Micro- and Nanomechanical Analysis of Articular Cartilage by Indentation-Type Atomic Force Microscopy: Validation with a Gel-Microfiber Composite

Loparić, Marko; Wirz, Dieter; Daniels, A. U.; Raiteri, Roberto; VanLandingham, Mark R.; Guex, Geraldine; Martín, Iván; Aebi, Ueli; Stolz, Martin

doi:10.1016/j.bpj.2010.02.013

Cited by 150 publications

(163 citation statements)

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“…This also explains why the moduli values reported here are an order of magnitude smaller than ones we previously reported on the tissue level (Szabó et al, 2011). Conventional nanoindentation assesses the overall feature behaviour of, for example, a lamella and its vicinity to the applied load (Loparic et al, 2010). To validate the cantilever-based nanoindentation, measurements of two more experiments were conducted to serve as "controls".…”

Section: Discussionmentioning

confidence: 63%

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Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level

Katsamenis

Chong

Andriotis

et al. 2013

Journal of the Mechanical Behavior of Biomedical Materials

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An improved understanding of bone mechanics is vital in the development of evaluation strategies for patients at risk of bone fracture. The current evaluation approach based on bone mineral density (BMD) measurements lacks sensitivity, and it has become clear that as well as bone mass, bone quality should also be evaluated.The latter includes, among other parameters, the bone matrix material properties, which in turn depend on the hierarchical structural features that make up bone as well as their composition. Optimal load transfer, energy dissipation and toughening mechanisms have, to some extent, been uncovered in bone. Yet, the origin of these properties and their dependence upon the hierarchical structure and composition of bone are largely unknown. Here we investigate load transfer in the osteonal and subosteonal levels and the mechanical behaviour of osteonal lamellae and interlamellar areas during loading. Using cantilever-based nanoindentation, in situ microtensile testing during atomic force microscopy (AFM) and digital image correlation (DIC), we report evidence for a previously unknown mechanism. This mechanism transfers load and movement in a manner analogous to the engineered "elastomeric bearing pads" used in large engineering structures. ȝ-RAMAN microscopy investigations 2 showed compositional differences between lamellae and interlamellar areas. The latter have lower collagen content but an increased concentration of noncollagenous proteins (NCPs). Hence, NCPs enriched areas on the microscale might be similarly important for bone failure as on the nanoscale. Finally, we managed to capture stable crack propagation within the interlamellar areas in a time-lapsed fashion, proving their significant contribution towards fracture toughness.

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Section: Discussionmentioning

confidence: 63%

“…Like articular cartilage (Loparic et al, 2010), bone is a nanocomposite material built from components with different mechanical properties (i.e. individual mineralized collagen fibrils and mineralized non-collagenous protein matrix).…”

Section: Discussionmentioning

confidence: 99%

Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level

Katsamenis

Chong

Andriotis

et al. 2013

Journal of the Mechanical Behavior of Biomedical Materials

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“…The related elastic moduli are calculated using the Hertz model (SI Text) (23,24). Note that the determined absolute moduli values depend on the tip shape and the used fitting model; sharp tips are expected to rather probe the local mechanics of the underlying fibrous network (SI Text) (25)(26)(27). The deduced elastic moduli recorded along the follicle axis are shown as boxplots in Fig.…”

Section: Resultsmentioning

confidence: 99%

Keratin network modifications lead to the mechanical stiffening of the hair follicle fiber

