Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles.

doi:10.1016/J.JBIOMECH.2010.10.044

Home
/
Papers
/
Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles.

Journal Article•DOI•

Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles.

Gretchen A. Meyer¹, Richard L. Lieber¹•Institutions (1)

University of California, San Diego¹

24 Feb 2011-Journal of Biomechanics (Elsevier)-Vol. 44, Iss: 4, pp 771-773

TL;DR: A new method to quantify viscoelastic ECM modulus is presented by combining tests of single muscle fibers and fiber bundles, which demonstrate that ECM is a highly nonlinearly elastic material, while muscle fibers are linearly elastic.

read less

About: This article is published in Journal of Biomechanics.The article was published on 2011-02-24 and is currently open access. It has received 156 citations till now. The article focuses on the topics: Skeletal muscle.

...read moreread less

Citations

PDF

Open Access

More filters

Journal Article•DOI•

Skeletal muscle fibrosis is associated with decreased muscle inflammation and weakness in patients with chronic kidney disease.

[...]

Matthew K. Abramowitz¹, William Paredes¹, Kehao Zhang¹, Camille R. Brightwell², Julia N. Newsom², Hyok Joon Kwon³, Matthew Custodio¹, Rupinder S. Buttar¹, Hina Farooq¹, Bushra Zaidi¹, Rima Pai¹, Jeffrey E. Pessin¹, Meredith Hawkins¹, Christopher S. Fry² - Show less +10 more•Institutions (3)

Albert Einstein College of Medicine¹, University of Texas Medical Branch², Rutgers University³

01 Dec 2018-American Journal of Physiology-renal Physiology

TL;DR: Skeletal muscle collagen content is increased in humans with CKD and is associated with functional parameters, and Muscle fibrosis correlated with increased FAP abundance, which may be due to insufficient macrophage-mediated TNF-α secretion.

...read moreread less

Abstract: Muscle dysfunction is an important cause of morbidity among patients with chronic kidney disease (CKD). Although muscle fibrosis is present in a CKD rodent model, its existence in humans and its im...

...read moreread less

31 citations

Book Chapter•DOI•

Exercise and Regulation of Bone and Collagen Tissue Biology.

[...]

Michael Kjaer¹, Niklas Rye Jørgensen², Katja M. Heinemeier³, S. Peter Magnusson¹•Institutions (3)

University of Copenhagen¹, University of Southern Denmark², Bispebjerg Hospital³

01 Jan 2015-Progress in Molecular Biology and Translational Science

TL;DR: The importance of regular mechanical load in order to preserve the stabilizing role of the connective tissue for the overall function of the musculoskeletal system in both daily activity and exercise is illustrated.

...read moreread less

Abstract: The musculoskeletal system and its connective tissue include the intramuscular connective tissue, the myotendinous junction, the tendon, the joints with their cartilage and ligaments, and the bone; they all together play a crucial role in maintaining the architecture of the skeletal muscle, ensuring force transmission, storing energy, protecting joint surface and stability, and ensuring the transfer of muscular forces into resulting limb movement. The musculoskeletal connective tissue structure is relatively stable, but mechanical loading and subsequent mechanotransduction and molecular anabolic signaling can result in some adaptation of the connective tissue, its size, its strength, and its mechanical properties, whereby it can improve its capacity by 5-20% with regular physical activity. For several of the mechanically loaded connective tissues, only limited information regarding molecular and cellular signaling pathways and their adaptation to exercise is available. In contrast to tissue responses with exercise, lack of mechanical tissue loading through inactivity or immobilization of the human body will result in a dramatic loss of connective tissue content, structure, and tolerable load within weeks, to a degree (30-40%) that mimics that of contractile skeletal musculature. This illustrates the importance of regular mechanical load in order to preserve the stabilizing role of the connective tissue for the overall function of the musculoskeletal system in both daily activity and exercise.

...read moreread less

31 citations

Journal Article•DOI•

Diverse and complex muscle spindle afferent firing properties emerge from multiscale muscle mechanics

[...]

