Skip to main content
Top
Published in: Anatomical Science International 1/2024

21-11-2023 | Original Article

Regeneration process of myotendinous junction injury induced by collagenase injection between Achilles tendon and soleus muscle in mice

Authors: Yutaro Yamamoto, Masahito Yamamoto, Hidetomo Hirouchi, Shuichiro Taniguchi, Genji Watanabe, Satoru Matsunaga, Shinichi Abe

Published in: Anatomical Science International | Issue 1/2024

Login to get access

Abstract

Recently, it has become clear that peri-muscular tissues play a significant role in the deterioration of muscle function. Understanding the function and regeneration of muscle, as well as its surrounding tissues, is crucial to determining the causes of muscular illnesses. However, the regeneration process of the myotendinous junction (MTJ), the most closely related peri-muscular tissue, is still unknown. Therefore, we generated a mouse model of MTJ injury by collagenase injection and searched for the process of regeneration of the MTJ and its adjacent regions. The MTJ region was damaged by collagenase injection, which greatly increased the tendon cross sectional area. Collagenase injections increased the proportion of myofibers with a central nucleus, which is a characteristic of regenerating muscle. The collagenase injection group had myofibers with central nuclei and expressing MTJ markers. Additionally, we measured the length of MTJs using serial cross sections of the soleus muscle and discovered that MTJs at 2 weeks after collagenase injection were shorter compared to the control group, with a propensity to progressively recover their length over time. The results showed that MTJs undergo morphological regeneration even when severely damaged, and that this regeneration occurs in conjunction with muscle regeneration. We anticipate that these findings will be valuable in upcoming research on motor unit regeneration.
Literature
go back to reference Argilés JM, Campos N, Lopez-Pedrosa JM et al (2016) Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc 17:789–796CrossRefPubMed Argilés JM, Campos N, Lopez-Pedrosa JM et al (2016) Skeletal muscle regulates metabolism via interorgan crosstalk: roles in health and disease. J Am Med Dir Assoc 17:789–796CrossRefPubMed
go back to reference Biltz NK, Collins KH, Shen KC et al (2020) Infiltration of intramuscular adipose tissue impairs skeletal muscle contraction. J Physiol 598:2669–2683CrossRefPubMed Biltz NK, Collins KH, Shen KC et al (2020) Infiltration of intramuscular adipose tissue impairs skeletal muscle contraction. J Physiol 598:2669–2683CrossRefPubMed
go back to reference Charvet B, Ruggiero F, Le Guellec DL (2012) The development of the myotendinous junction. A review. Muscles Ligaments Tendons J 2:53–63PubMedPubMedCentral Charvet B, Ruggiero F, Le Guellec DL (2012) The development of the myotendinous junction. A review. Muscles Ligaments Tendons J 2:53–63PubMedPubMedCentral
go back to reference Curzi D, Lattanzi D, Ciuffoli S et al (2013) Growth hormone plus resistance exercise attenuate structural changes in rat myotendinous junctions resulting from chronic unloading. Eur J Histochem 57:e37CrossRefPubMedPubMedCentral Curzi D, Lattanzi D, Ciuffoli S et al (2013) Growth hormone plus resistance exercise attenuate structural changes in rat myotendinous junctions resulting from chronic unloading. Eur J Histochem 57:e37CrossRefPubMedPubMedCentral
go back to reference Esteves de Lima J, Blavet C, Bonnin MA et al (2021) Unexpected contribution of fibroblasts to muscle lineage as a mechanism for limb muscle patterning. Nat Commun 12:3851CrossRefPubMedPubMedCentral Esteves de Lima J, Blavet C, Bonnin MA et al (2021) Unexpected contribution of fibroblasts to muscle lineage as a mechanism for limb muscle patterning. Nat Commun 12:3851CrossRefPubMedPubMedCentral
go back to reference Fry CS, Lee JD, Mula J et al (2015) Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 21:76–80CrossRefPubMed Fry CS, Lee JD, Mula J et al (2015) Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 21:76–80CrossRefPubMed