Bornschlögl

Bildstein

Thibaut

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The complex mechanical properties of biomaterials such as hair, horn, skin, or bone are determined by the architecture of the underlying fibrous bionetworks. Although much is known about the influence of the cytoskeleton on the mechanics of isolated cells, this has been less studied in tridimensional tissues. We used the hair follicle as a model to link changes in the keratin network composition and architecture to the mechanical properties of the nascent hair. We show using atomic force microscopy that the soft keratinocyte matrix at the base of the follicle stiffens by a factor of ∼360, from 30 kPa to 11 MPa along the first millimeter of the follicle. The early mechanical stiffening is concomitant to an increase in diameter of the keratin macrofibrils, their continuous compaction, and increasingly parallel orientation. The related stiffening of the material follows a power law, typical of the mechanics of nonthermal bending-dominated fiber networks. In addition, we used X-ray diffraction to monitor changes in the (supra)molecular organization within the keratin fibers. At later keratinization stages, the inner mechanical properties of the macrofibrils dominate the stiffening due to the progressive setting up of the cystine network. Our findings corroborate existing models on the sequence of biological and structural events during hair keratinization.atomic force microscopy | elastic modulus | human hair follicle | biomechanics | X-ray diffraction B iological tissues are structurally complex materials with remarkable mechanics and elastic moduli that can range from a few pascals to several gigapascals (1-3). An active field aims at understanding how the local structural and mechanical properties of bionetworks define its macroscopic mechanics from a molecular scale toward a cellular and tissue scale (4-6). One challenge is that the properties of these networks have to be considered over multiple length and force scales with macroscopic mechanical forces being transduced from the whole tissue scale down to the cellular and molecular level and vice versa.At the cellular level, the last decades witnessed for a considerable advancement toward a better understanding of how the cytoskeleton composed of actin, microtubules, and intermediate filaments (IFs) determines cellular mechanics (1,(6)(7)(8). In vitro studies on isolated cells (6) and reconstituted in vitro bionetworks with controllable architecture and composition (9-12) considerably advanced our knowledge of cytoskeletal mechanics. However, these models are only approximations of the complex tridimensional architecture of most tissues. At the tissue level, the mechanical anisotropy together with the variety of mechanically different constituents usually hamper direct correlations between network architecture and mechanical properties (3, 13). Analytical models and computer modeling allow to theoretically link the macroscopic mechanical properties of the network with parameters of the local network architecture (5, 14, 15).The human hair follicle was used here...

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“…S1) or Hertzian theory equations (28). Nano-and microscale moduli exhibited a small increase between HH 28 and 30 (P = 0.11 for nanoscale, P = 0.66 for microscale); changed minimally between HH 30 and 38; and then increased significantly from HH 38-43, where modulus at each stage was significantly different from the preceding stage (P < 0.05) (Fig.…”

mentioning

confidence: 85%

Characterization of mechanical and biochemical properties of developing embryonic tendon

Marturano

Arena

Schiller

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

166

277

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Tendons have uniquely high tensile strength, critical to their function to transfer force from muscle to bone. When injured, their innate healing response results in aberrant matrix organization and functional properties. Efforts to regenerate tendon are challenged by limited understanding of its normal development. Consequently, there are few known markers to assess tendon formation and parameters to design tissue engineering scaffolds. We profiled mechanical and biological properties of embryonic tendon and demonstrated functional properties of developing tendon are not wholly reflected by protein expression and tissue morphology. Using force volume-atomic force microscopy, we found that nano-and microscale tendon elastic moduli increase nonlinearly and become increasingly spatially heterogeneous during embryonic development. When we analyzed potential biochemical contributors to modulus, we found statistically significant but weak correlation between elastic modulus and collagen content, and no correlation with DNA or glycosaminoglycan content, indicating there are additional contributors to mechanical properties. To investigate collagen cross-linking as a potential contributor, we inhibited lysyl oxidasemediated collagen cross-linking, which significantly reduced tendon elastic modulus without affecting collagen morphology or DNA, glycosaminoglycan, and collagen content. This suggests that lysyl oxidase-mediated cross-linking plays a significant role in the development of embryonic tendon functional properties and demonstrates that changes in cross-links alter mechanical properties without affecting matrix content and organization. Taken together, these data demonstrate the importance of functional markers to assess tendon development and provide a profile of tenogenic mechanical properties that may be implemented in tissue engineering scaffold design to mechanoregulate new tendon regeneration.musculoskeletal | second harmonic generation T endon is a principal tissue involved in movement, functioning primarily to transfer loads from muscle to bone. Acute and chronic tendon injuries are significant clinical problems due to poor innate healing ability and drawbacks associated with surgical repair (1, 2). In 2006, musculoskeletal symptoms were the second most frequent reason for physician visits in the United States, resulting in over 130 million visits at a cost of nearly $850 billion (3). Almost half of these visits involved tendons and ligaments, with incidence expected to rise with an aging population. Thus, efforts have focused on engineering new tissues for replacement, although this has been challenged by a paucity of markers with which to assess functional tendon development and few known cues to direct differentiation and new tissue formation.Characterization of tendon formation in embryonic or engineered tissue has typically relied on molecular markers, as well as matrix composition and organization (4-9). Although useful for assessing cell differentiation and ECM deposition during tissue formation, t...

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Micro- and Nanomechanical Analysis of Articular Cartilage by Indentation-Type Atomic Force Microscopy: Validation with a Gel-Microfiber Composite

Cited by 150 publications

References 42 publications

Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level

Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level

Keratin network modifications lead to the mechanical stiffening of the hair follicle fiber

Characterization of mechanical and biochemical properties of developing embryonic tendon

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