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Journal Club Theme of Feb. 1 2008: Mechanics of Protein Structures and Materials - Silks, Amyloids and Muscle Fibers

Proteins are the key building blocks of all biological matter. While engineers predominantly use concrete, metals, ceramics and synthetic polymers as structural materials for their high strength and durability, Nature exploits complex mechanical and chemical features of proteins for building strong, elastic and robust materials and structures. For example, spider silk, amyloid (sturdy protein fibrils found in many diseases) and muscle fibers are made entirely of proteins and blend extensibility with high strength to achive extreme toughness. These super-fibers represent an alternative scheme of material design to biomineralization, which allows for incorporation of minerals in protein scaffolds to build very stiff and tough materials such as nacre, mollusk shells and bone. Many scientists have been intrigued by Nature's unknown recipe for creating soft yet durable and strong materials. These materials are different from their synthetic equivalents because they employ hydrogen bonds that are much weaker than covalent or metallic bonds, and exhibit entropic elasticity at the nano-scale.

Protein materials such as spider silk have a modular, hierarchical architecture that extends from nano to macro. This leads to very complex mechanical behavior at macro-scale which can't easily be described by simple continuum formulations. Early attempts in the field to explain elasticity of biopolymers such as silk illustrated the need to take into account the micro-structural features of the material for describing the mechanical behavior. The first paper by Yves Termonia [1] is one of the early modeling attempts of spider silk elasticity using structural evidence from X-ray diffraction studies. A key finding from this paper is that the size of beta-sheet nanocrystals in spider silk influences elastic behavior and the observed structures in silk are optimal from a mechanical perspective.

The second paper [2] is a recent review on the mechanical characterization of individual proteins using experimental techniques (for instance Atomic Force Microscopy [AFM]) and computational approaches (for instance Steered Molecular Dynamics [SMD] simulations). The studies reviewed in this work explore mechanical functions of proteins at the nano-scale and molecular mechanisms of the elasticity of extracellular matrix and muscle proteins. Nanomechanical characterization of proteins by computational and experimental approaches is a crucial step in building multi-scale models that can accurately predict macro-scale behavior of biological materials. Therefore, scientists working in this field generally need to appreciate both continuum approaches (constitutive relations, FEM studies etc.) as well as biophysical studies (single protein manipulation, statistical mechanics).

The last paper [3] is a very recent study on amyloids, protein materials that were subject to a tremendous amount of research in the past decade due to their association with many diseases. Amyloid protein structures constitute an intriguing class of protein materials that self-assemble at room temperature into very stable and structured fibrils. Amyloid deposits in tissue are known to be linked to pathological conditions that occur in diseases such as Alzheimer's, Parkinson's, prion diseases or type II diabetes. Amyloids also have intriguing properties that resemble spider silk, and are found in many natural adhesives. The AFM study referenced here is one of the few experiments that investigated the elasticity and fracture behavior of amyloids. Along with other studies, this paper shows that the intriguing mechanical properties (e.g. elastic modulus comparable to spider silk) of amyloid fibrils derive from generic interbackbone hydrogen-bonding network common to all amyloids.

These are only a few examples of the many inspirational and exciting works that study protein materials from a mechanical perspective. The three papers included here are not nearly enough to cover all aspects of the rapidly developing field of protein mechanics, but will hopefully illustrate promising directions in the field and promote some discussion regarding elasticity, deformation and fracture mechanics of protein structures and materials.


1. Termonia, Y., Molecular Modeling of Spider Silk Elasticity. Macromolecules, 1994. 27(25): p. 7378-7381.

2. Sotomayor, M. and K. Schulten, Single-molecule experiments in vitro and in silico. Science, 2007. 316(5828): p. 1144-1148.

3. Knowles, T.P., et al., Role of intermolecular forces in defining material properties of protein nanofibrils. Science, 2007. 318(5858): p. 1900-1903.



Keten, Thanks for your writing up the jClub article for Feb 1st.

As you mentioned about Termonia's paper, it is conceived that beta-sheet is responsible for elasticity. However, Termonia's viewpoint may not be sufficient to represent the elasticity of spider silk protein, To my knowledge, Hansma and coworkers published the elasticity of spider silk protein based on single-molecule AFM experiments at Nature Materials (Click Here). In their work, they remarkably found that the spider silk protein has the heirarchical molecular structures based on their observation that the elastic responses of bulk spider silk and spider silk protein are qualitatively comparable to each other. In that paper, Dima Makarov and Hellen Hansma suggested the hierarhical spring model for spider silk protein.

