Highly Aligned Ternary Nanofiber Matrices Loaded with MXene Expedite Regeneration of Volumetric Muscle Loss
Corresponding Author: Dong‑Wook Han
Nano-Micro Letters,
Vol. 16 (2024), Article Number: 73
Abstract
Current therapeutic approaches for volumetric muscle loss (VML) face challenges due to limited graft availability and insufficient bioactivities. To overcome these limitations, tissue-engineered scaffolds have emerged as a promising alternative. In this study, we developed aligned ternary nanofibrous matrices comprised of poly(lactide-co-ε-caprolactone) integrated with collagen and Ti3C2Tx MXene nanoparticles (NPs) (PCM matrices), and explored their myogenic potential for skeletal muscle tissue regeneration. The PCM matrices demonstrated favorable physicochemical properties, including structural uniformity, alignment, microporosity, and hydrophilicity. In vitro assays revealed that the PCM matrices promoted cellular behaviors and myogenic differentiation of C2C12 myoblasts. Moreover, in vivo experiments demonstrated enhanced muscle remodeling and recovery in mice treated with PCM matrices following VML injury. Mechanistic insights from next-generation sequencing revealed that MXene NPs facilitated protein and ion availability within PCM matrices, leading to elevated intracellular Ca2+ levels in myoblasts through the activation of inducible nitric oxide synthase (iNOS) and serum/glucocorticoid regulated kinase 1 (SGK1), ultimately promoting myogenic differentiation via the mTOR-AKT pathway. Additionally, upregulated iNOS and increased NO– contributed to myoblast proliferation and fiber fusion, thereby facilitating overall myoblast maturation. These findings underscore the potential of MXene NPs loaded within highly aligned matrices as therapeutic agents to promote skeletal muscle tissue recovery.
Highlights:
1 The aligned ternary nanofibrous matrices composed of poly(lactide-co-ε-caprolactone), collagen, and Ti3C2Tx MXene nanoparticles were fabricated (referred as PCM matrices).
2 The aligned PCM matrices exhibited favorable physicochemical properties and excellent cytocompatibility and myogenic properties, which in turn promoted fast regeneration of volumetric muscle loss in vivo.
3 The Ca2+ binding of MXene nanoparticles activated inducible nitric oxide synthase and serum/glucocorticoid regulated kinase 1-mediated mTOR-AKT pathway to promote myoblast differentiation and maturation.
Keywords
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- B.F. Grogan, J.R. Hsu, Volumetric muscle loss. Am. Acad. Orthop. Surg. 19, S35–S37 (2011). https://doi.org/10.5435/00124635-201102001-00007
- S. Tamai, S. Komatsu, H. Sakamoto, S. Sano, N. Sasauchi, Free muscle transplants in dogs, with microsurgical neurovascular anastomoses. Plast. Reconstr. Surg. 46, 219–225 (1970). https://doi.org/10.1097/00006534-197009000-00002
- K. Doi, Y. Arakawa, Y. Hattori, A.S. Baliarsing, Restoration of elbow flexion with functioning free muscle transfer in arthrogryposis: a report of two cases. J. Bone Joint Surg. Am. 93, e105 (2011). https://doi.org/10.2106/JBJS.J.01846
- T.C. Burns, D.J. Stinner, D.R. Possley, A.W. Mack, T.T. Eckel et al., Does the zone of injury in combat-related type III open tibia fractures preclude the use of local soft tissue coverage? J. Orthop. Trauma 24, 697–703 (2010). https://doi.org/10.1097/BOT.0b013e3181d048b8
- J.G. Owens, J.A. Blair, J.C. Patzkowski, R.V. Blanck, J.R. Hsu, Return to running and sports participation after limb salvage. J. Trauma Inj. Infect. Crit. Care 71, S120–S124 (2011). https://doi.org/10.1097/ta.0b013e3182219225
- J.C. Patzkowski, R.V. Blanck, J.G. Owens, J.M. Wilken, J.A. Blair et al., Can an ankle-foot orthosis change hearts and minds? J. Surg. Orthop. Adv. 20, 8–18 (2011)
- S. Ostrovidov, V. Hosseini, S. Ahadian, T. Fujie, S.P. Parthiban et al., Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng. Part B Rev. 20, 403–436 (2014). https://doi.org/10.1089/ten.TEB.2013.0534
