Biomechanical Origins of Muscle Stem Cell Signal Transduction

Morrissey, James B.; Cheng, Richard; Davoudi, Sadegh; Gilbert, Penney M.

doi:10.1016/j.jmb.2015.05.004

Cited by 23 publications

(16 citation statements)

References 199 publications

(208 reference statements)

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“…The relationship between scaffold modulus and VML repair outcome has not been investigated, but in‐vitro studies have shown that muscle progenitor cells sense and respond to substrate stiffness. Muscle progenitor cell myogenesis is significantly enhanced when the cells are grown on soft substrates like ECM and reduced on stiff substrates like tissue culture plastic . Similar cell‐substrate stiffness interactions have been noted for other cell types including cardiomyocytes .…”

Section: Discussionsupporting

confidence: 52%

Development of an infusion bioreactor for the accelerated preparation of decellularized skeletal muscle scaffolds

Kasukonis

Kim

Washington

et al. 2016

Biotechnology Progress

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The implantation of decellularized tissue has shown effectiveness as a strategy for the treatment of volumetric muscle loss (VML) injuries. The preparation of decellularized tissue typically relies on the diffusion driven removal of cellular debris. For bulky tissues like muscle, the process can be lengthy, which introduces opportunities for both tissue contamination and degradation of key ECM molecules. In this study we report on the accelerated preparation of decellularized skeletal muscle (DSM) scaffolds using a infusion system and examine scaffold performance for the repair of VML injuries. The preparation of DSM scaffolds using infusion was dramatically accelerated. As the infusion rate (1% SDS) was increased from 0.1 to 1 and 10ml/hr, the time needed to remove intracellular myoglobin and actin decreased from a maximum of 140±3hrs to 45±3hrs and 10±2hrs respectively. Although infusion appeared to remove cellular debris more aggressively, it did not significantly decrease the collagen or glycosaminoglycan composition of DSM samples when compared to un-infused controls. Infusion prepared DSM samples retained the aligned network structure and mechanical integrity of control samples. Infusion prepared DSM samples supported the attachment and in-vitro proliferation of myoblast cells and was well tolerated by the host when examined in-vivo.

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Section: Discussionsupporting

confidence: 52%

Development of an infusion bioreactor for the accelerated preparation of decellularized skeletal muscle scaffolds

Kasukonis

Kim

Washington

et al. 2016

Biotechnology Progress

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“…In particular, for mesenchymal stem cells matrix stiffness can influence differentiation, biasing cells on a physiologically soft substrate (E ≲ 1000 Pa) toward adipogenesis and those on a physiologically stiff substrate (E ≳ 25000 Pa) toward osteogenesis [3]. Substrate stiffness is also found to play a role in enhancing the proliferation and self-renewal of muscle satellite cells [4,5] and in neural stem cell differentiation [6]. More broadly, additional substrate properties, including topography and extracellular matrix protein spacing, have also been found to influence cellular morphology, organization, and fate specification in a variety of self-renewing populations including mesenchymal stem cells [7,8], pluripotent cells [9,10], and epidermal tissues [11].…”

Section: Introductionmentioning

confidence: 99%

A semi-interpenetrating network of polyacrylamide and recombinant basement membrane allows pluripotent cell culture in a soft, ligand-rich microenvironment

Price

Huang

Sebastiano³

et al. 2017

Biomaterials

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The physical properties of the extracellular matrix play an essential role in guiding stem cell differentiation and tissue morphogenesis both in vivo and in vitro. Existing work to investigate the role of matrix mechanics in directing stem cell proliferation, self-renewal, and differentiation has been limited by the poor attachment and survival of human pluripotent cells cultured on soft matrices (Young's modulus E ≲ 1000 Pa). To address this limitation we developed a protocol for generating semi-interpenetrating networks of polyacrylamide and recombinant basement membrane. Using these materials, we found that human embryonic stem cells (hESCs) remained proliferative and pluripotent even when grown in small colonies and on surfaces ranging in stiffness from 150 to 12000 Pa, spanning the range of tissue stiffnesses likely to be encountered in the embryo. Considerable recent attention has focused on the role of the transcriptional coactivator and Hippo effector YAP in regulating differentiation and cell proliferation both in the early embryo and in vitro. We found that while YAP localized to the nucleus on substrates of E ≳ 1000 Pa, its localization was heterogeneous on substrates of moduli ≲ 450 Pa, with predominantly nuclear localization at the colony periphery and mixed cytoplasmic and nuclear localization for cells in the colony interior, a pattern reminiscent of YAP subcellular localization in the inner cell mass (ICM) of the early embryo. In addition, hESC colony dynamics were highly responsive to substrate stiffness, with cells assembling into monolayers, multilayer structures, and transient, hollow rosettes in response to decreasing substrate stiffnesses in the range of 12000 to 150 Pa. We suggest that soft, ligand-rich substrates such as are described here provide a promising means of recapitulating aspects of early mammalian development that are otherwise inaccessible, and more broadly may be useful in the derivation of complex tissues from pluripotent cells in an in vitro setting.

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“…The importance of accurately matching scaffold modulus values to native muscle tissue during VML repair has not been investigated, but in-vitro studies have shown that muscle progenitor cells sense and respond to substrate stiffness. Muscle progenitor cell myogenesis is significantly enhanced when grown on soft substrate and reduced on stiff substrates [59, 60]. Similar cell-substrate stiffness interactions have been noted for other cells including cardiomyocytes [61].…”

Section: Discussionmentioning

confidence: 93%

The characterization of decellularized human skeletal muscle as a blueprint for mimetic scaffolds

Wilson

Terlouw

Roberts

et al. 2016

J Mater Sci: Mater Med

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The use of decellularized skeletal muscle (DSM) as a cell substrate and scaffold for the repair of volumetric muscle loss injuries has shown therapeutic promise. The performance of DSM materials motivated our interest in exploring the chemical and physical properties of this promising material. We suggest that these properties could serve as a blueprint for the development of next generation engineered materials with DSM mimetic properties. In this study, whole human lower limb rectus femoris (n=10) and upper limb supraspinatus muscle samples (n=10) were collected from both male and female tissue donors. Skeletal muscle samples were decellularized and nine property values, capturing key compositional, architectural, and mechanical properties, were measured and statistically analyzed. Mean values for each property were determined across muscle types and genders. Additionally, the influence of muscle type (upper versus lower limb) and donor gender (male versus female) on each of the DSM material properties was examined. The data suggests that DSM materials prepared from lower limb rectus femoris samples have an increased modulus and contain a higher collagen content then upper limb supraspinatus muscles. Specifically, lower limb rectus femoris DSM material modulus and collagen content was approximately twice that of lower limb supraspinatus DSM samples. While muscle type did show some influence on material properties, we did not find significant trends related to gender. The material properties reported herein may be used as a blueprint for the data-driven design of next generation engineered scaffolds with muscle mimetic properties, as well as inputs for computational and physical models of skeletal muscle.

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Biomechanical Origins of Muscle Stem Cell Signal Transduction

Cited by 23 publications

References 199 publications

Development of an infusion bioreactor for the accelerated preparation of decellularized skeletal muscle scaffolds

Development of an infusion bioreactor for the accelerated preparation of decellularized skeletal muscle scaffolds

A semi-interpenetrating network of polyacrylamide and recombinant basement membrane allows pluripotent cell culture in a soft, ligand-rich microenvironment

The characterization of decellularized human skeletal muscle as a blueprint for mimetic scaffolds

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