Skip to main content

Advertisement

Log in

The Use of Collagen Methacrylate in Actuating Polyethylene Glycol Diacrylate–Acrylic Acid Scaffolds for Muscle Regeneration

  • Original Article
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

After muscle loss or injury, skeletal muscle tissue has the ability to regenerate and return its function. However, large volume defects in skeletal muscle tissue pose a challenge to regenerate due to the absence of regenerative elements such as biophysical and biochemical cues, making the development of new treatments necessary. One potential solution is to utilize electroactive polymers that can change size or shape in response to an external electric field. Poly(ethylene glycol) diacrylate (PEGDA) is one such polymer, which holds great potential as a scaffold for muscle tissue regeneration due to its mechanical properties. In addition, the versatile chemistry of this polymer allows for the conjugation of new functional groups to enhance its electroactive properties and biocompatibility. Herein, we have developed an electroactive copolymer of PEGDA and acrylic acid (AA) in combination with collagen methacrylate (CMA) to promote cell adhesion and proliferation. The electroactive properties of the CMA + PEGDA:AA constructs were investigated through actuation studies. Furthermore, the biological properties of the hydrogel were investigated in a 14-day in vitro study to evaluate myosin light chain (MLC) expression and metabolic activity of C2C12 mouse myoblast cells. The addition of CMA improved some aspects of material bioactivity, such as MLC expression in C2C12 mouse myoblast cells. However, the incorporation of CMA in the PEGDA:AA hydrogels reduced the sample movement when placed under an electric field, possibly due to steric hindrance from the CMA. Further research is needed to optimize the use of CMA in combination with PEGDA:AA as a potential scaffold for skeletal muscle tissue engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9
Figure 10
Figure 11

Similar content being viewed by others

References

  1. Agley, C. C., C. P. Velloso, N. R. Lazarus, and S. D. Harridge. An image analysis method for the precise selection and quantitation of fluorescently labeled cellular constituents: application to the measurement of human muscle cells in culture. J. Histochem. Cytochem. 60(6):428–438, 2012. https://doi.org/10.1369/0022155412442897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Apsite, I., J. M. Uribe, A. F. Posada, S. Rosenfeldt, S. Salehi, and L. Ionov. 4D biofabrication of skeletal muscle microtissues. Biofabrication.12:015016, 2019.

    PubMed  Google Scholar 

  3. Bach, A. D., J. P. Beier, J. Stern-Staeter, and R. E. Horch. Skeletal muscle tissue engineering. J. Cell. Mol. Med. 8(4):413–422, 2004.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bar-Cohen, Y. Electroactive polymer (EAP) actuators as artificial muscles: reality, potential, and challenges, 2nd ed. Bellingham, WA: SPIE Press, p. xvii, 2004.

    Google Scholar 

  5. Bar-Cohen, Y. Electroactive polymers as an enabling materials technology. Proc. Inst. Mech. Eng. G. 221(4):553–564, 2007.

    CAS  Google Scholar 

  6. Bauer, A., L. Gu, B. Kwee, W. A. Li, M. Dellacherie, A. D. Celiz, et al. Hydrogel substrate stress-relaxation regulates the spreading and proliferation of mouse myoblasts. Acta Biomater. 62:82–90, 2017.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Beier, J. P., J. Stern-Straeter, V. T. Foerster, U. Kneser, G. B. Stark, and A. D. Bach. Tissue engineering of injectable muscle: three-dimensional myoblast-fibrin injection in the syngeneic rat animal model. Plast. Reconstr. Surg. 118(5):1113–1121, 2006.

    CAS  PubMed  Google Scholar 

  8. Browe, D. P., C. Wood, M. T. Sze, K. A. White, T. Scott, R. M. Olabisi, et al. Characterization and optimization of actuating poly(ethylene glycol) diacrylate/acrylic acid hydrogels as artificial muscles. Polymer. 117:331–341, 2017.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Cai, A., M. Hardt, P. Schneider, R. Schmid, C. Lange, D. Dippold, et al. Myogenic differentiation of primary myoblasts and mesenchymal stromal cells under serum-free conditions on PCL–collagen I-nanoscaffolds. BMC Biotechnol. 18(1):1–12, 2018.

