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Solving conflicting functional requirements by hierarchical structuring—Examples from biological materials

Published online by Cambridge University Press:  08 September 2016

Richard Weinkamer
Affiliation:
Department of Biomaterials, Campus Golm, Max Planck Institute of Colloids and Interfaces, Germany; [email protected]
Peter Fratzl
Affiliation:
Department of Biomaterials, Campus Golm, Max Planck Institute of Colloids and Interfaces, Germany; [email protected]
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Abstract

Hierarchical structure is a hallmark of many biological materials that naturally originate from their growth process, which starts with the biosynthesis of molecular building blocks that self-assemble into larger units. Compartmentalization is used to locally control the synthesis and self-assembly and, thus bridge multiple length scales between the atomistic and macroscopic worlds. Multiscalar structures have the advantage that different physical properties may be adjusted at various structural levels. In particular, when these properties are conflicting, the result can lead to exceptional multifunctional materials. The fiber is a ubiquitous structural motif of biological materials, although its biochemical basis can be diverse. While fibers perform well under tension, they do not under compression. Biological materials are also adaptive and possess self-repair capabilities—properties that require the transport of matter and information. This requires networks of transport and communication that are also hierarchically organized to conciliate the conflicting goals of maximum accessibility and minimal perforation of the material volume. Several examples are discussed in this article.