Kyle P. Blum¹, Kyle P. Blum², Kenneth S. Campbell³, Brian C. Horslen², Paul Nardelli², Stephen N. Housley², Timothy C. Cope², Lena H. Ting², Lena H. Ting⁴ - Show less +5 more•Institutions (4)

Northwestern University¹, Georgia Institute of Technology², University of Kentucky³, Emory University⁴

28 Dec 2020-eLife

TL;DR: Depending on the neuromechanical conditions, the muscle spindle model output appears to ‘encode’ aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.

...read moreread less

Abstract: Despite decades of research, we lack a mechanistic framework capable of predicting how movement-related signals are transformed into the diversity of muscle spindle afferent firing patterns observed experimentally, particularly in naturalistic behaviors. Here, a biophysical model demonstrates that well-known firing characteristics of mammalian muscle spindle Ia afferents - including movement history dependence, and nonlinear scaling with muscle stretch velocity - emerge from first principles of muscle contractile mechanics. Further, mechanical interactions of the muscle spindle with muscle-tendon dynamics reveal how motor commands to the muscle (alpha drive) versus muscle spindle (gamma drive) can cause highly variable and complex activity during active muscle contraction and muscle stretch that defy simple explanation. Depending on the neuromechanical conditions, the muscle spindle model output appears to 'encode' aspects of muscle force, yank, length, stiffness, velocity, and/or acceleration, providing an extendable, multiscale, biophysical framework for understanding and predicting proprioceptive sensory signals in health and disease.

...read moreread less

31 citations

Journal Article•DOI•

A homogenization model of the Voigt type for skeletal muscle.

[...]

L. A. Spyrou, M. Agoras¹, Kostas Danas²•Institutions (2)

University of Thessaly¹, Université Paris-Saclay²

07 Feb 2017-Journal of Theoretical Biology

TL;DR: A three-dimensional constitutive model for skeletal muscle incorporating microstructural characteristics is developed and numerically implemented in a general purpose finite element program and found to be in very good agreement with both the experimental data and the finite element results.

...read moreread less

30 citations

Cites background from "Elucidation of extracellular matrix..."

...…z-axis. following properties: • the unit cell is periodic, i.e, it is representative and ergodic in the sense of the strict mathematical terminology of homogenization and describes completely the homogenized material response by using appropriate periodic boundary conditions (Michel et al., 1999)....
[...]
...(29), 1For a detailed proof of the fact that the applied ̂F corresponds to the volume average of F in the unit cell the reader is referred to Michel et al. (1999) and Javili et al. (2013)....
[...]

Journal Article•DOI•

Multiscale modeling of skeletal muscle tissues based on analytical and numerical homogenization.

[...]

L. A. Spyrou, Sébastien Brisard¹, Kostas Danas²•Institutions (2)

University of Paris¹, Université Paris-Saclay²

01 Apr 2019-Journal of The Mechanical Behavior of Biomedical Materials

TL;DR: A novel multiscale modeling framework for skeletal muscles based on analytical and numerical homogenization methods is presented to study the mechanical muscle response at finite strains under three-dimensional loading conditions.

...read moreread less

Abstract: A novel multiscale modeling framework for skeletal muscles based on analytical and numerical homogeniza-tion methods is presented to study the mechanical muscle response at finite strains under three-dimensional loading conditions. First an analytical microstructure-based constitutive model is developed and numerically implemented in a general purpose finite element program. The analytical model takes into account explicitly the volume fractions, the material properties, and the spatial distribution of muscle's constituents by using homogenization techniques to bridge the different length scales of the muscle structure. Next, a numerical homogenization model is developed using periodic eroded Voronoi tessellation to virtually represent skeletal muscle microstructures. The eroded Voronoi unit cells are then resolved by finite element simulations and are used to assess the analytical homogenization model. The material parameters of the analytical model are identified successfully by use of available experimental data. The analytical model is found to be in very good agreement with the numerical model for the full range of loadings, and a wide range of different volume fractions and heterogeneity contrasts between muscle's constituents. A qualitative application of the model on fusiform and pennate muscle structures shows its efficiency to examine the effect of muscle fiber concentration variations in an organ-scale model simulation.

...read moreread less

30 citations

Cites background or result from "Elucidation of extracellular matrix..."