    Google Scholar 

  10. Chaturvedi, V., D. Naskar, B. F. Kinnear, E. Grenik, D. E. Dye, M. D. Grounds, et al. Silk fibroin scaffolds with muscle-like elasticity support in vitro differentiation of human skeletal muscle cells. J. Tissue Eng. Regen. Med. 11:3178–3192, 2017.

    CAS  PubMed  Google Scholar 

  11. Chaubaroux, C., F. Perrin-Schmitt, B. Senger, L. Vidal, J. C. Voegel, P. Schaaf, et al. Cell alignment driven by mechanically induced collagen fiber alignment in collagen/alginate coatings. Tissue Eng. C. 21(9):881–888, 2015.

    CAS  Google Scholar 

  12. Chen, S., T. Nakamoto, N. Kawazoe, and G. Chen. Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds. Biomaterials. 73:23–31, 2015. https://doi.org/10.1016/j.biomaterials.2015.09.010.

    Article  CAS  PubMed  Google Scholar 

  13. Choi, Y. J., Y. J. Jun, D. Y. Kim, H. G. Yi, S. H. Chae, J. Kang, et al. A 3D cell printed muscle construct with tissue-derived bioink for the treatment of volumetric muscle loss. Biomaterials. 206:160–169, 2019.

    CAS  PubMed  Google Scholar 

  14. Choi, Y. J., T. G. Kim, J. Jeong, H. G. Yi, J. W. Park, W. Hwang, et al. 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink. Adv. Healthc. Mater. 5(20):2636–2645, 2016.

    CAS  PubMed  Google Scholar 

  15. Clark, M. E. editor Pain issues among OEF and OIF returnees. In: VA/DOD Emerging Concepts Conference, 2007, Las Vegas, NV.

  16. De Deyne, P. G. Formation of sarcomeres in developing myotubes: role of mechanical stretch and contractile activation. Am. J. Physiol. Cell Physiol. 279(6):C1801–C1811, 2000.

    CAS  PubMed  Google Scholar 

  17. De Santis, M. M., H. N. Alsafadi, S. Tas, D. A. Bolukbas, S. Prithiviraj, I. A. N. Da Silva, et al. Extracellular-matrix-reinforced bioinks for 3D bioprinting human tissue. Adv. Mater.33:e2005476, 2021.

    PubMed  Google Scholar 

  18. Denes, L. T., L. A. Riley, J. R. Mijares, J. D. Arboleda, K. McKee, K. A. Esser, et al. Culturing C2C12 myotubes on micromolded gelatin hydrogels accelerates myotube maturation. Skelet. Muscle. 9(1):17, 2019.

    PubMed  PubMed Central  Google Scholar 

  19. Drzewiecki, K. E., A. S. Parmar, I. D. Gaudet, J. R. Branch, D. H. Pike, V. Nanda, et al. Methacrylation induces rapid, temperature-dependent, reversible self-assembly of type-I collagen. Langmuir. 30(37):11204–11211, 2014.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Fujita, H., T. Nedachi, and M. Kanzaki. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp. Cell Res. 313(9):1853–1865, 2007.

    CAS  PubMed  Google Scholar 

  21. Fujita, H., K. Shimizu, and E. Nagamori. Novel method for fabrication of skeletal muscle construct from the C2C12 myoblast cell line using serum-free medium AIM-V. Biotechnol. Bioeng. 103(5):1034–1041, 2009.

    CAS  PubMed  Google Scholar 

  22. Garcia-Lizarribar, A., X. Fernandez-Garibay, F. Velasco-Mallorqui, A. G. Castano, J. Samitier, and J. Ramon-Azcon. Composite biomaterials as long-lasting scaffolds for 3D bioprinting of highly aligned muscle tissue. Macromol. Biosci.18:e1800167, 2018.

