nat. Struct. Mol. Biol. 21, 841 (2014).CrossRefGoogle Scholar
Caplan, J., Niethammer, M., Taylor, R.M., Czymmek, K.J., Curr. Opin. Struct. Biol. 21, 686 (2011).CrossRefGoogle Scholar
Giepmans, B.N.G., Histochem. Cell Biol. 130, 211 (2008).CrossRefGoogle Scholar
Merkle, A., Lechner, L., Steinbach, A., Gelb, J., Kienle, M., Phaneuf, M., Unrau, D., Singh, S., Chawla, N., Microsc. Anal. 28, S10 (2014).Google Scholar
Handschuh, S., Baeumler, N., Schwaha, T., Ruthensteiner, B., Front. Zool. 10, 1 (2013).CrossRefGoogle Scholar
Schneider, G., Guttmann, P., Rehbein, S., Werner, S., Follath, R., J. Struct. Biol. 177, 212 (2012).CrossRefGoogle Scholar
Smith, E.A., McDermott, G., Do, M., Leung, K., Panning, B., Le Gros, M., Larabell, C.A., Biophys. J. 107, 1988 (2014).CrossRefGoogle Scholar
Liebi, M., Georgiadis, M., Menzel, A., Schneider, P., Kohlbrecher, J., Bunk, O., Guizar-Sicairos, M., Nature 527, 349 (2015).CrossRefGoogle Scholar
Withers, P.J., Preuss, M., Annu. Rev. Mater. Res. 42, 81 (2012).CrossRefGoogle Scholar
Maire, E., Withers, P.J., Int. Mater. Rev. 59, 1 (2014).CrossRefGoogle Scholar
Barth, H.D., Zimmermann, E.A., Schaible, E., Tang, S.Y., Alliston, T., Ritchie, R.O., Biomaterials 32, 8892 (2011).CrossRefGoogle Scholar
Lowe, T., Garwood, R.J., Simonsen, T.J., Bradley, R.S., Withers, P.J., J. R. Soc. Interface 10, 20130304 (2013).CrossRefGoogle Scholar
Walker, S.M., Schwyn, D.A., Mokso, R., Wicklein, M., Müller, T., Doube, M., Stampanoni, M., Krapp, H.G., Taylor, G.K., PLoS Biol. 12, e1001823 (2014).CrossRefGoogle Scholar
Jang, A.T., Lin, J.D., Seo, Y., Etchin, S., Merkle, A., Fahey, K., Ho, S.P., J. Vis. Exp. 85, e51147 (2014).Google Scholar
Wiest, W., Zabler, S., Rack, A., Fella, C., Balles, A., Nelson, K., Schmelzeisen, R., Hanke, R., J. Synchrotron Radiat. 22, 1492 (2015).CrossRefGoogle Scholar
Patterson, B., Cordes, N.L., Henderson, K., Mertens, J.C.E., Clarke, A.J., Lu, X., Hartwell, R., Hornberger, B., Merkle, A., Etchin, S., Tkachuk, A., Leibowitz, M., Trapp, D., Qiu, W., Zhang, B., Bale, H., Withers, P.J., Bradley, R.S., Exp. Mech. (forthcoming).Google Scholar
Wegst, U.G.K., Bai, H., Saiz, E., Tomsia, A.P., Ritchie, R.O., Nat. Mater. 14, 23 (2015).CrossRefGoogle Scholar
Ilnicka, A., Lukaszewicz, J.P., Front. Mater. 2, 20 (2015), doi:10.3389/fmats.2015.00020.CrossRefGoogle Scholar
Heinzer, S., Krucker, T., Stampanoni, M., Abela, R., Meyer, E.P., Schuler, A., Schneider, P., Müller, R., Neuroimage 32, 626 (2006).CrossRefGoogle Scholar