The role of mechanics in biological and bio-inspired systems

Nature Communications

Volumn 6, Issue , 2015, Pages

  Egan, Paul ^a   Sinko, Robert ^b   Leduc, Philip R ^a   Keten, Sinan ^b  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b Northwestern University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; NANOCRYSTAL; SILK; BIOMATERIAL; BIOMIMETIC MATERIAL;

BIOMECHANICS; BREAKTHROUGH CURVE; MEDICINE; STRENGTH; WEIGHT;

BIOENGINEERING; BIOLOGY; BIOMECHANICS; BIOMIMETICS; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; REVIEW; CHEMISTRY; MECHANICS; NANOTECHNOLOGY;

BIOCOMPATIBLE MATERIALS; BIOMECHANICAL PHENOMENA; BIOMIMETIC MATERIALS; MECHANICS; NANOTECHNOLOGY;

EID: 84936797766     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8418     Document Type: Review

References (110)

1. Cranford, S., de Boer, J., van Blitterswijk, C. & Buehler, M. Materiomics: an-omics approach to biomaterials research. Adv. Mater. 25, 802-824 (2013).
2. Chen, P.-Y., McKittrick, J. & Meyers, M. A. Biological materials: functional adaptations and bioinspired designs. Prog. Mater. Sci. 57, 1492-1704 (2012).
3. Espinosa, H. D., Rim, J. E., Barthelat, F. & Buehler, M. J. Merger of structure and material in nacre and bone-perspectives on de novo biomimetic materials. Prog. Mater. Sci. 54, 1059-1100 (2009).
4. Weaver, J. C. et al. The stomatopod dactyl club: a formidable damage-tolerant biological hammer. Science 336, 1275-1280 (2012).
5. Modery-Pawlowski, C. L. et al. Approaches to synthetic platelet analogs. Biomaterials 34, 526-541 (2013).
6. Munch, E. et al. Tough, bio-inspired hybrid materials. Science 322, 1516-1520 (2008).
7. Nudelman, F., Gotliv, B. A., Addadi, L. & Weiner, S. Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. J. Struct. Biol. 153, 176-187 (2006).
8. Seki, Y., Schneider, M. S. & Meyers, M. A. Structure and mechanical behavior of a toucan beak. Acta Mater. 53, 5281-5296 (2005).
9. Szulgit, G. K. & Shadwick, R. E. Dynamic mechanical characterization of a mutable collagenous tissue: response of sea cucumber dermis to cell lysis and dermal extracts. J. Exp. Biol. 203, 1539-1550 (2000).
10. Burgert, I., Eder, M., Gierlinger, N. & Fratzl, P. Tensile and compressive stresses in tracheids are induced by swelling based on geometrical constraints of the wood cell. Planta 226, 981-987 (2007).
11. Vollrath, F. & Knight, D. P. Liquid crystalline spinning of spider silk. Nature 410, 541-548 (2001).
12. Resnicow, D. I., Deacon, J. C., Warrick, H. M., Spudich, J. A. & Leinwand, L. A. Functional diversity among a family of human skeletal muscle myosin motors. Proc. Natl Acad. Sci. USA 107, 1053-1058 (2010).
13. Egan, P., Cagan, J., Schunn, C. & LeDuc, P. Design of complex biologically based nanoscale systems using multi-agent simulations and structure-behavior-function representations. J. Mech. Design 135, 061005 (2013).
14. Studart, A. R. Towards high-performance bioinspired composites. Adv. Mater. 24, 5024-5044 (2012).
15. Marshall, R. C., Orwin, D. F. G. & Gillespie, J. M. Structure and biochemistry of mammalian hard keratin. Electron Microsc. Rev. 4, 47-83 (1991).
16. Ackbarow, T., Chen, X., Keten, S. & Buehler, M. J. Hierarchies, multiple energy barriers, and robustness govern the fracture mechanics of alpha-helical and beta-sheet protein domains. Proc. Natl Acad. Sci. USA 104, 16410-16415 (2007).