    PubMed  Google Scholar 

  23. Gaudet, I. D., and D. I. Shreiber. Characterization of methacrylated type-I collagen as a dynamic, photoactive hydrogel. Biointerphases. 7(1–4):25, 2012.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Gong, H. Y., J. Park, W. Kim, J. Kim, J. Y. Lee, and W. G. Koh. A novel conductive and micropatterned PEG-based hydrogel enabling the topographical and electrical stimulation of myoblasts. ACS Appl. Mater. Interfaces. 11:47695–47706, 2019.

    CAS  PubMed  Google Scholar 

  25. Gribova, V., C. Y. Liu, A. Nishiguchi, M. Matsusaki, T. Boudou, C. Picart, et al. Construction and myogenic differentiation of 3D myoblast tissues fabricated by fibronectin–gelatin nanofilm coating. Biochem. Biophys. Res. Commun. 474:515–521, 2016.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Hill, E., T. Boontheekul, and D. J. Mooney. Designing scaffolds to enhance transplanted myoblast survival and migration. Tissue Eng. 12:1295–1304, 2006.

    CAS  PubMed  Google Scholar 

  27. Hitti, M. Report: Nearly 5.6 Million Americans Paralyzed: Web MD, 2009.

  28. Iyer, S. R., N. Udpa, and Y. Gao. Chitosan selectively promotes adhesion of myoblasts over fibroblasts. J. Biomed. Mater. Res. A. 103:1899–1906, 2015.

    CAS  PubMed  Google Scholar 

  29. Jo, H., M. Sim, S. Kim, S. Yang, Y. Yoo, J. H. Park, et al. Electrically conductive graphene/polyacrylamide hydrogels produced by mild chemical reduction for enhanced myoblast growth and differentiation. Acta Biomater. 48:100–109, 2017.

    CAS  PubMed  Google Scholar 

  30. Joglekar, D., R. Warren, D. Browe, E. Ekwueme, M. Dariani, N. D. Padliya, et al. Investigating the effects of fertilized egg yolk extract on myoblast proliferation and differentiation. Regen. Eng. Transl. Med. 6:125–137, 2020.

    CAS  Google Scholar 

  31. Kim, W., C. H. Jang, and G. H. Kim. A myoblast-laden collagen bioink with fully aligned Au nanowires for muscle-tissue regeneration. Nano Lett. 19:8612–8620, 2019.

    CAS  PubMed  Google Scholar 

  32. Kim, W., H. Lee, J. Lee, A. Atala, J. J. Yoo, S. J. Lee, et al. Efficient myotube formation in 3D bioprinted tissue construct by biochemical and topographical cues. Biomaterials.230:119632, 2020.

    CAS  PubMed  Google Scholar 

  33. Ko, U. H., S. Park, H. Bang, M. Kim, H. Shin, and J. H. Shin. Promotion of myogenic maturation by timely application of electric field along the topographical alignment. Tissue Eng. A. 24:752–760, 2018.

    CAS  Google Scholar 

  34. Kung, F. H., D. Sillitti, A. B. Shrirao, D. I. Shreiber, and B. L. Firestein. Collagen nanofibre anisotropy induces myotube differentiation and acetylcholine receptor clustering. J. Tissue Eng. Regen. Med. 12:e2010–e2019, 2018.

    CAS  PubMed  Google Scholar 

  35. Lee, H., W. Kim, J. Lee, J. J. Yoo, G. H. Kim, and S. J. Lee. Effect of hierarchical scaffold consisting of aligned dECM nanofibers and poly(lactide-co-glycolide) struts on the orientation and maturation of human muscle progenitor cells. ACS Appl. Mater. Interfaces. 11:39449–39458, 2019.

    CAS  PubMed  Google Scholar 

  36. Levett, P. A., F. P. W. Melchels, K. Schrobback, D. W. Hutmacher, J. Malda, and T. J. Klein. A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate. Acta Biomater. 10(1):214–223, 2014. https://doi.org/10.1016/j.actbio.2013.10.005.

    Article  CAS  PubMed  Google Scholar 

  37. Li, R., N. L. McRae, D. R. McCulloch, M. Boyd-Moss, C. J. Barrow, D. R. Nisbet, et al. Large and small assembly: combining functional macromolecules with small peptides to control the morphology of skeletal muscle progenitor cells. Biomacromolecules. 19:825–837, 2018.

