Arterial Extracellular Matrix: A Mechanobiological Study of the Contributions and Interactions of Elastin and Collagen

Chow, Ming-Jay; Turcotte, Raphaël; Lin, Charles P.; Zhang, Yanhang

doi:10.1016/j.bpj.2014.05.014

Cited by 173 publications

(196 citation statements)

References 55 publications

(65 reference statements)

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“…Upon mechanical loading, the collagen bundles progressively unfold [8,21]. The measurement of fiber waviness [11,44,53,49] revealed in particular that recruitment, or engagement of collagen fibers, is gradual (unsynchronized among fibers) and starts at a finite strain [23,13]. The process can differ whether the observed vascular region is close or remote from the heart (distal regions vs. proximal regions) [55].…”

Section: Introductionmentioning

confidence: 99%

Kinematics of collagen fibers in carotid arteries under tension-inflation loading

Krasny

Magoariec

Morin

et al. 2018

Journal of the Mechanical Behavior of Biomedical Materials

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Biomechanics of the extracellular matrix in arteries determines their macroscopic mechanical behavior. In particular, the distribution of collagen fibers and bundles plays a significant role. Experimental data showed that in most arterial walls there are preferred fiber directions. However, the realignment of collagen fibers during tissue deformation is still controversial: whilst authors claim that fibers should undergo affine deformations, others showed the contrary. In order to have an insight about this important question of affine deformations at the microscopic scale, we measured the realignment of collagen fibers in the adventitia layer of carotid arteries using multiphoton microscopy combined with an unprecedented Fourier based method. We compared the realignment for two types of macroscopic loading applied on arterial segments: axial tension under constant pressure (scenario 1) and inflation under constant axial length (scenario 2). Results showed that, although the tissue underwent macroscopic stretches beyond 1.5 in the circumferential direction, fiber directions remained unchanged during scenario 2 loading. Conversely, fibers strongly realigned along the axis direction for scenario 1 loading. In both cases, the motion of collagen fibers did not satisfy affine deformations, with a significant difference between both cases: affine predictions strongly under-estimated fiber reorientations in uniaxial tension and over-estimated fiber reorientations during inflation at constant length. Finally, we explained this specific kinematics of collagen fibers by the complex tension-compression interactions between very stiff collagen fibers and compliant surrounding proteins. A tensegrity representation of the extracellular matrix in the adventitia taking into account these interactions was proposed to model the motion of collagen fibers during tissue deformation.

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Section: Introductionmentioning

confidence: 99%

Kinematics of collagen fibers in carotid arteries under tension-inflation loading

Krasny

Magoariec

Morin

et al. 2018

Journal of the Mechanical Behavior of Biomedical Materials

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“…Perhaps because of this characteristic, the structure of medial collagen changes at the onset of biaxial loading in porcine arteries, when elastin is engaged, whereas adventitial collagen displays a comparative delay. 5 Another difference between medial and adventitial collagens is in their size and orientation. Medial collagen fibers are smaller and tend to align circumferentially when stretched, whereas the comparatively larger adventitial fibers display more diverse orientation under biaxial strain.…”

Section: See Related Article Pp 890-896mentioning

confidence: 99%

“…Medial collagen fibers are smaller and tend to align circumferentially when stretched, whereas the comparatively larger adventitial fibers display more diverse orientation under biaxial strain. 5 Nevertheless, both medial and adventitial collagen display a realignment under uneven biaxial strain that favors the more heavily loaded orientation. 5 It would be interesting to see how such differences between medial and adventitial collagen evolve in the setting of chronic hypertension.…”

Section: See Related Article Pp 890-896mentioning

confidence: 99%

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Adventures in the Adventitia

