The dorsal portion of the bovine diaphragm as a useful tissue for producing a 3D muscle scaffold.
bovine diaphragm
decellularization tissue
muscle skeletal scaffold
organoid
Journal
Journal of anatomy
ISSN: 1469-7580
Titre abrégé: J Anat
Pays: England
ID NLM: 0137162
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
24
05
2023
received:
07
02
2023
accepted:
01
06
2023
pmc-release:
15
06
2025
medline:
23
10
2023
pubmed:
16
6
2023
entrez:
16
6
2023
Statut:
ppublish
Résumé
Three-dimensional (3D) organoids are an innovative approach to obtain an in vitro model for ex vivo studies to overcome the limitations of monolayer cell culture and reduce the use of animal models. An organoid of skeletal muscle requires the presence of the extracellular matrix to represent a functional muscle in vitro, which is why decellularized tissue is an optimal choice. Various muscles have been considered to produce a muscle organoid, most from rodents or small animals, and only recently some studies have been reported on the muscles of large animals. This work presents a muscular organoid produced from the bovine diaphragm, which has a peculiar multilayered structure with different fibre orientations depending on the considered area. This paper analyses the anatomical structure of the bovine diaphragm, selects the most appropriate portion, and presents a decellularization protocol for a multilayered muscle. In addition, a preliminary test of recellularization with primary bovine myocytes was presented with the future aim of obtaining a 3D muscle allogenic organoid, completely bovine-derived. The results demonstrate that the dorsal portion of bovine diaphragm presents a regular alternation of muscular and fibrous layers and that the complete decellularization does not affect the biocompatibility. These results provide a strong foundation for the potential application of this portion of tissue as a scaffold for in vitro studies of muscle organoids.
Identifiants
pubmed: 37322832
doi: 10.1111/joa.13915
pmc: PMC10557388
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
878-885Informations de copyright
© 2023 Anatomical Society.
Références
Akyürek, E.E., Busato, F., Murgiano, L., Bianchini, E., Carotti, M., Sandonà, D. et al. (2022) Differential analysis of Gly211Val and Gly286Val mutations affecting Sarco(endo)plasmic reticulum Ca2+ATPase (SERCA1) in congenital pseudomyotonia Romagnola cattle. International Journal of Molecular Sciences, 23, 12364. Available from: https://doi.org/10.3390/ijms232012364
Barbon, S., Stocco, E., Contran, M., Facchin, F., Boscolo-Berto, R., Todros, S. et al. (2022) Preclinical development of bioengineered allografts derived from decellularized human diaphragm. Biomedicine, 10(4), 739. Available from: https://doi.org/10.3390/biomedicines10040739
Bentzinger, C.F., Wang, Y.X., von Maltzahn, J., Soleimani, V.D., Yin, H. & Rudnicki, M.A. (2013) Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell, 12(1), 75-87.
Borschel, G.H., Dennis, R.G. & Kuzon, W.M. (2004) Contractile skeletal muscle tissue-engineered on an acellular scaffold. Plastic and Reconstructive Surgery, 113(2), 595-602.
Boso, D., Carraro, E., Maghin, E., Todros, S., Dedja, A., Giomo, M. et al. (2021) Porcine decellularized diaphragm hydrogel: a new option for skeletal muscle malformations. Biomedicine, 9(7), 709. Available from: https://doi.org/10.3390/biomedicines9070709
Brody, I.A. (1996) Muscle contracture induced by exercise: a syndrome attributable to decreased relaxing factor. The New England Journal of Medicine, 281, 187-192.
Dennis, R.G. & Kosnik, P.E. (2000) Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro. In Vitro Cellular and Developmental Biology. Animal, 36(5), 327-335.
Fatehullah, A., Tan, S.H. & Barker, N. (2016) Organoids as an in vitro model of human development and disease. Nature Cell Biology, 18(3), 246-254.