go back to reference Guardiola O, Andolfi G, Tirone M et al (2017) Induction of acute skeletal muscle regeneration by cardiotoxin injection. J vis Exp 119:54515 Guardiola O, Andolfi G, Tirone M et al (2017) Induction of acute skeletal muscle regeneration by cardiotoxin injection. J vis Exp 119:54515
go back to reference Jacobson KR, Sarah L, Acuna A et al (2020) Comparative analysis of the extracellular matrix proteome across the myotendinous junction. J Proteome Res 19(10):3955–3967CrossRefPubMedPubMedCentral Jacobson KR, Sarah L, Acuna A et al (2020) Comparative analysis of the extracellular matrix proteome across the myotendinous junction. J Proteome Res 19(10):3955–3967CrossRefPubMedPubMedCentral
go back to reference Järvinen TA, Józsa L, Kannus P et al (2002) Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles. An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil 23:245–254CrossRefPubMed Järvinen TA, Józsa L, Kannus P et al (2002) Organization and distribution of intramuscular connective tissue in normal and immobilized skeletal muscles. An immunohistochemical, polarization and scanning electron microscopic study. J Muscle Res Cell Motil 23:245–254CrossRefPubMed
go back to reference Kawai S, Takagi Y, Kaneko S et al (2011) Effect of three types of mixed anesthetic agents alternate to ketamine in mice. Exp Anim 60:481–487CrossRefPubMed Kawai S, Takagi Y, Kaneko S et al (2011) Effect of three types of mixed anesthetic agents alternate to ketamine in mice. Exp Anim 60:481–487CrossRefPubMed
go back to reference Kawamoto T (2003) Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole animals, insects and plants. Arch Histol Cytol 66:123–143CrossRefPubMed Kawamoto T (2003) Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole animals, insects and plants. Arch Histol Cytol 66:123–143CrossRefPubMed
go back to reference Kim JW, Kwon OY, Kim MH (2007) Differentially expressed genes and morphological changes during lengthened immobilization in rat soleus muscle. Differentiation 75:147–157CrossRefPubMed Kim JW, Kwon OY, Kim MH (2007) Differentially expressed genes and morphological changes during lengthened immobilization in rat soleus muscle. Differentiation 75:147–157CrossRefPubMed
go back to reference Kojima H, Sakuma E, Mabuchi Y et al (2008) Ultrastructural changes at the myotendinous junction induced by exercise. J Orthop Sci 13:233–239CrossRefPubMed Kojima H, Sakuma E, Mabuchi Y et al (2008) Ultrastructural changes at the myotendinous junction induced by exercise. J Orthop Sci 13:233–239CrossRefPubMed
go back to reference Malbouyres M, Guiraud A, Lefrançois C et al (2022) Lack of the myotendinous junction marker col22a1 results in posture and locomotion disabilities in zebrafish. Matrix Biol 109:1–18CrossRefPubMed Malbouyres M, Guiraud A, Lefrançois C et al (2022) Lack of the myotendinous junction marker col22a1 results in posture and locomotion disabilities in zebrafish. Matrix Biol 109:1–18CrossRefPubMed
go back to reference Nielsen KB, Lal NN, Sheard PW (2018) Age-related remodeling of the myotendinous junction in the mouse soleus muscle. Exp Gerontol 104:52–59CrossRefPubMed Nielsen KB, Lal NN, Sheard PW (2018) Age-related remodeling of the myotendinous junction in the mouse soleus muscle. Exp Gerontol 104:52–59CrossRefPubMed
go back to reference Nikolaou PK, Macdonald BL, Glisson RR et al (1987) Biomechanical and histological evaluation of muscle after controlled strain injury. Am J Sports Med 15:9–14CrossRefPubMed Nikolaou PK, Macdonald BL, Glisson RR et al (1987) Biomechanical and histological evaluation of muscle after controlled strain injury. Am J Sports Med 15:9–14CrossRefPubMed
go back to reference Perucca Orfei C, Lovati AB, Viganò M et al (2016) Dose-related and time-dependent development of collagenase-induced tendinopathy in rats. PLoS ONE 11:e0161590CrossRefPubMedPubMedCentral Perucca Orfei C, Lovati AB, Viganò M et al (2016) Dose-related and time-dependent development of collagenase-induced tendinopathy in rats. PLoS ONE 11:e0161590CrossRefPubMedPubMedCentral