...In addition, our findings probe successfully the experimental results of Meyer and Lieber [37], who revealed the primary contribution of ECM on muscle’s stiffness and highly nonlinear response under tensile loading in the muscle fiber direction....
[...]
...(23) is set to c = 95% according to Lieber et al. [28] data for normal muscles....
[...]
...Recent experimental data have shown a linear stress-strain passive behavior of single muscle fibers [37, 50],...
[...]

1
2
3
…
4
5
6
7
8
9
10
…
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32

Collapse

References

PDF

Open Access

More filters

Journal Article•DOI•

Matrix elasticity directs stem cell lineage specification.

[...]

Adam J. Engler¹, Shamik Sen¹, H. Lee Sweeney¹, Dennis E. Discher•Institutions (1)

University of Pennsylvania¹

25 Aug 2006-Cell

TL;DR: Naive mesenchymal stem cells are shown here to specify lineage and commit to phenotypes with extreme sensitivity to tissue-level elasticity, consistent with the elasticity-insensitive commitment of differentiated cell types.

...read moreread less

12,204 citations

"Elucidation of extracellular matrix..." refers background in this paper

...Since substrate biomechanical properties have been shown to be critical in the biology of tissue development and remodeling (Engler et al., 2006; Gilbert et al., 2010), it is likely that mechanics are critical for ECM to perform its function....
[...]

Journal Article•DOI•

Substrate Elasticity Regulates Skeletal Muscle Stem Cell Self-Renewal in Culture

[...]

Penney M. Gilbert¹, Karen Havenstrite¹, Klas E. G. Magnusson¹, Klas E. G. Magnusson², Alessandra Sacco¹, Nora Leonardi³, Nora Leonardi¹, Peggy E. Kraft¹, N. K. Nguyen¹, Sebastian Thrun¹, Matthias P. Lutolf³, Helen M. Blau¹ - Show less +8 more•Institutions (3)

Stanford University¹, Royal Institute of Technology², École Polytechnique Fédérale de Lausanne³

27 Aug 2010-Science

TL;DR: Using a bioengineered substrate to recapitulate key biophysical and biochemical niche features in conjunction with a highly automated single-cell tracking algorithm, it is shown that substrate elasticity is a potent regulator of MuSC fate in culture.

...read moreread less

Abstract: Stem cells that naturally reside in adult tissues, such as muscle stem cells (MuSCs), exhibit robust regenerative capacity in vivo that is rapidly lost in culture. Using a bioengineered substrate to recapitulate key biophysical and biochemical niche features in conjunction with a highly automated single-cell tracking algorithm, we show that substrate elasticity is a potent regulator of MuSC fate in culture. Unlike MuSCs on rigid plastic dishes (approximately 10(6) kilopascals), MuSCs cultured on soft hydrogel substrates that mimic the elasticity of muscle (12 kilopascals) self-renew in vitro and contribute extensively to muscle regeneration when subsequently transplanted into mice and assayed histologically and quantitatively by noninvasive bioluminescence imaging. Our studies provide novel evidence that by recapitulating physiological tissue rigidity, propagation of adult muscle stem cells is possible, enabling future cell-based therapies for muscle-wasting diseases.

...read moreread less

1,428 citations

"Elucidation of extracellular matrix..." refers background in this paper

...Since substrate biomechanical properties have been shown to be critical in the biology of tissue development and remodeling (Engler et al., 2006; Gilbert et al., 2010), it is likely that mechanics are critical for ECM to perform its function....
[...]

Journal Article•DOI•

Matrix elasticity directs stem cell lineage — Soluble factors that limit osteogenesis

[...]

D.E. Discher¹•Institutions (1)

University of Pennsylvania¹

01 Jun 2009-Bone

1,224 citations

"Elucidation of extracellular matrix..." refers background in this paper

...Since substrate biomechanical properties have been shown to be critical in the biology of tissue development and remodeling (Engler et al., 2006; Gilbert et al., 2010), it is likely that mechanics are critical for ECM to perform its function....
[...]

Journal Article•DOI•

Cell surface receptors for extracellular matrix molecules

[...]

