Cyclic stretch induces decorin expression via yes-associated protein in tenocytes: A possible mechanism for hyperplasia in masticatory muscle tendon-aponeurosis hyperplasia

Hayashi, Naoki; Sato, Tsuyoshi; Yumoto, M; Kokabu, Shoichiro; Fukushima, Yukio; Kawata, Yumiko; Kajihara, Takeshi; Mizuno, Yumi; Mizuno, Yosuke; Kawakami, Tetsuji; Kirita, Tadaaki; Hayata, Tadayoshi; Noda, Masaki; Yoda, Tetsuya

doi:10.1016/j.ajoms.2018.12.012

Cited by 9 publications

(7 citation statements)

References 29 publications

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“…However, we previously found that calcification was detected in the temporal tendon in MMTAH (3). Our previous study using proteome analysis revealed that beta-crystallin A4, which is increased by tensile force in tenocytes, is up-regulated in patients with MMTAH when compared to patients with facial deformity (FD) (4). Moreover, we showed that tendons in patients with MMTAH abundantly express decorin protein, which was induced by cyclic stretch via yes-associated protein signaling (5).…”

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confidence: 90%

Analysis of Masticatory Muscle Tendon-aponeurosis Hyperplasia by Using Next-generation Sequencing

Yumoto

Mizuno

Isozaki

et al. 2022

In Vivo

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Background/Aim: Masticatory muscle tendonaponeurosis hyperplasia (MMTAH) is a disease associated with a mouth opening limitation. Here, we conducted a bioinformatics analysis to examine gene expression patterns in patients with MMTAH in comparison to those with facial deformity (FD). Materials and Methods: Seven MMTAH patients and three FD patients were recruited. We conducted RNA sequencing analysis, quantitative reverse transcription polymerase chain reaction and immunoblot analysis. Results: Of the identified 19,767 mapped read tags that showed clear differential expression, 2,471 genes were significantly up-regulated and 2,849 genes were significantly down-regulated in patients with MMTAH compared to those in patients with FD. Among the up-regulated genes, ten genes were significantly increased. The distribution of upregulated and down-regulated genes at different ages tended to be similar. Moreover, the protein levels of Ankyrin Repeat Domain 2, Troponin T1 and myosin heavy chain 7, which are associated with slow twitch fibers and mechanical loading, were strongly expressed in patients with MMTAH compared to those in patients with FD. Conclusion: The gene expression pattern in MMTAH patients was similar regardless of age. As the transition of fast-to-slow twitch in the skeletal muscle is induced by mechanical loading, and up-regulation of slow twitch molecules was observed in MMTAH patients, mechanical loading is suggested to be implicated in MMTAH.

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confidence: 90%

Analysis of Masticatory Muscle Tendon-aponeurosis Hyperplasia by Using Next-generation Sequencing

Yumoto

Mizuno

Isozaki

et al. 2022

In Vivo

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“…Furthermore, their relative expression decreases during development precisely when fibril lengths/diameters grow rapidly (Birk et al, 1995;Chen and Birk, 2013). However, previous work indicates that decorin expression is positively correlated to mechanical stimulation (Hayashi et al, 2019). This suggests that the reduction in the fibril:tissue strain ratio (potentially due to a retardation in collagen fibril elongation) seen with flaccid paralysis (Figure 7A) may not be due to a change in decorin or biglycan expression.…”

Section: Discussionmentioning

confidence: 87%

Mechanical Stimulation via Muscle Activity Is Necessary for the Maturation of Tendon Multiscale Mechanics During Embryonic Development

Peterson

Rolfe

Kunselman

et al. 2021

Front. Cell Dev. Biol.

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During embryonic development, tendons transform into a hypocellular tissue with robust tensile load-bearing capabilities. Previous work suggests that this mechanical transformation is due to increases in collagen fibril length and is dependent on mechanical stimulation via muscle activity. However, the relationship between changes in the microscale tissue structure and changes in macroscale tendon mechanics is still unclear. Additionally, the specific effect of mechanical stimulation on the multiscale structure-function relationships of developing tendons is also unknown. Therefore, the objective of this study was to measure the changes in tendon mechanics and structure at multiple length scales during embryonic development with and without skeletal muscle paralysis. Tensile testing of tendons from chick embryos was performed to determine the macroscale tensile modulus as well as the magnitude of the fibril strains and interfibrillar sliding with applied tissue strain. Embryos were also treated with either decamethonium bromide or pancuronium bromide to produce rigid or flaccid paralysis. Histology was performed to assess changes in tendon size, spacing between tendon subunits, and collagen fiber diameter. We found that the increase in the macroscale modulus observed with development is accompanied by an increase in the fibril:tissue strain ratio, which is consistent with an increase in collagen fibril length. Additionally, we found that flaccid paralysis reduced the macroscale tendon modulus and the fibril:tissue strain ratio, whereas less pronounced effects that were not statistically significant were observed with rigid paralysis. Finally, skeletal paralysis also reduced the size of collagen fibril bundles (i.e., fibers). Together, these data suggest that more of the applied tissue strain is transmitted to the collagen fibrils at later embryonic ages, which leads to an increase in the tendon macroscale tensile mechanics. Furthermore, our data suggest that mechanical stimulation during development is necessary to induce structural and mechanical changes at multiple physical length scales. This information provides valuable insight into the multiscale structure-function relationships of developing tendons and the importance of mechanical stimulation in producing a robust tensile load-bearing soft tissue.