17. Qin, G., Hu, X., Cebe, P. & Kaplan, D. L. Mechanism of resilin elasticity. Nat. Commun. 3, 1003 (2012).
18. Elvin, C. M. et al. Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437, 999-1002 (2005).
19. Mammoto, A., Mammoto, T. & Ingber, D. E. Mechanosensitive mechanisms in transcriptional regulation. J. Cell Sci. 125, 3061-3073 (2012).
20. Lecuit, T., Lenne, P.-F. & Munro, E. Force Generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27, 157-184 (2011).
21. Cheng, C.-M. et al. Probing localized neural mechanotransduction through surface-modified elastomeric matrices and electrophysiology. Nat. Protoc. 5, 714-724 (2010).
22. Chou, S.-Y., Cheng, C.-M., Chen, C.-C. & LeDuc, P. R. Localized neurite outgrowth sensing via substrates with alternative rigidities. Soft Matter 7, 9871-9877 (2011).
23. Tan, C., Saurabh, S., Bruchez, M. P., Schwartz, R. & LeDuc, P. Molecular crowding shapes gene expression in synthetic cellular nanosystems. Nat. Nanotechnol. 8, 602-608 (2013).
24. Huveneers, S. & de Rooij, J. Mechanosensitive systems at the cadherin-F-actin interface. J. Cell. Sci. 126, 403-413 (2013).
25. Lutolf, M. P., Gilbert, P. M. & Blau, H. M. Designing materials to direct stem-cell fate. Nature 462, 433-441 (2009).
26. Guilak, F., Butler, D. L., Goldstein, S. A. & Baaijens, F. Biomechanics and mechanobiology in functional tissue engineering. J. Biomech. 47, 1933-1940 (2014).
27. Cross, S. E., Jin, Y.-S., Rao, J. & Gimzewski, J. K. Nanomechanical analysis of cells from cancer patients. Nat. Nanotechnol. 2, 780-783 (2007).
28. Kumar, S. & Weaver, V. M. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113-127 (2009).
29. Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009).
30. Tse, J. M. et al. Mechanical compression drives cancer cells toward invasive phenotype. Proc. Natl Acad. Sci. USA 109, 911-916 (2012).
31. Ruder, W. C. et al. Three-dimensional microfiber devices that mimic physiological environments to probe cell mechanics and signaling. Lab Chip 12, 1775-1779 (2012).
32. Bao, G. & Suresh, S. Cell and molecular mechanics of biological materials. Nat. Mater. 2, 715-725 (2003).
33. Fratzl, P. Biomimetic materials research: what can we really learn from nature's structural materials? J. R. Soc. Interface 4, 637-642 (2007).
34. Gao, H. J., Ji, B. H., Jager, I. L., Arzt, E. & Fratzl, P. Materials become insensitive to flaws at nanoscale: lessons from nature. Proc. Natl Acad. Sci. USA 100, 5597-5600 (2003).
35. Janmey, P. A. & McCulloch, C. A. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9, 1-34 (2007).
36. Naraghi, M., Arshad, S. N. & Chasiotis, I. Molecular orientation and mechanical property size effects in electrospun polyacrylonitrile nanofibers. Polymer 52, 1612-1618 (2011).
37. Szymanski, D. B. & Cosgrove, D. J. Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr. Biol. 19, R800-R811 (2009).
38. Tang, Z. Y., Kotov, N. A., Magonov, S. & Ozturk, B. Nanostructured artificial nacre. Nat. Mater. 2, U413-U418 (2003).
39. Gautieri, A., Vesentini, S., Redaelli, A. & Buehler, M. J. Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett. 11, 757-766 (2011).
40. Meyers, M. et al. Structural biological composites: An overview. JOM 58, 35-41 (2006).
41. Zimmermann, E. A. et al. Mechanical adaptability of the Bouligand-type structure in natural dermal armour. Nat. Commun. 4, 2634 (2013).