Faustino Martins, J.M., Fischer, C., Urzi, A., Vidal, R., Kunz, S., Ruffault, P.L. et al. (2020) Self-organizing 3D human trunk neuromuscular organoids. Cell Stem Cell, 26(2), 172-186.
Fogarty, M.J. & Sieck, G.C. (2019) Evolution and functional differentiation of the diaphragm muscle of mammals. Comprehensive Physiology, 9(2), 715-766.
Gamba, P.G., Conconi, M.T., lo Piccolo, R., Zara, G., Spinazzi, R. & Parnigotto, P.P. (2002) Experimental abdominal wall defect repaired with acellular matrix. Pediatric Surgery International, 18(5-6), 327-331.
Gattazzo, F., Urciuolo, A. & Bonaldo, P. (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochimica et Biophysica Acta, 1840, 2506-2519.
Khodabukus, A., Prabhu, N., Wang, J. & Bursac, N. (2018) In vitro tissue-engineered skeletal muscle models for studying muscle physiology and disease. Advanced Healthcare Materials, 7(15), e1701498. Available from: https://doi.org/10.1002/adhm.201701498
Kim, W., Gwon, Y., Park, S., Kim, H. & Kim, J. (2023) Therapeutic strategies of three-dimensional stem cell spheroids and organoids for tissue repair and regeneration. Bioactive Materials, 19, 50-74.
Lin, C.H., Yang, J.R., Chiang, N.J., Ma, H. & Tsay, R.Y. (2014) Evaluation of decellularized extracellular matrix of skeletal muscle for tissue engineering. International Journal of Artificial Organs, 37(7), 546-555.
Maghin, E., Carraro, E., Boso, D., Dedja, A., Giagante, M., Caccin, P. et al. (2022) Customized bioreactor enables the production of 3D diaphragmatic constructs influencing matrix remodeling and fibroblast overgrowth. NPJ Regenerative Medicine, 7(1), 25. Available from: https://doi.org/10.1038/s41536-022-00222-x
Martinello, T., Bronzini, I., Volpin, A., Vindigni, V., Maccatrozzo, L., Caporale, G. et al. (2014) Successful recellularization of human tendon scaffolds using adipose-derived mesenchymal stem cells and collagen gel. Journal of Tissue Engineering and Regenerative Medicine, 8(8), 612-619. Available from: https://doi.org/10.1002/term.1557
Merritt, E.K., Hammers, D.W., Tierney, M., Suggs, L.J., Walters, T.J. & Farrar, R.P. (2010) Functional assessment of skeletal muscle regeneration utilizing homologous extracellular matrix as scaffolding. Tissue Engineering. Part A, 16(4), 1395-1405.
Osaki, T., Uzel, S.G.M. & Kamm, R.D. (2020) On-chip 3D neuromuscular model for drug screening and precision medicine in neuromuscular disease. Nature Protocols, 15(2), 421-449.
Patel, K.H., Dunn, A.J., Talovic, M., Haas, G.J., Marcinczyk, M., Elmashhady, H. et al. (2019) Aligned nanofibers of decellularized muscle ECM support myogenic activity in primary satellite cells in vitro. Biomedical Materials (Bristol), 14(3), 035010. Available from: https://doi.org/10.1088/1748-605X/ab0b06
Philips, C., Terrie, L. & Thorrez, L. (2022) Decellularized skeletal muscle: a versatile biomaterial in tissue engineering and regenerative medicine. Biomaterials, 283, 121436. Available from: https://doi.org/10.1016/j.biomaterials.2022.121436
Piccoli, M., Urbani, L., Alvarez-Fallas, M.E., Franzin, C., Dedja, A., Bertin, E. et al. (2016) Improvement of diaphragmatic performance through orthotopic application of decellularized extracellular matrix patch. Biomaterials, 74, 245-255.