Clayton A. Buck¹, Alan F. Horwitz•Institutions (1)

Wistar Institute¹

01 Jan 1987-Annual Review of Cell Biology

TL;DR: Avian integrin shows little specificity and appears to behave as a multifunctional, promiscuous receptor for extracellular matrix molecules, and post-translational modifications provide yet another mechanism for regulating integrin-ligand binding.

...read moreread less

Abstract: Table 2 lists most of the extracellular matrix and related receptors identified to date. The wide range of binding affinities of these receptors for their ligands may be important to their function. The affinity of integrins for fibronectin is moderate, with a dissociation constant in the micromolar range. This affinity level leads to relatively rapid dissociation and reformation of receptor-ligand complexes. Thus changes in component concentration can shift binding equilibria within minutes (the time scale of many biologic phenomena) and change the number or organization of adhesive complexes. This type of interaction would be useful in motile cells, in which adhesions must form and dissociate rapidly. In contrast, the affinity of the 68-kDa laminin receptor for its ligand is three orders of magnitude higher. Such levels of affinity would be useful in stabilizing tissue. Members of the integrin family appear to recognize an RGD sequence on the ligands to which they bind. Since there are many ligands containing the RGD sequence, the question of specificity arises. Avian integrin shows little specificity and appears to behave as a multifunctional, promiscuous receptor for extracellular matrix molecules. Figure 1 summarizes our current view of the structural and functional features of avian integrin. In contrast, the mammalian receptors for vitronectin and fibronectin are specific for their respective ligands. More than one of these receptors may be present simultaneously on a cell surface, e.g. fibroblasts express receptors for fibronectin, laminin, and vitronectin at the same time. This multiplicity of receptors provides potential mechanisms for generating the adhesive differences among cells believed to play a prominent role in morphogenesis. Further adhesive differences may stem from the formation of different combinations of various alpha- and beta-subunits expressed in the cell. The mechanism of regulation of adhesive interactions with the extracellular matrix is only beginning to be explored. There are several levels at which this regulation might occur. Integrin appears to be more regionalized in more developed cells that are integral parts of tissue structures. Changes in receptor distribution could alter the relative strength of adhesive interactions. In certain instances, avian integrin disappears, or its concentration is reduced, e.g. during the development of embryonic lung (Chen et al 1986) and erythroid cells (Patel & Lodish 1985). Post-translational modifications provide yet another mechanism for regulating integrin-ligand binding.(ABSTRACT TRUNCATED AT 400 WORDS)

...read moreread less

784 citations

"Elucidation of extracellular matrix..." refers background in this paper

...Extracellular matrix (ECM) is essential for the development, maintenance and regeneration of skeletal muscle (Buck and Horwitz, 1987; Purslow, 2002)....
[...]
...The importance of the extracellular matrix (ECM) in muscle is widely recognized, since ECM plays a central role in proper muscle development (Buck and Horwitz, 1987), tissue structural support (Purslow, 2002), and transmission ofmechanical signals between fibers and tendon (Huijing, 1999)....
[...]
...…r a c t The importance of the extracellular matrix (ECM) in muscle is widely recognized, since ECM plays a central role in proper muscle development (Buck and Horwitz, 1987), tissue structural support (Purslow, 2002), and transmission ofmechanical signals between fibers and tendon (Huijing, 1999)....
[...]

Journal Article•DOI•

Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments.

[...]

Henk Granzier¹, Thomas C. Irving¹•Institutions (1)

Washington State University¹

01 Mar 1995-Biophysical Journal

TL;DR: The passive tension-sarcomere length relation of rat cardiac muscle was investigated by studying passive (or not activated) single myocytes and trabeculae and the contribution of collagen, titin, microtubules, and intermediate filaments to tension and stiffness was investigated.

...read moreread less

587 citations

"Elucidation of extracellular matrix..." refers methods in this paper

...Previous studies used methods of subtraction, where the ECM was ‘‘preferentially’’ digested from muscle and its properties inferred from subtracting the digested state from the undigested state (see review by Fomovsky et al., 2010; Granzier and Irving, 1995)....
[...]