Type
Research Article
Copyright
Copyright © Materials Research Society 2016 

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References

Fratzl, P., Dunlop, J.W.C., Weinkamer, R., Eds., Materials Design Inspired by Nature: Function through Inner Architecture, RSC Smart Materials No. 4 (RSC Publishing, Cambridge, UK, 2013).Google Scholar
Fratzl, P., J.R. Soc. Interface 4, 637 (2007).Google Scholar
Wegst, U.G.K., Bai, H., Saiz, E., Tomsia, A.P., Ritchie, R.O., Nat. Mater. 14, 23 (2015).Google Scholar
Grinthal, A., Aizenberg, J., Chem. Soc. Rev. 42, 7072 (2013).Google Scholar
Ortiz, C., Boyce, M.C., Science 319, 1053 (2008).Google Scholar
Bhushan, B., Philos. Trans. R. Soc. Lond. A 367, 1445 (2009).Google Scholar
Fratzl, P., Weinkamer, R., Prog. Mater. Sci. 52, 1263 (2007).CrossRefGoogle Scholar
Spaargaren, D.H., Oceanol. Acta 14, 569 (1991).Google Scholar
Degtyar, E., Harrington, M.J., Politi, Y., Fratzl, P., Angew. Chem. Int. Ed. 53, 12026 (2014).Google Scholar
Lichtenegger, H.C., Schoberl, T., Ruokolainen, J.T., Cross, J.O., Heald, S.M., Birkedal, H., Waite, J.H., Stucky, G.D., Proc. Natl. Acad. Sci. U.S.A. 100, 9144 (2003).Google Scholar
Harrington, M.J., Masic, A., Holten-Andersen, N., Waite, J.H., Fratzl, P., Science 328, 216 (2010).Google Scholar
Politi, Y., Priewasser, M., Pippel, E., Zaslansky, P., Hartmann, J., Siegel, S., Li, C.H., Barth, F.G., Fratzl, P., Adv. Funct. Mater. 22, 2519 (2012).Google Scholar
Fratzl, P., Collagen: Structure and Mechanics (Springer, New York, 2008).Google Scholar
Wang, B., Yang, W., McKittrick, J., Meyers, M.A., Prog. Mater. Sci. 76, 229 (2016).Google Scholar
Heim, M., Keerl, D., Scheibel, T., Angew. Chem. Int. Ed. 48, 3584 (2009).CrossRefGoogle Scholar
Keten, S., Xu, Z.P., Ihle, B., Buehler, M.J., Nat. Mater. 9, 359 (2010).CrossRefGoogle Scholar
Fabritius, H.O., Sachs, C., Triguero, P.R., Roobe, D., Adv. Mater. 21, 391 (2009).Google Scholar
Roach, H.I., Cell Biol. Int. 18, 617 (1994).Google Scholar
Shoulders, M.D., Raines, R.T., Annu. Rev. Biochem. 78, 929 (2009).Google Scholar
Knott, L., Bailey, A.J., Bone 22 (3), 181 (1998).Google Scholar
Bouligan, Y., Tissue Cell 4, 189 (1972).Google Scholar
Zimmermann, E.A., Gludovatz, B., Schaible, E., Dave, N.K.N., Yang, W., Meyers, M.A., Ritchie, R.O., Nat. Commun. 4, 2634 (2013).Google Scholar
Langer, M., Pacureanu, A., Suhonen, H., Grimal, Q., Cloetens, P., Peyrin, F., PLoS One 7, e35691 (2012).Google Scholar
Lefevre, C.T., Bennet, M., Landau, L., Vach, P., Pignol, D., Bazylinski, D.A., Frankel, R.B., Klumpp, S., Faivre, D., Biophys. J. 107, 527 (2014).Google Scholar
Faivre, D., MRS Bull. 40, 509 (2015).Google Scholar
Chen, A.P., Berounsky, V.M., Chan, M.K., Blackford, M.G., Cady, C., Moskowitz, B.M., Kraal, P., Lima, E.A., Kopp, R.E., Lumpkin, G.R., Weiss, B.P., Hesse, P., Vella, N.G.F., Nat. Commun. 5, 4797 (2014).CrossRefGoogle Scholar
Gao, H.J., Ji, B.H., Jager, I.L., Arzt, E., Fratzl, P., Proc. Natl. Acad. Sci. U.S.A. 100, 5597 (2003).Google Scholar
Kolednik, O., Predan, J., Fischer, F.D., Fratzl, P., Acta Mater. 68, 279 (2014).Google Scholar
Zlotnikov, I., Shilo, D., Dauphin, Y., Blumtritt, H., Werner, P., Zolotoyabko, E., Fratzl, P., RSC Adv. 3, 5798 (2013).Google Scholar
Wu, X., Erbe, A., Raabe, D., Fabritius, H.O., Adv. Funct. Mater. 23, 3615 (2013).Google Scholar
Vukusic, P., Sambles, J.R., Nature 424, 852 (2003).CrossRefGoogle Scholar
Parker, A.R., J. Opt. A Pure Appl. Opt. 2, R15 (2000).CrossRefGoogle Scholar
Glover, B.J., Whitney, H.M., Ann Bot. 105, 505 (2010).Google Scholar
Doucet, S.M., Meadows, M.G., J.R. Soc. Interface 6, S115 (2009).Google Scholar
Liu, F., Dong, B.Q., Liu, X.H., Zheng, Y.M., Zi, J., Opt. Express 17, 16183 (2009).Google Scholar
Gur, D., Palmer, B.A., Leshem, B., Oron, D., Fratzl, P., Weiner, S., Addadi, L., Angew. Chem. Int. Ed. 54, 12426 (2015).Google Scholar
Su, Y.W., Ji, B.H., Huang, Y., Hwang, K.C., Langmuir 26, 18926 (2010).Google Scholar
Arzt, E., Gorb, S., Spolenak, R., Proc. Natl. Acad. Sci. U.S.A. 100, 10603 (2003).Google Scholar
Arzt, E., Mater. Sci. Eng. C 26, 1245 (2006).Google Scholar
Fratzl, P., Kolednik, O., Fischer, F.D., Dean, M.N., Chem. Soc. Rev. 45, 252 (2016).Google Scholar
Gao, H.J., Wang, X., Yao, H.M., Gorb, S., Arzt, E., Mech. Mater. 37, 275 (2005).Google Scholar
Sun, J., Bhushan, B., RSC Adv. 2 (20), 7617 (2012).Google Scholar
Bruet, B.J.F., Song, J.H., Boyce, M.C., Ortiz, C., Nat. Mater. 7, 748 (2008).Google Scholar
Krauss, S., Monsonego-Ornan, E., Zelzer, E., Fratzl, P., Shahar, R., Adv. Mater. 21, 407 (2009).Google 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
Fratzl, P., Barth, F.G., Nature 462, 442 (2009).CrossRefGoogle Scholar
Loyau, A., Gomez, D., Moureau, B.T., Thery, M., Hart, N.S., Saint Jalme, M., Bennett, A.T.D., Sorci, G., Behav. Ecol. 18, 1123 (2007).Google Scholar
Zi, J., Yu, X.D., Li, Y.Z., Hu, X.H., Xu, C., Wang, X.J., Liu, X.H., Fu, R.T., Proc. Natl. Acad. Sci. U.S.A. 100, 12576 (2003).Google Scholar
Weiss, I.M., Kirchner, H.O.K., J. Exp. Zool. A 313A, 690 (2010).Google Scholar
Pabisch, S., Puchegger, S., Kirchner, H.O.K., Weiss, I.M., Peterlik, H., J. Struct. Biol. 172, 270 (2010).Google Scholar
Bonewald, L.F., J. Bone Miner. Res. 26, 229 (2011).Google Scholar
Kerschnitzki, M., Kollmannsberger, P., Burghammer, M., Duda, G.N., Weinkamer, R., Wagermaier, W., Fratzl, P., J. Bone Miner. Res. 28, 1837 (2013).Google Scholar