- R. Yu, H. Zhang, B. Guo, Conductive biomaterials as bioactive wound dressing for wound healing and skin tissue engineering. Nano-Micro Lett. 14, 1 (2021). https://doi.org/10.1007/s40820-021-00751-y
- L. Wang, Y. Wu, B. Guo, P.X. Ma, Nanofiber yarn/hydrogel core-shell scaffolds mimicking native skeletal muscle tissue for guiding 3D myoblast alignment, elongation, and differentiation. ACS Nano 9, 9167–9179 (2015). https://doi.org/10.1021/acsnano.5b03644
- R. Dong, P.X. Ma, B. Guo, Conductive biomaterials for muscle tissue engineering. Biomaterials 229, 119584 (2020). https://doi.org/10.1016/j.biomaterials.2019.119584
- Y. Liang, L. Qiao, B. Qiao, B. Guo, Conductive hydrogels for tissue repair. Chem. Sci. 14, 3091–3116 (2023). https://doi.org/10.1039/d3sc00145h
- C. Mao, F. Wang, B. Cao, Controlling nanostructures of mesoporous silica fibers by supramolecular assembly of genetically modifiable bacteriophages. Angew. Chem. Int. Ed. 51, 6411–6415 (2012). https://doi.org/10.1002/anie.201107824
- Y. Zhou, Q. Zhao, M. Wang, Biomanufacturing of biomimetic three-dimensional nanofibrous multicellular constructs for tissue regeneration. Colloids Surf. B Biointerfaces 223, 113189 (2023). https://doi.org/10.1016/j.colsurfb.2023.113189
- L. Liu, F. Xu, H. Jin, B. Qiu, J. Yang et al., Integrated manufacturing of suspended and aligned nanofibrous scaffold for structural maturation and synchronous contraction of HiPSC-derived cardiomyocytes. Bioengineering 10, 702 (2023). https://doi.org/10.3390/bioengineering10060702
- T. Jiang, D. Kai, S. Liu, X. Huang, S. Heng et al., Mechanically cartilage-mimicking poly(PCL-PTHF urethane)/collagen nanofibers induce chondrogenesis by blocking NF-kappa B signaling pathway. Biomaterials 178, 281–292 (2018). https://doi.org/10.1016/j.biomaterials.2018.06.023
- B.J. Kwee, D.J. Mooney, Biomaterials for skeletal muscle tissue engineering. Curr. Opin. Biotechnol. 47, 16–22 (2017). https://doi.org/10.1016/j.copbio.2017.05.003
- Y. Zheng, X. Hong, J. Wang, L. Feng, T. Fan et al., 2D nanomaterials for tissue engineering and regenerative nanomedicines: recent advances and future challenges. Adv. Healthc. Mater. 10, e2001743 (2021). https://doi.org/10.1002/adhm.202001743
- X. Wu, T. Tu, Y. Dai, P. Tang, Y. Zhang et al., Direct ink writing of highly conductive MXene frames for tunable electromagnetic interference shielding and electromagnetic wave-induced thermochromism. Nano-Micro Lett. 13, 148 (2021). https://doi.org/10.1007/s40820-021-00665-9
- S. Hao, H. Han, Z. Yang, M. Chen, Y. Jiang et al., Recent advancements on photothermal conversion and antibacterial applications over MXenes-based materials. Nano-Micro Lett. 14, 178 (2022). https://doi.org/10.1007/s40820-022-00901-w
- A. Parihar, A. Singhal, N. Kumar, R. Khan, M.A. Khan et al., Next-generation intelligent MXene-based electrochemical aptasensors for point-of-care cancer diagnostics. Nano-Micro Lett. 14, 100 (2022). https://doi.org/10.1007/s40820-022-00845-1
- T. Xu, Q. Song, K. Liu, H. Liu, J. Pan et al., Nanocellulose-assisted construction of multifunctional MXene-based aerogels with engineering biomimetic texture for pressure sensor and compressible electrode. Nano-Micro Lett. 15, 98 (2023). https://doi.org/10.1007/s40820-023-01073-x
- E. Mostafavi, S. Iravani, MXene-graphene composites: a perspective on biomedical potentials. Nano-Micro Lett. 14, 130 (2022). https://doi.org/10.1007/s40820-022-00880-y
- J. Yin, S. Pan, X. Guo, Y. Gao, D. Zhu et al., Nb2C MXene-functionalized scaffolds enables osteosarcoma phototherapy and angiogenesis/osteogenesis of bone defects. Nano-Micro Lett. 13, 30 (2021). https://doi.org/10.1007/s40820-020-00547-6