go back to reference Pimentel Neto J, Rocha LC, Barbosa GK et al (2020) Myotendinous junction adaptations to ladder-based resistance training: identification of a new telocyte niche. Sci Rep 10:14124CrossRefPubMedPubMedCentral Pimentel Neto J, Rocha LC, Barbosa GK et al (2020) Myotendinous junction adaptations to ladder-based resistance training: identification of a new telocyte niche. Sci Rep 10:14124CrossRefPubMedPubMedCentral
go back to reference Rissatto Sierra L, Fávaro G, Cerri BR et al (2018) Myotendinous junction plasticity in aged ovariectomized rats submitted to aquatic training. Microsc Res Tech 81:816–822CrossRefPubMed Rissatto Sierra L, Fávaro G, Cerri BR et al (2018) Myotendinous junction plasticity in aged ovariectomized rats submitted to aquatic training. Microsc Res Tech 81:816–822CrossRefPubMed
go back to reference Roffino S, Carnino A, Charpiot P et al (1998) Increase in rat soleus myotendinous interface after a 14-d spaceflight. C R Acad Sci III 321:557–564CrossRefPubMed Roffino S, Carnino A, Charpiot P et al (1998) Increase in rat soleus myotendinous interface after a 14-d spaceflight. C R Acad Sci III 321:557–564CrossRefPubMed
go back to reference Sikes KJ, Andrie KM, McConnell A et al (2021) Clinical and histologic manifestations of a novel rectus femoris myotendinous junction injury in rats. Muscle Ligaments Tendons J 11:600–613CrossRef Sikes KJ, Andrie KM, McConnell A et al (2021) Clinical and histologic manifestations of a novel rectus femoris myotendinous junction injury in rats. Muscle Ligaments Tendons J 11:600–613CrossRef
go back to reference Tidball JG, Quan DM (1985) Reduction in myotendinous junction surface area of rats subjected to 4-day spaceflight. J Appl Physiol 73:59–64CrossRef Tidball JG, Quan DM (1985) Reduction in myotendinous junction surface area of rats subjected to 4-day spaceflight. J Appl Physiol 73:59–64CrossRef
go back to reference Tidball JG, Quan DM (1992) Modifications in myotendinous junction structure following denervation. Acta Neuropathol 84:135–140CrossRefPubMed Tidball JG, Quan DM (1992) Modifications in myotendinous junction structure following denervation. Acta Neuropathol 84:135–140CrossRefPubMed
go back to reference Wosczyna MN, Konishi CT, Perez Carbajal EEP et al (2019) Mesenchymal stromal cells are required for regeneration and homeostatic maintenance of skeletal muscle. Cell Rep 27:2029–35.e5CrossRefPubMedPubMedCentral Wosczyna MN, Konishi CT, Perez Carbajal EEP et al (2019) Mesenchymal stromal cells are required for regeneration and homeostatic maintenance of skeletal muscle. Cell Rep 27:2029–35.e5CrossRefPubMedPubMedCentral
go back to reference Yamamoto M, Sakiyama K, Kitamura K et al (2022) Development and regeneration of muscle, tendon, and myotendinous junctions in striated skeletal muscle. Int J Mol Sci 23:3006CrossRefPubMedPubMedCentral Yamamoto M, Sakiyama K, Kitamura K et al (2022) Development and regeneration of muscle, tendon, and myotendinous junctions in striated skeletal muscle. Int J Mol Sci 23:3006CrossRefPubMedPubMedCentral
go back to reference Yan R, Zhang H, Ma Y et al (2022) Discovery of muscle-tendon progenitor subpopulation in human myotendinous junction at single-cell resolution. Research (wash D c) 2022:9760390PubMed Yan R, Zhang H, Ma Y et al (2022) Discovery of muscle-tendon progenitor subpopulation in human myotendinous junction at single-cell resolution. Research (wash D c) 2022:9760390PubMed
go back to reference Yaseen W, Kraft-Sheleg O, Zaffryar-Eilot S et al (2021) Fibroblast fusion to the muscle fiber regulates myotendinous junction formation. Nat Commun 12:3852CrossRefPubMedPubMedCentral Yaseen W, Kraft-Sheleg O, Zaffryar-Eilot S et al (2021) Fibroblast fusion to the muscle fiber regulates myotendinous junction formation. Nat Commun 12:3852CrossRefPubMedPubMedCentral
Metadata
Title
Regeneration process of myotendinous junction injury induced by collagenase injection between Achilles tendon and soleus muscle in mice
Authors
Yutaro Yamamoto
Masahito Yamamoto
Hidetomo Hirouchi
Shuichiro Taniguchi
Genji Watanabe
Satoru Matsunaga
Shinichi Abe
Publication date
21-11-2023
Publisher
Springer Nature Singapore
Published in
Anatomical Science International / Issue 1/2024
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-023-00748-0

Other articles of this Issue 1/2024

Anatomical Science International 1/2024 Go to the issue