    PubMed  Google Scholar 

  38. Liao, I. C., J. B. Liu, N. Bursac, and K. W. Leong, editors. Effect of electromechanical stimulation on the maturation of myotubes on aligned electrospun fibers. In: Annual Meeting of the Biomedical-Engineering-Society, 2 Oct 2008, St Louis, MO, 2008.

  39. Liu, X., Y. Gao, X. Long, T. Hayashi, K. Mizuno, S. Hattori, et al. Type I collagen promotes the migration and myogenic differentiation of C2C12 myoblasts via the release of interleukin-6 mediated by FAK/NF-κB p65 activation. Food Funct. 11(1):328–338, 2020.

    CAS  PubMed  Google Scholar 

  40. Lumia, R., and M. Shahinpoor. IPMC microgripper research and development. J. Phys. Conf. Ser. 127(1):1–15, 2008.

    Google Scholar 

  41. Manchineella, S., G. Thrivikraman, K. K. Khanum, P. C. Ramamurthy, B. Basu, and T. Govindaraju. Pigmented silk nanofibrous composite for skeletal muscle tissue engineering. Adv. Healthc. Mater. 5:1222–1232, 2016.

    CAS  PubMed  Google Scholar 

  42. Markert, C. D., A. Atala, J. K. Cann, G. Christ, M. Furth, F. Ambrosio, et al. Mesenchymal stem cells: emerging therapy for Duchenne muscular dystrophy. PM&R. 1(6):547–559, 2009.

    Google Scholar 

  43. Mazzoccoli, J. P., D. L. Feke, H. Baskaran, and P. N. Pintauro. Mechanical and cell viability properties of crosslinked low- and high-molecular weight poly (ethylene glycol) diacrylate blends. J. Biomed. Mater. Res. A. 93(2):558–566, 2010.

    PubMed  PubMed Central  Google Scholar 

  44. Meriggioli, M. N., and D. B. Sanders. Autoimmune myasthenia gravis: emerging clinical and biological heterogeneity. Lancet Neurol. 8(5):475–490, 2009.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Nagai, Y., H. Yokoi, K. Kaihara, and K. Naruse. The mechanical stimulation of cells in 3D culture within a self-assembling peptide hydrogel. Biomaterials. 33:1044–1051, 2012.

    CAS  PubMed  Google Scholar 

  46. Narayanan, N., Z. Jia, K. H. Kim, L. Kuang, P. Lengemann, G. Shafer, et al. Biomimetic glycosaminoglycan-based scaffolds improve skeletal muscle regeneration in a murine volumetric muscle loss model. Bioact. Mater. 6:1201–1213, 2021.

    CAS  PubMed  Google Scholar 

  47. Narayanan, N., C. Jiang, C. Wang, G. Uzunalli, N. Whittern, D. Chen, et al. Harnessing fiber diameter-dependent effects of myoblasts toward biomimetic scaffold-based skeletal muscle regeneration. Front. Bioeng. Biotechnol. 8:203, 2020.

    PubMed  PubMed Central  Google Scholar 

  48. Neuhaus, R., N. Zahiri, J. Petrs, et al. Integrating ionic electroactive polymer actuators and sensors into adaptive building skins—potentials and limitations. Front. Built Environ. 2020. https://doi.org/10.3389/fbuil.2020.00095.

    Article  Google Scholar 

  49. Ngan, C., A. Quigley, C. O’Connell, M. Kita, J. Bourke, G. G. Wallace, et al. 3D bioprinting and differentiation of primary skeletal muscle progenitor cells. Methods Mol. Biol. 2140:229–242, 2020.

    CAS  PubMed  Google Scholar 

  50. Ostrovidov, S., S. Ahadian, J. Ramon-Azcon, V. Hosseini, T. Fujie, S. P. Parthiban, et al. Three-dimensional co-culture of C2C12/PC12 cells improves skeletal muscle tissue formation and function. J. Tissue Eng. Regen. Med. 11:582–595, 2017.