42. Qin, Z. & Buehler, M. J. Impact tolerance in mussel thread networks by heterogeneous material distribution. Nat. Commun. 4, 2187 (2013).
43. Keten, S. & Buehler, M. J. Atomistic model of the spider silk nanostructure. Appl. Phys. Lett. 96, 153701 (2010).
44. Keten, S. & Buehler, M. J. Nanostructure and molecular mechanics of spider dragline silk protein assemblies. J. R. Soc. Interface 7, 1709-1721 (2010).
45. Rammensee, S., Slotta, U., Scheibel, T. & Bausch, A. R. Assembly mechanism of recombinant spider silk proteins. Proc. Natl Acad. Sci. USA 105, 6590-6595 (2008).
46. Knowles, T. P. et al. Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900-1903 (2007).
47. Keten, S., Xu, Z., Ihle, B. & Buehler, M. J. Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nat. Mater. 9, 359-367 (2010).
48. Ruiz, L., VonAchen, P., Lazzara, T. D., Xu, T. & Keten, S. Persistence length and stochastic fragmentation of supramolecular nanotubes under mechanical force. Nanotechnology 24, 195103 (2013).
49. Knowles, T. P. J. & Buehler, M. J. Nanomechanics of functional and pathological amyloid materials. Nat. Nanotechnol. 6, 469-479 (2011).
50. Sinko, R., Mishra, S., Ruiz, L., Brandis, N. & Keten, S. Dimensions of biological cellulose nanocrystals maximize fracture strength. ACS Macro Lett. 3, 64-69 (2013).
51. Fullenkamp, D. E. et al. Mussel-inspired silver-releasing antibacterial hydrogels. Biomaterials 33, 3783-3791 (2012).
52. Espinosa, H. D. et al. Tablet-level origin of toughening in abalone shells and translation to synthetic composite materials. Nat. Commun. 2, 173 (2011).
53. Balazs, A. C., Kuksenok, O. & Alexeev, A. Modeling the interactions between membranes and inclusions: designing self-cleaning films and resealing pores. Macromol. Theory Simul. 18, 11-24 (2009).
54. Capadona, J. R., Shanmuganathan, K., Tyler, D. J., Rowan, S. J. & Weder, C. Stimuli-responsive polymer nanocomposites inspired by the sea cucumber dermis. Science 319, 1370-1374 (2008).
55. Neiman, V. J. & Varghese, S. Synthetic bio-actuators and their applications in biomedicine. Smart Struct. Syst. 7, 185-198 (2011).
56. Erb, R. M., Sander, J. S., Grisch, R. & Studart, A. R. Self-shaping composites with programmable bioinspired microstructures. Nat. Commun. 4, 1712 (2013).
57. Archer, R. R. & Wilson, B. F. Apical control of branch movements in white pine: compression wood action. Wood Sci. Technol. 16, 181-191 (1982).
58. Blackledge, T. A. et al. How super is supercontraction? Persistent versus cyclic responses to humidity in spider dragline silk. J. Exp. Biol. 212, 1981-1989 (2009).
59. Calvert, P. Gel Sensors and actuators. MRS Bull. 33, 207-212 (2008).
60. Haines, C. S. et al. Artificial muscles from fishing line and sewing thread. Science 343, 868-872 (2014).
61. Illeperuma, W. R. K., Sun, J.-Y., Suo, Z. & Vlassak, J. J. Force and stroke of a hydrogel actuator. Soft Matter 9, 8504-8511 (2013).
62. Knoblauch, M. et al. ATP-independent contractile proteins from plants (vol 2, pg 600, 2003). Nat. Mater. 4, 353-353 (2005).
63. Leary, M., Schiavone, F. & Subic, A. Lagging for control of shape memory alloy actuator response time. Mater. Des. 31, 2124-2128 (2010).
64. Lee, H., Xia, C., Fang, N. X. & Asme in Proceedings of (ASME 2008 International Mechanical Engineering Congress and Exposition), 765-769 (Boston, Massachusetts, USA, 2008).