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“…To the best of our knowledge, our study is the first to compare the gene expression profiles of the Achilles tendon and tendons of the masticatory muscles in the Japanese macaque using next-generation sequencing. Our previous study showed that cyclic tensile strain induces decorin expression via yes-associated protein in cultured tenocytes and tendons of patients with MMTAH, suggesting that in MMTAH, tendons are subjected to cyclic tensile strain [ 24 ]. Since DEGs in the tendon of masticatory muscles under tensile strain were enriched for the GO term division, it can be speculated that tensile strain promotes cell proliferation in these tendons.…”

Section: Discussionmentioning

confidence: 99%

“…tendons are subjected to cyclic tensile strain [24]. Since DEGs in the tendon of masticatory muscles under tensile strain were enriched for the GO term division, it can be speculated that tensile strain promotes cell proliferation in these tendons.…”

Section: Plos Onementioning

confidence: 99%

Gene expression profiling of the masticatory muscle tendons and Achilles tendons under tensile strain in the Japanese macaque Macaca fuscata

Ito

Tatsumoto

et al. 2023

PLoS ONE

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Both Achilles and masticatory muscle tendons are large load-bearing structures, and excessive mechanical loading leads to hypertrophic changes in these tendons. In the maxillofacial region, hyperplasia of the masticatory muscle tendons and aponeurosis affect muscle extensibility resulting in limited mouth opening. Although gene expression profiles of Achilles and patellar tendons under mechanical strain are well investigated in rodents, the gene expression profile of the masticatory muscle tendons remains unexplored. Herein, we examined the gene expression pattern of masticatory muscle tendons and compared it with that of Achilles tendons under tensile strain conditions in the Japanese macaque Macaca fuscata. Primary tenocytes isolated from the masticatory muscle tendons (temporal tendon and masseter aponeurosis) and Achilles tendons were mechanically loaded using the tensile force and gene expression was analyzed using the next-generation sequencing. In tendons exposed to tensile strain, we identified 1076 differentially expressed genes with a false discovery rate (FDR) < 10−10. To identify genes that are differentially expressed in temporal tendon and masseter aponeurosis, an FDR of < 10−10 was used, whereas the FDR for Achilles tendons was set at > 0.05. Results showed that 147 genes are differentially expressed between temporal tendons and masseter aponeurosis, out of which, 125 human orthologs were identified using the Ensemble database. Eight of these orthologs were related to tendons and among them the expression of the glycoprotein nmb and sphingosine kinase 1 was increased in temporal tendons and masseter aponeurosis following exposure to tensile strain. Moreover, the expression of tubulin beta 3 class III, which promotes cell cycle progression, and septin 9, which promotes cytoskeletal rearrangements, were decreased in stretched Achilles tendon cells and their expression was increased in stretched masseter aponeurosis and temporal tendon cells. In conclusion, cyclic strain differentially affects gene expression in Achilles tendons and tendons of the masticatory muscles.

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Cyclic stretch induces decorin expression via yes-associated protein in tenocytes: A possible mechanism for hyperplasia in masticatory muscle tendon-aponeurosis hyperplasia

Cited by 9 publications

References 29 publications

Analysis of Masticatory Muscle Tendon-aponeurosis Hyperplasia by Using Next-generation Sequencing

Analysis of Masticatory Muscle Tendon-aponeurosis Hyperplasia by Using Next-generation Sequencing

Mechanical Stimulation via Muscle Activity Is Necessary for the Maturation of Tendon Multiscale Mechanics During Embryonic Development

Gene expression profiling of the masticatory muscle tendons and Achilles tendons under tensile strain in the Japanese macaque Macaca fuscata

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