    CAS  PubMed  Google Scholar 

  51. Ostrovidov, S., X. Shi, L. Zhang, X. Liang, S. B. Kim, T. Fujie, et al. Myotube formation on gelatin nanofibers–multi-walled carbon nanotubes hybrid scaffolds. Biomaterials. 35:6268–6277, 2014.

    CAS  PubMed  Google Scholar 

  52. Pankongadisak, P., E. Tsekoura, O. Suwantong, and H. Uludag. Electrospun gelatin matrices with bioactive pDNA polyplexes. Int. J. Biol. Macromol. 149:296–308, 2020.

    CAS  PubMed  Google Scholar 

  53. Park, J., J. H. Choi, S. Kim, I. Jang, S. Jeong, and J. Y. Lee. Micropatterned conductive hydrogels as multifunctional muscle-mimicking biomaterials: graphene-incorporated hydrogels directly patterned with femtosecond laser ablation. Acta Biomater. 97:141–153, 2019.

    CAS  PubMed  Google Scholar 

  54. Patel, K. H., A. J. Dunn, M. Talovic, G. J. Haas, M. Marcinczyk, H. Elmashhady, et al. Aligned nanofibers of decellularized muscle ECM support myogenic activity in primary satellite cells in vitro. Biomed. Mater.14:035010, 2019.

    CAS  PubMed  Google Scholar 

  55. Patel, A., S. Vendrell-Gonzalez, G. Haas, M. Marcinczyk, N. Ziemkiewicz, M. Talovic, et al. Regulation of myogenic activity by substrate and electrical stimulation in vitro. BioResearch Open Access. 8:129–138, 2019.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Pollot, B. E., C. R. Rathbone, J. C. Wenke, and T. Guda. Natural polymeric hydrogel evaluation for skeletal muscle tissue engineering. J. Biomed. Mater. Res. B. 106:672–679, 2018.

    CAS  Google Scholar 

  57. Porzionato, A., M. M. Sfriso, A. Pontini, V. Macchi, L. Petrelli, P. G. Pavan, et al. Decellularized human skeletal muscle as biologic scaffold for reconstructive surgery. Int. J. Mol. Sci. 16:14808–14831, 2015.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Pruller, J., I. Mannhardt, T. Eschenhagen, P. S. Zammit, and N. Figeac. Satellite cells delivered in their niche efficiently generate functional myotubes in three-dimensional cell culture. PLoS ONE.13:e0202574, 2018.

    PubMed  PubMed Central  Google Scholar 

  59. Punga, A. R., and M. A. Ruegg. Signaling and aging at the neuromuscular synapse: lessons learnt from neuromuscular diseases. Curr. Opin. Pharmacol. 12(3):340–346, 2012.

    CAS  PubMed  Google Scholar 

  60. Rando, T. A. Non-viral gene therapy for Duchenne muscular dystrophy: progress and challenges. Biochim. Biophys. Acta Mol. Basis Dis. 1772(2):263–271, 2007.

    CAS  Google Scholar 

  61. Romanazzo, S., G. Forte, M. Ebara, K. Uto, S. Pagliari, T. Aoyagi, et al. Substrate stiffness affects skeletal myoblast differentiation in vitro. Sci. Technol. Adv. Mater.13(6):064211, 2012.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Rowley, J. A., and D. J. Mooney. Alginate type and RGD density control myoblast phenotype. J. Biomed. Mater. Res. 60:217–223, 2002.

    CAS  PubMed  Google Scholar 

  63. Scott, T. E., A. Khalili, B. Newton, R. Warren, D. P. Browe, and J. W. Freeman. Characterization and optimization of a positively charged poly(ethylene glycol) diacrylate hydrogel as an actuating muscle tissue engineering scaffold. Polym. Adv. Technol. 30(10):2604–2612, 2019.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Serena, E., M. Flaibani, S. Carnio, L. Boldrin, L. Vitiello, P. De Coppi, et al. Electrophysiologic stimulation improves myogenic potential of muscle precursor cells grown in a 3D collagen scaffold. Neurol. Res. 30:207–214, 2008.

    CAS  PubMed  Google Scholar 

  65. Somers, S. M., N. Y. Zhang, J. B. F. Morrissette-McAlmon, K. Tran, H. Q. Mao, and W. L. Grayson. Myoblast maturity on aligned microfiber bundles at the onset of strain application impacts myogenic outcomes. Acta Biomater. 94:232–242, 2019.