65. Lima, M. D. et al. Electrically, chemically, and photonically powered torsional and tensile actuation of hybrid carbon nanotube yarn muscles. Science 338, 928-932 (2012).
66. Morales, D., Palleau, E., Dickey, M. D. & Velev, O. D. Electro-actuated hydrogel walkers with dual responsive legs. Soft Matter 10, 1337-1348 (2014).
67. Saralegi, A. et al. Shape-memory bionanocomposites based on chitin nanocrystals and thermoplastic polyurethane with a highly crystalline soft segment. Biomacromolecules 14, 4475-4482 (2013).
68. Smith, S. et al. Force generation of different human cardiac valve interstitial cells: relevance to individual valve function and tissue engineering. J. Heart Valve Dis. 16, 440-446 (2007).
69. Volkov, A. G., Adesina, T., Markin, V. S. & Jovanov, E. Kinetics and mechanism of dionaea muscipula trap closing. Plant Physiol. 146, 694-702 (2008).
70. Elbaum, R., Zaltzman, L., Burgert, I. & Fratzl, P. The role of wheat awns in the seed dispersal unit. Science 316, 884-886 (2007).
71. Fratzl, P. & Barth, F. G. Biomaterial systems for mechanosensing and actuation. Nature 462, 442-448 (2009).
72. Nawroth, J. C. et al. A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 30, 792-797 (2012).
73. Spatz, J. P. Bio-MEMS: building up micromuscles. Nat. Mater. 4, 115-116 (2005).
74. Ruff, C., Fuch, M., Brenner, B., Manstein, D. J. & Meyhoefer., E. Single-molecule tracking of myosins with genetically engineered amplifier domains. Nat. Struct. Biol. 8, 226-229 (2001).
75. Rome, L. C. Design and function of superfast muscles. Annu. Rev. Physiol. 68, 22.21-22.29 (2005).
76. Ito, K. et al. Kinetic mechanism of the fastest motor protein, Chara myosin J. Biol. Chem. 282, 19534-19545 (2007).
77. Harris, D. E., Work, S. S., Wright, R. K., Alpert, N. R. & Warshaw., D. M. Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. J. Muscle Res. Cell Motil. 15, 11-19 (1994).
78. Tsiavaliaris, G., Fujita-Becker, S. & Manstein, D. J. Molecular engineering of a backwards-moving myosin motor. Nature 427, 558-561 (2004).
79. Egan, P., Moore, J., Schunn, C., Cagan, J. & LeDuc, P. Emergent systems energy laws for predicting myosin ensemble processivity. PLoS Comput. Biol. 11, e1004177 (2015).
80. Li, L. & Kiick, K. L. Resilin-based materials for biomedical applications. ACS Macro Lett. 2, 635-640 (2013).
81. Renner, J. N., Cherry, K. M., Su, R. S. C. & Liu, J. C. Characterization of resilin-based materials for tissue engineering applications. Biomacromolecules 13, 3678-3685 (2012).
82. Eichhorn, S. J. & Young, R. J. The Young's modulus of a microcrystalline cellulose. Cellulose 8, 197-207 (2001).
83. Martinez-Camacho, A. P. et al. Extruded films of blended chitosan, low density polyethylene and ethylene acrylic acid. Carbohydr. Polym. 91, 666-674 (2013).
84. Bhowmik, R., Katti, K. S. & Katti, D. R. Mechanics of molecular collagen is influenced by hydroxyapatite in natural bone. J. Mater. Sci. 42, 8795-8803 (2007).
85. Buehler, M. J. Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization. Nanotechnology 18, 295102 (2007).
86. Gao, H. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int. J. Fract. 138, 101-137 (2006).
87. Hamed, E. & Jasiuk, I. Elastic modeling of bone at nanostructural level. Mater. Sci. Eng. R 73, 27-49 (2012).