Porzionato, A., Sfriso, M.M., Pontini, A., Macchi, V., Petrelli, L., Pavan, P.G. et al. (2015) Decellularized human skeletal muscle as biologic scaffold for reconstructive surgery. International Journal of Molecular Sciences, 16(7), 14808-14831.
Quarta, M., Cromie, M., Chacon, R., Blonigan, J., Garcia, V., Akimenko, I. et al. (2017) Bioengineered constructs combined with exercise enhance stem cell-mediated treatment of volumetric muscle loss. Nature Communications, 8, 15613. Available from: https://doi.org/10.1038/ncomms15613
Remya, V., Kumar, N., Saxena, S., Shrivastava, S., Sharma, A.K., Kutty, M. et al. (2020) Mesenchymal stem cell tailored bioengineered scaffolds derived from bubaline diaphragm and aortic matrices for reconstruction of abdominal wall defects. Journal of Tissue Engineering and Regenerative Medicine, 14(12), 1763-1778.
Ren, Y., Yang, X., Ma, Z., Sun, X., Zhang, Y., Li, W. et al. (2021) Developments and opportunities for 3D bioprinted organoids. International Journal of Bioprinting, 7(3), 18-36.
Sanes, Y.R. (1982) Laminin, fibronectin and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. Journal of Cell Biology, 93, 442-451.
Sanes, Y.R. (2003) The basement membrane/basal lamina of skeletal muscle. The Journal of Biological Chemistry, 278, 12601-12604. Available from: https://doi.org/10.1074/jbc.R200027200
Saunders, S.K., Cole, S.Y., Sierra, V.A., Bracamonte, J.H., Toldo, S. & Soares, J.S. (2022) Evaluation of perfusion-driven cell seeding of small diameter engineered tissue vascular grafts with a custom-designed seed-and-culture bioreactor. PLoS One, 17(6), e0269499. Available from: https://doi.org/10.1371/journal.pone.0269499
Scano, M., Benetollo, A., Nogara, L., Bondì, M., Dalla Barba, F., Soardi, M. et al. (2021) CFTR corrector C17 is effective in muscular dystrophy, in vivo proof of concept in LGMDR3. Human Molecular Genetics, 31(4), 499-509.
Shamir, E.R. & Ewald, A.J. (2014) Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nature Reviews Molecular Cell Biology, 15(10), 647-664.
Takahashi, H., Shimizu, T. & Okano, T. (2018) Engineered human contractile Myofiber sheets as a platform for studies of skeletal muscle physiology. Scientific Reports, 8(1), 13932. Available from: https://doi.org/10.1038/s41598-018-32163-1
Tan, Y.H., Helms, H.R. & Nakayama, K.H. (2022) Decellularization strategies for regenerating cardiac and skeletal muscle tissues. Frontiers in Bioengineering and Biotechnology, 10, 831300. Available from: https://doi.org/10.3389/fbioe.2022.831300
Turner, N.J., Badylak, J.S., Weber, D.J. & Badylak, S.F. (2012) Biologic scaffold remodelling in a dog model of complex musculoskeletal injury. The Journal of Surgical Research, 176(2), 490-502.
Turner, N.J., Yates, A.J., Weber, D.J., Qureshi, I.R., Stolz, D.B., Gilbert, T.W. et al. (2010) Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Engineering, 16(11), 3309-3317.
Urciuolo, A., Quarta, M., Morbidoni, V., Gattazzo, F., Molon, S., Grumati, P. et al. (2013) Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nature Communications, 4, 1964.
Zhang, K., Bai, L., Xu, W. & Shen, C. (2022) Human neuromuscular junction three-dimensional organoid models and the insight in motor disorders. Journal of Molecular Cell Biology, 13(11), 767-773.
Zschüntzsch, J., Meyer, S., Shahriyari, M., Kummer, K., Schmidt, M., Kummer, S. et al. (2022) The evolution of complex muscle cell In vitro models to study Pathomechanisms and drug development of neuromuscular disease. Cell, 11(7), 1233.