Alterations of Extracellular Matrix Mechanical Properties Contribute to Age-Related Functional Impairment of Human Skeletal Muscles

Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are the determinants of such change. To answer this question, we compared the passive stress generated by elongation of fibers alone and arrange...

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Published in	International journal of molecular sciences Vol. 21; no. 11; p. 3992
Main Authors	Pavan, Piero, Monti, Elena, Bondí, Michela, Fan, Chenglei, Stecco, Carla, Narici, Marco, Reggiani, Carlo, Marcucci, Lorenzo
Format	Journal Article
Language	English
Published	Switzerland MDPI AG 02.06.2020 MDPI
Subjects	Adolescent Adult Age groups Aged Aged, 80 and over Aging Aging - pathology Biomechanical Phenomena Collagen - chemistry Extracellular matrix Extracellular Matrix - physiology Female Humans Male Mechanical properties Middle Aged Muscle Fibers, Skeletal - pathology Muscle, Skeletal - physiopathology Musculoskeletal system Sarcomeres - metabolism Stress, Mechanical Tendons Young Adult collagen aging resting tension skeletal muscle extracellular matrix single muscle fiber
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ISSN	1422-0067 1661-6596 1422-0067
DOI	10.3390/ijms21113992

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Abstract	Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are the determinants of such change. To answer this question, we compared the passive stress generated by elongation of fibers alone and arranged in small bundles in young healthy (Y: 21 years) and elderly (E: 67 years) subjects. The physiological range of sarcomere length (SL) 2.5–3.3 μm was explored. The area of ECM between muscle fibers was determined on transversal sections with picrosirius red, a staining specific for collagen fibers. The passive tension of fiber bundles was significantly higher in E compared to Y at all SL. However, the resistance to elongation of fibers alone was not different between the two groups, while the ECM contribution was significantly increased in E compared to Y. The proportion of muscle area occupied by ECM increased from 3.3% in Y to 8.2% in E. When the contribution of ECM to bundle tension was normalized to the fraction of area occupied by ECM, the difference disappeared. We conclude that, in human skeletal muscles, the age-related reduced compliance is due to an increased stiffness of ECM, mainly caused by collagen accumulation.
AbstractList	Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are the determinants of such change. To answer this question, we compared the passive stress generated by elongation of fibers alone and arranged in small bundles in young healthy (Y: 21 years) and elderly (E: 67 years) subjects. The physiological range of sarcomere length (SL) 2.5–3.3 μm was explored. The area of ECM between muscle fibers was determined on transversal sections with picrosirius red, a staining specific for collagen fibers. The passive tension of fiber bundles was significantly higher in E compared to Y at all SL. However, the resistance to elongation of fibers alone was not different between the two groups, while the ECM contribution was significantly increased in E compared to Y. The proportion of muscle area occupied by ECM increased from 3.3% in Y to 8.2% in E. When the contribution of ECM to bundle tension was normalized to the fraction of area occupied by ECM, the difference disappeared. We conclude that, in human skeletal muscles, the age-related reduced compliance is due to an increased stiffness of ECM, mainly caused by collagen accumulation. Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are the determinants of such change. To answer this question, we compared the passive stress generated by elongation of fibers alone and arranged in small bundles in young healthy (Y: 21 years) and elderly (E: 67 years) subjects. The physiological range of sarcomere length (SL) 2.5-3.3 μm was explored. The area of ECM between muscle fibers was determined on transversal sections with picrosirius red, a staining specific for collagen fibers. The passive tension of fiber bundles was significantly higher in E compared to Y at all SL. However, the resistance to elongation of fibers alone was not different between the two groups, while the ECM contribution was significantly increased in E compared to Y. The proportion of muscle area occupied by ECM increased from 3.3% in Y to 8.2% in E. When the contribution of ECM to bundle tension was normalized to the fraction of area occupied by ECM, the difference disappeared. We conclude that, in human skeletal muscles, the age-related reduced compliance is due to an increased stiffness of ECM, mainly caused by collagen accumulation.Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are the determinants of such change. To answer this question, we compared the passive stress generated by elongation of fibers alone and arranged in small bundles in young healthy (Y: 21 years) and elderly (E: 67 years) subjects. The physiological range of sarcomere length (SL) 2.5-3.3 μm was explored. The area of ECM between muscle fibers was determined on transversal sections with picrosirius red, a staining specific for collagen fibers. The passive tension of fiber bundles was significantly higher in E compared to Y at all SL. However, the resistance to elongation of fibers alone was not different between the two groups, while the ECM contribution was significantly increased in E compared to Y. The proportion of muscle area occupied by ECM increased from 3.3% in Y to 8.2% in E. When the contribution of ECM to bundle tension was normalized to the fraction of area occupied by ECM, the difference disappeared. We conclude that, in human skeletal muscles, the age-related reduced compliance is due to an increased stiffness of ECM, mainly caused by collagen accumulation.
Author	Bondí, Michela Reggiani, Carlo Stecco, Carla Pavan, Piero Fan, Chenglei Narici, Marco Monti, Elena Marcucci, Lorenzo
AuthorAffiliation	1 Department of Industrial Engineering, University of Padova, 35131 Padova, Italy; piero.pavan@unipd.it 6 Science and Research Centre, ZRS, Institute for Kinesiology, 6000 Koper, Slovenia 8 Center for Biosystems Dynamics Research, RIKEN, Suita, Osaka 565-0874, Japan 5 Department of Neurosciences, Institute of Human Anatomy, University of Padova, 35128 Padova, Italy; yutianfan1218@163.com (C.F.); carla.stecco@unipd.it (C.S.) 4 Department of Biomedical Sciences, University of Padova, 35131 Padova, Italy; elena.monti.1@phd.unipd.it (E.M.); michela.bondi@unipd.it (M.B.); marco.narici@unipd.it (M.N.) 2 Fondazione Istituto di Ricerca Pediatrica Città della Speranza, 35127 Padova, Italy 7 CIR-Myo Myology Center, University of Padova, 35121 Padova, Italy 3 Centre for Mechanics of Biological Materials, University of Padova, 35131 Padova, Italy; carlo.reggiani@unipd.it
AuthorAffiliation_xml	– name: 2 Fondazione Istituto di Ricerca Pediatrica Città della Speranza, 35127 Padova, Italy – name: 1 Department of Industrial Engineering, University of Padova, 35131 Padova, Italy; piero.pavan@unipd.it – name: 4 Department of Biomedical Sciences, University of Padova, 35131 Padova, Italy; elena.monti.1@phd.unipd.it (E.M.); michela.bondi@unipd.it (M.B.); marco.narici@unipd.it (M.N.) – name: 7 CIR-Myo Myology Center, University of Padova, 35121 Padova, Italy – name: 3 Centre for Mechanics of Biological Materials, University of Padova, 35131 Padova, Italy; carlo.reggiani@unipd.it – name: 8 Center for Biosystems Dynamics Research, RIKEN, Suita, Osaka 565-0874, Japan – name: 6 Science and Research Centre, ZRS, Institute for Kinesiology, 6000 Koper, Slovenia – name: 5 Department of Neurosciences, Institute of Human Anatomy, University of Padova, 35128 Padova, Italy; yutianfan1218@163.com (C.F.); carla.stecco@unipd.it (C.S.)
Author_xml	– sequence: 1 givenname: Piero surname: Pavan fullname: Pavan, Piero – sequence: 2 givenname: Elena surname: Monti fullname: Monti, Elena – sequence: 3 givenname: Michela surname: Bondí fullname: Bondí, Michela – sequence: 4 givenname: Chenglei orcidid: 0000-0002-1129-0379 surname: Fan fullname: Fan, Chenglei – sequence: 5 givenname: Carla orcidid: 0000-0002-8767-4555 surname: Stecco fullname: Stecco, Carla – sequence: 6 givenname: Marco orcidid: 0000-0003-0167-1845 surname: Narici fullname: Narici, Marco – sequence: 7 givenname: Carlo orcidid: 0000-0001-8080-361X surname: Reggiani fullname: Reggiani, Carlo – sequence: 8 givenname: Lorenzo orcidid: 0000-0002-9542-4417 surname: Marcucci fullname: Marcucci, Lorenzo
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Snippet	Aging of human skeletal muscles is associated with increased passive stiffness, but it is still debated whether muscle fibers or extracellular matrix (ECM) are...
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SubjectTerms	Adolescent Adult Age groups Aged Aged, 80 and over Aging Aging - pathology Biomechanical Phenomena Collagen - chemistry Extracellular matrix Extracellular Matrix - physiology Female Humans Male Mechanical properties Middle Aged Muscle Fibers, Skeletal - pathology Muscle, Skeletal - physiopathology Musculoskeletal system Sarcomeres - metabolism Stress, Mechanical Tendons Young Adult
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Title	Alterations of Extracellular Matrix Mechanical Properties Contribute to Age-Related Functional Impairment of Human Skeletal Muscles
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