88. Sellinger, A. et al. Continuous self-assembly of organic-inorganic nanocomposite coatings that mimic nacre. Nature 394, 256-260 (1998).
89. Korin, N. et al. Shear-activated nanotherapeutics for drug targeting to obstructed blood vessels. Science 337, 738-742 (2012).
90. Yoo, J.-W., Doshi, N. & Mitragotri, S. Adaptive micro and nanoparticles: temporal control over carrier properties to facilitate drug delivery. Adv. Drug Deliv. Rev. 63, 1247-1256 (2011).
91. Merkel, T. J. et al. Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proc. Natl Acad. Sci. USA 108, 586-591 (2011).
92. Xia, F. & Jiang, L. Bio-inspired, smart, multiscale interfacial materials. Adv. Mater. 20, 2842-2858 (2008).
93. Kratz, K. et al. Probing and repairing damaged surfaces with nanoparticle-containing microcapsules. Nat. Nanotechnol. 7, 87-90 (2012).
94. Menges, A. & Reichert, S. Material capacity: embedded responsiveness. Archit. Design 82, 52-59 (2012).
95. LeDuc, P. R. et al. Towards an in vivo biologically inspired nanofactory. Nat. Nanotechnol. 2, 3-7 (2007).
96. Moon, R. J., Martini, A., Nairn, J., Simonsen, J. & Youngblood, J. Cellulose nanomaterials review: structure, properties and nanocomposites. Chem. Soc. Rev. 40, 3941-3994 (2011).
97. Yang, K.-K., Wang, X.-L. & Wang, Y.-Z. Progress in nanocomposite of biodegradable polymer. J. Ind. Eng. Chem. 13, 485-500 (2007).
98. Jackson, A. P., Vincent, J. F. V. & Turner, R. M. The mechanical design of nacre. Proc. R. Soc. Lond. B 234, 415-440 (1988).
99. Carpi, F. & Smela, E. Biomedical Applications of Electroactive Polymer Actuators (John Wiley & Sons, 2009).
100. Matsumoto, N. & Nairn, J. A. The fracture toughness of medium density fiberboard (MDF) including the effects of fiber bridging and crack-plane interference. Eng. Fract. Mech. 76, 2748-2757 (2009).
101. Ritchie, R. O., Buehler, M. J. & Hansma, P. Plasticity and toughness in bone. Phys. Today 62, 41-47 (2009).
102. Dirks, J.-H. & Taylor, D. Fracture toughness of locust cuticle. J. Exp. Biol. 215, 1502-1508 (2012).
103. Taylor, D., O'Mara, N., Ryan, E., Takaza, M. & Simms, C. The fracture toughness of soft tissues. J. Mech. Behav. Biomed. Mater. 6, 139-147 (2012).
104. Dastjerdi, A., Pagano, M., Kaartinen, M., McKee, M. & Barthelat, F. in Conference Proceedings of the Society for Experimental Mechanics Series, Vol. 5 (eds Prorok, B. C. et al.) Ch. 29 207-215 (Springer, 2013).
105. Porter, D., Guan, J. & Vollrath, F. Spider Silk: super material or thin fibre? Adv. Mater. 25, 1275-1279 (2013).
106. Wang, C.-A., Huang, Y., Zan, Q., Guo, H. & Cai, S. Biomimetic structure design-a possible approach to change the brittleness of ceramics in nature. Mater. Sci. Eng. C 11, 9-12 (2000).
107. Okubo, K., Fujii, T. & Yamashita, N. Improvement of interfacial adhesion in bamboo polymer composite enhanced with micro-fibrillated cellulose. JSME Int. J. A-Solid M. 48, 199-204 (2005).
108. Mushi, N. E., Utsel, S. & Berglund, L. A. Nanostructured biocomposite films of high toughness based on native chitin nanofibers and chitosan. Front. Chem. 2, 99 (2014).
109. Bratzel, G. & Buehler, M. J. Sequence-structure correlations in silk: poly-Ala repeat of N. clavipes MaSp1 is naturally optimized at a critical length scale. J. Mech. Behav. Biomed. Mater. 7, 30-40 (2012).
110. Harrington, M. J. et al. Origami-like unfolding of hydro-actuated ice plant seed capsules. Nat. Commun. 2, 337 (2011).