Strain-dependent dynamic re-alignment of collagen fibers in skeletal muscle extracellular matrix.
| Title: | Strain-dependent dynamic re-alignment of collagen fibers in skeletal muscle extracellular matrix. |
|---|---|
| Authors: | Wohlgemuth RP; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States.; Sriram S; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States.; Henricson KE; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States.; Dinh DT; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States.; Brashear SE; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States.; Smith LR; Department of Neurobiology, Physiology, & Behavior, University of California Davis, United States; Department of Physical Medicine and Rehabilitation, University of California Davis, United States. Electronic address: lucsmith@ucdavis.edu. |
| Source: | Acta biomaterialia [Acta Biomater] 2024 Oct 01; Vol. 187, pp. 227-241. Date of Electronic Publication: 2024 Aug 30. |
| Publication Type: | Journal Article; Research Support, N.I.H., Extramural; Research Support, U.S. Gov't, Non-P.H.S. |
| Language: | English |
| Journal Info: | Publisher: Elsevier Country of Publication: England NLM ID: 101233144 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1878-7568 (Electronic) Linking ISSN: 17427061 NLM ISO Abbreviation: Acta Biomater Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Kidlington, Oxford, UK : Elsevier, c2004- |
| MeSH Terms: | Extracellular Matrix*/metabolism ; Muscle, Skeletal*/metabolism ; Collagen*/metabolism; Collagenases/metabolism ; Animals ; Mice ; Mice, Inbred DBA ; Stress, Mechanical ; Male |
| Abstract: | Collagen fiber architecture within the skeletal muscle extracellular matrix (ECM) is significant to passive muscle mechanics. While it is thought that collagen fibers re-orient themselves in response to changes in muscle length, this has not been dynamically visualized and quantified within a muscle. The goal of this study was to measure changes in collagen alignment across a range of muscle lengths and compare the corresponding alignment to muscle mechanics. We hypothesized that collagen fibers dynamically increase alignment in response to muscle stretching, and this change in alignment is related to passive muscle stiffness. Further, we hypothesized that digesting collagen fibers with collagenase would reduce the re-alignment response to muscle stretching. Using DBA/2J and D2.mdx mice, we isolated extensor digitorum longus (EDL), soleus, and diaphragm muscles for collagenase or sham treatment and decellularization to isolate intact or collagenase-digested decellularized muscles (DCMs). These DCMs were mechanically tested and imaged using second harmonic generation microscopy to measure collagen alignment across a range of strains. We found that collagen alignment increased in a strain-dependent fashion, but collagenase did not significantly affect the strain-dependent change in alignment. We also saw that the collagen fibers in the diaphragm epimysium (surface ECM) and perimysium (deep ECM) started at different angles, but still re-oriented in the same direction in response to stretching. These robust changes in collagen alignment were weakly related to passive DCM stiffness. Overall, we demonstrated that the architecture of muscle ECM is dynamic in response to strain and is related to passive muscle mechanics. STATEMENT OF SIGNIFICANCE: Our study presents a unique visualization and quantification of strain-induced changes in muscle collagen fiber alignment as they relate to passive mechanics. Using dynamic imaging of collagen in skeletal muscle we demonstrate that as skeletal muscle is stretched, collagen fibers re-orient themselves along the axis of stretch and increase their alignment. The degree of alignment and the increase in alignment are each weakly related to passive muscle stiffness. Collagenase treatments further demonstrate that the basis for muscle Extracellular matrix stiffness is dependent on factors beyond collagen crosslinking and alignment. Together the study contributes to the knowledge of the structure-function relationships of muscle extracellular matrix to tissue stiffness relevant to conditions of fibrosis and aberrant stiffness.; (Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.) |
| Competing Interests: | Conflict of Interest The authors declare that they have no known competing financial interests or personal relationships that could have influenced that work reported in this manuscript. |
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| Grant Information: | F31 AR082695 United States AR NIAMS NIH HHS; R01 AR079545 United States AR NIAMS NIH HHS |
| Contributed Indexing: | Keywords: Collagen architecture; Extracellular matrix; Muscle mechanics; Second harmonic generation; Skeletal muscle |
| Substance Nomenclature: | 9007-34-5 (Collagen); EC 3.4.24.- (Collagenases) |
| Entry Date(s): | Date Created: 20240829 Date Completed: 20241002 Latest Revision: 20250604 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC11804869 |
| DOI: | 10.1016/j.actbio.2024.08.035 |
| PMID: | 39209134 |
| Database: | MEDLINE |
Journal Article; Research Support, N.I.H., Extramural; Research Support, U.S. Gov't, Non-P.H.S.