Lehoux

2016

Hypertension

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A rterial hypertension, by definition, imparts accrued strain on the vascular wall. This in turn elicits counteracting radial and tangential forces, driving transformations in the vessel wall that aim to accommodate the new conditions and to ultimately restore basal levels of tensile stress. Vascular accumulation of type I, III, and IV collagen in hypertensive patients and in animal models of hypertension effectively counteracts the distending force of blood pressure, but at length it also results in increased vascular stiffness. Clinically, vascular stiffness translates to greater pulse pressure, which is an independent predictor of mortality in patients with end-stage renal failure, hypertension, and diabetes mellitus and in older individuals. 1Conventionally, hypertensive vascular remodeling has been ascribed essentially to smooth muscle cell hypertrophy and amplified collagen synthesis by these cells. However, there is a growing body of knowledge that points to the adventitia as a significant and perhaps even the principal contributor to pathological hypertensive remodeling. In this issue of Hypertension, Bersi et al 2 provide convincing evidence that when it comes to stiffness and stress, we ought to take a closer look at the outer aspect of the arterial wall.Bersi et al 2 found that a 2-or 4-week infusion of angiotensin II (Ang II) in mice, augmenting blood pressure significantly and persistently, resulted in arteries that are both less distensible and less extensible, associated with reduced elastic energy storage. The increased stiffness was attributed essentially to the thickened wall structure. Although smooth muscle hypertrophy and greater deposition of collagen within the lamellae were observed in the aortas of hypertensive mice, the most striking difference between these animals and their normotensive counterparts was in the extent of adventitial fibrillar collagen accumulation. The adventitial collagen was thus considered to bear a greater amount of load under hypertensive conditions compared with normotensive conditions (Figure).These results are reminiscent of and lend strong support to observations made by the same group using a model of carotid artery banding in mice. Both morphological and biaxial mechanical responses were recorded after 6 weeks. In banded arteries, increased pulse pressure and systolic pressure were found to correlate with arterial thickening, adventitial collagen accumulation, as well as decreased axial stretch. 3Moreover, although the media contained a greater fraction of type III collagen, the adventitia contained instead a greater proportion of type I collagen.This latter point is of fundamental importance because there are key differences between medial and adventitial collagen that bear mentioning. For one thing, type III collagen is more extensible than the type I collagen. 4 It forms a relatively elastic network that stores kinetic energy. Perhaps because of this characteristic, the structure of medial collagen changes at the onset of biaxial loading in porcine arteri...

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“…One particularly relevant example is the use of fast Fourier transforms (2D-FFT) to measure fibre misalignment in conventional carbon fibre composites (fibre diameter on the order of 7 µm) [26]. On a smaller scale, 2D-FFT methods have been successfully applied to determine the alignment of electrospun scaffolds [27] and analyse elastin networks [28]. Using these examples as inspiration, a method was developed to measure the orientation of CNT veils, via image processing of electron micrographs via 2D-FFT.…”

Section: Accepted Manuscriptmentioning

confidence: 99%

Mapping carbon nanotube orientation by fast fourier transform of scanning electron micrographs

Brandley

Greenhalgh

Shaffer

et al. 2018

Carbon

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Please cite this article as: E. Brandley, E.S. Greenhalgh, M.S.P. Shaffer, Q. Li, Mapping carbon nanotube orientation by fast fourier transform of scanning electron micrographs, Carbon (2018), doi: 10.1016/j.carbon.2018.04.063. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AbstractA novel method of applying a two-dimensional Fourier transform (2D-FFT) to SEM was developed to map the CNT orientation in pre-formed arrays. Local 2D-FFTs were integrated azimuthally to determine an orientation distribution function and the associated Herman parameter. This approach provides data rapidly and over a wide range of lengthscales.Although likely to be applicable to a wide range of anisotropic nanoscale structures, the method was specifically developed to study CNT veils, a system in which orientation critically controls mechanical properties. Using this system as a model, key parameters for the 2D-FFT analysis were optimised, including magnification and domain size; a model set of CNT veils were pre-strained to 5%, 10% and 15%, to vary the alignment degree. The algorithm confirmed a narrower orientation distribution function and increasing Herman parameter, with increasing pre-strain.To validate the algorithm, the local orientation was compared to that derived from a common polarised Raman spectroscopy. Orientation maps of the Herman parameter, derived by both methods, showed good agreement. Quantitatively, the mean Herman parameter calculated using the polarised Raman spectroscopy was 0.42±0.004 compared to 0.32±0.002 for the 2D-FFT method, with a correlation coefficient of 0.73. Possible reasons for the modest and systematic discrepancy were discussed.

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Arterial Extracellular Matrix: A Mechanobiological Study of the Contributions and Interactions of Elastin and Collagen

Cited by 173 publications

References 55 publications

Kinematics of collagen fibers in carotid arteries under tension-inflation loading

Kinematics of collagen fibers in carotid arteries under tension-inflation loading

Adventures in the Adventitia

Mapping carbon nanotube orientation by fast fourier transform of scanning electron micrographs

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