There are recent works on AFM experiments for finding the mechanical properties of biomolecules such as amyloid fibril and microtubule. If one is interested in the paper 3 (Welland's paper in Science), then the paper by Florin will be also interesting (Click Here). In Florin's paper, the relationship between persistence length (representing the bending rigidity) and the contour length for microtubule fiber is suggested based on simple elastic beam model (Timoshenko beam model).

Dr. Eom, thanks for your post regarding spider silk properties and pointing out to the interesting article by Hansma and coworkers. To the best of my knowledge, this is one of the few models developed for spider capture silk, along with the hierarchical chain model developed by Zhou et al. whereas Termonia's model focused on the spider dragline silk. I'd be curious to know if there is any molecular structure based model that can explain both dragline and capture silk's mechanical signature, using for instance different input parameters.

MichelleLOyen's picture

I have been very curious to see recent work on AFM indentation of proteins or protein bundles, especially in the context of fibrillar proteins such as collagen.  I can understand what is being measured in the single-molecule protein unfolding experiments using AFM, but the indentation experiments are also being done.  Fibrillar protein materials have very low transverse stiffness due to very little covalent bonding between individual molecules, and would be very different in transverse compression compared with in tension.  The tensile behavior, in which the strong covalent bonds are more or less aligned in the tensile direction, would seem more obvious to me for study using say  optical tweezers experiments rather than indentation.   I have thus had a difficult time parsing what is being measured in an indentation on a transversely-lying fibril; some longitudinal measurements have been made in resin-embedded samples in cross section (hair, silk) and those I can understand much better than the transverse ones.  Perhaps someone has an idea of what is being sought in measuring transverse fibrils by indentation.

Hi Michelle, this is an excellent comment. Transverse experiments have come up primarily in amyloid studies as far as I know. Amyloid structure is quite intriguing because the weak H-bonds are oriented in the direction of the fibril axis and the beta-sheet strands are stacked up such that the covalently bonded polypeptide chains lie in transverse direction. So the analogous loading conditions to single molecule pulling experiments would be transverse loading in amyloids, where H-bonds are sheared between  beta-strands. Protein structures such as Ig domains in titin have a shear topology that makes them resistant to external forces since H-bonds are uniformly sheared in parallel. Transversely loaded amyloid fibrils hypothetically exhibit similar mechanical features governed by the rupture of interstrand H-bonds. The most interesting observation would be that the bending stiffness and elastic moduli calculated from these experiments are significantly high, comparable to steel or dragline silk, despite the weak hydrogen bonding. It is very intriguing how a material made primarily out of weak bonds can exhibit such high a modulus and strength.

Tensile testing for a fibrillar material like collagen makes much more intuitive sense as the monomeric molecules run in the same direction as the fibril axis. Also, collagenous tissues such as tendons (bundles of collagen fibres) are anatomically arranged so that most of the applied work done is in the same direction as the fibril axis.

However, I do feel that there is a need to examine the transverse properties as this reflects how the material, at fibrillar and tissue level, reacts due to impact and compressions that may occur say during sport (eg being kicked on ankle - Achilles tendon)

Thanks for giving an introduction to this interesting topic.

I am not familiar with this field, but just remember recently I saw a paper provide a general model for silk mechanical properites based on linear viscoelasticity in PRL (Igor Krasnov, Imke Diddens, Nadine Hauptmann, Gesa Helms, Malte Ogurreck, Tilo Seydel, Sérgio S. Funari, and Martin Müller, 2008, PRL, "Mechanical Properties of Silk: Interplay of Deformation on Macroscopic and Molecular Length Scales").

Hope this might be helpful.

Thanks a lot for this interesting discussion. I think that indentation of cross section and in situ imaging will uncover some structural feature and the mechanical properties across the section. Another cross checking test will help to validate the results - like tensile test using a nanotensile tester. I think that Mother Nature has already created an excellent recipe for making composite fibers - silks. This may inspire us to make silk -like composite fiber materials. There are still a lot we need to learn from nature.  Again, thanks for this nice J-Club theme .


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