    PubMed  Google Scholar 

  66. Ungerleide, J. L., T. D. Johnson, N. Rao, and K. L. Christman. Fabrication and characterization of injectable hydrogels derived from decellularized skeletal and cardiac muscle. Methods. 84:53–59, 2015.

    Google Scholar 

  67. Ungerleider, J. L., T. D. Johnson, M. J. Hernandez, D. I. Elhag, R. L. Braden, M. Dzieciatkowska, et al. Extracellular matrix hydrogel promotes tissue remodeling, arteriogenesis, and perfusion in a rat hindlimb ischemia model. JACC Basic Transl. Sci. 1(1–2):32–44, 2016.

    PubMed  PubMed Central  Google Scholar 

  68. Vartanian, A. D., A. Audfray, B. A. Jaam, M. Janot, S. Legardinier, A. Maftah, et al. Protein O-fucosyltransferase 1 expression impacts myogenic C2C12 cell commitment via the Notch signaling pathway. Mol. Cell. Biol. 35(2):391–405, 2015.

    Google Scholar 

  69. Venugopal, J., L. L. Ma, T. Yong, and S. Ramakrishna. In vitro study of smooth muscle cells on polycaprolactone and collagen nanofibrous matrices. Cell Biol. Int. 29(10):861–867, 2005. https://doi.org/10.1016/j.cellbi.2005.03.026.

    Article  CAS  PubMed  Google Scholar 

  70. Villanueva, P., S. Pereira, A. Olmo, P. Perez, Y. Yuste, A. Yufera, et al. Electrical pulse stimulation of skeletal myoblasts cell cultures with simulated action potentials. J. Tissue Eng. Regen. Med. 13:1265–1269, 2019.

    CAS  PubMed  Google Scholar 

  71. Wagner, K. R., N. Lechtzin, and D. P. Judge. Current treatment of adult Duchenne muscular dystrophy. Biochim. Biophys. Acta Mol. Basis Dis. 1772(2):229–237, 2007.

    CAS  Google Scholar 

  72. Wang, W., M. Fan, L. Zhang, S. H. Liu, L. Sun, and C. Y. Wang. Compatibility of hyaluronic acid hydrogel and skeletal muscle myoblasts. Biomed. Mater.4:025011, 2009.

    PubMed  Google Scholar 

  73. Willmann, R., S. Possekel, J. Dubach-Powell, T. Meier, and M. A. Ruegg. Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul. Disord. 19(4):241–249, 2009.

    PubMed  Google Scholar 

  74. Yeo, M., and G. Kim. Nano/microscale topographically designed alginate/PCL scaffolds for inducing myoblast alignment and myogenic differentiation. Carbohydr. Polym.223:115041, 2019.

    CAS  PubMed  Google Scholar 

  75. Yeo, M., and G. Kim. Micro/nano-hierarchical scaffold fabricated using a cell electrospinning/3D printing process for co-culturing myoblasts and HUVECs to induce myoblast alignment and differentiation. Acta Biomater. 107:102–114, 2020.

    CAS  PubMed  Google Scholar 

  76. Zhang, J., Z. Q. Hu, N. J. Turner, S. F. Teng, W. Y. Cheng, H. Y. Zhou, et al. Perfusion-decellularized skeletal muscle as a three-dimensional scaffold with a vascular network template. Biomaterials. 89:114–126, 2016.

    CAS  PubMed  Google Scholar 

Download references

Conflict of interest

No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph W. Freeman.

Additional information

Associate Editor Elizabeth Cosgriff-Hernandez oversaw the review of this article.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miranda Alarcón, Y.S., Jazwinska, D., Lymon, T. et al. The Use of Collagen Methacrylate in Actuating Polyethylene Glycol Diacrylate–Acrylic Acid Scaffolds for Muscle Regeneration. Ann Biomed Eng 51, 1165–1180 (2023). https://doi.org/10.1007/s10439-023-03139-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-023-03139-8

Keywords

Navigation