- S. Umrao, R. Tabassian, J. Kim, V.H. Nguyen, Q. Zhou et al., MXene artificial muscles based on ionically cross-linked Ti3C2Tx electrode for kinetic soft robotics. Sci. Robot. 4, eaaw7797 (2019). https://doi.org/10.1126/scirobotics.aaw7797
- P. Xue, Y. Chen, Y. Xu, C. Valenzuela, X. Zhang et al., Bioinspired MXene-based soft actuators exhibiting angle-independent structural color. Nano-Micro Lett. 15, 1 (2022). https://doi.org/10.1007/s40820-022-00977-4
- M. Soleymaniha, M.A. Shahbazi, A.R. Rafieerad, A. Maleki, A. Amiri, Promoting role of MXene nanosheets in biomedical sciences: therapeutic and biosensing innovations. Adv. Healthc. Mater. 8, e1801137 (2019). https://doi.org/10.1002/adhm.201801137
- T. Li, J. Ma, W. Wang, B. Lei, Bioactive MXene promoting angiogenesis and skeletal muscle regeneration through regulating M2 polarization and oxidation stress. Adv. Healthc. Mater. 12, e2201862 (2023). https://doi.org/10.1002/adhm.202201862
- S. Boularaoui, A. Shanti, M. Lanotte, S. Luo, S. Bawazir et al., Nanocomposite conductive bioinks based on low-concentration GelMA and MXene nanosheets/gold nanops providing enhanced printability of functional skeletal muscle tissues. ACS Biomater. Sci. Eng. 7, 5810–5822 (2021). https://doi.org/10.1021/acsbiomaterials.1c01193
- M. Khazaei, A. Ranjbar, M. Arai, S. Yunoki, Topological insulators in the ordered double transition metals M2′M′′C2MXenes (M′=Mo, W;M′′=Ti, Zr, Hf). Phys. Rev. B 94, 125152 (2016). https://doi.org/10.1103/physrevb.94.125152
- Z.-Q. Huang, M.-L. Xu, G. Macam, C.-H. Hsu, F.-C. Chuang, Large-gap topological insulators in functionalized ordered double transition metal carbide MXenes. Phys. Rev. B 102, 075306 (2020). https://doi.org/10.1103/physrevb.102.075306
- I. Persson, L.-Å. Näslund, J. Halim, M.W. Barsoum, V. Darakchieva et al., On the organization and thermal behavior of functional groups on Ti3C2 MXene surfaces in vacuum. 2D Mater. 5, 015002 (2017). https://doi.org/10.1088/2053-1583/aa89cd
- N.C. Osti, M. Naguib, A. Ostadhossein, Y. Xie, P.R. Kent et al., Effect of metal ion intercalation on the structure of MXene and water dynamics on its internal surfaces. ACS Appl. Mater. Interfaces 8, 8859–8863 (2016). https://doi.org/10.1021/acsami.6b01490
- S. Goodwin, J.D. McPherson, W.R. McCombie, Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333–351 (2016). https://doi.org/10.1038/nrg.2016.49
- S.C. Schuster, Next-generation sequencing transforms today’s biology. Nat. Methods 5, 16–18 (2008). https://doi.org/10.1038/nmeth1156
- S.H. Lee, S. Jeon, X. Qu, M.S. Kang, J.H. Lee et al., Ternary MXene-loaded PLCL/collagen nanofibrous scaffolds that promote spontaneous osteogenic differentiation. Nano Converg. 9, 38 (2022). https://doi.org/10.1186/s40580-022-00329-3
- Y.B. Lee, S.-J. Song, Y.C. Shin, Y.J. Jung, B. Kim et al., Ternary nanofiber matrices composed of PCL/black phosphorus/collagen to enhance osteodifferentiation. J. Ind. Eng. Chem. 80, 802–810 (2019). https://doi.org/10.1016/j.jiec.2019.06.055
- D. Szklarczyk, A.L. Gable, D. Lyon, A. Junge, S. Wyder et al., STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019). https://doi.org/10.1093/nar/gky1131
- P. Shannon, A. Markiel, O. Ozier, N.S. Baliga, J.T. Wang et al., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003). https://doi.org/10.1101/gr.1239303
- T. Wu, E. Hu, S. Xu, M. Chen, P. Guo et al., clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021). https://doi.org/10.1016/j.xinn.2021.100141
- S. Iravani, R.S. Varma, MXene-based composites as nanozymes in biomedicine: a perspective. Nano-Micro Lett. 14, 213 (2022). https://doi.org/10.1007/s40820-022-00958-7
- G. Wang, X. Shen, B. Wang, J. Yao, J. Park, Synthesis and characterisation of hydrophilic and organophilic graphene nanosheets. Carbon 47, 1359–1364 (2009). https://doi.org/10.1016/j.carbon.2009.01.027
- M. Alhabeb, K. Maleski, B. Anasori, P. Lelyukh, L. Clark et al., Guidelines for Synthesis and Processing of Two-Dimensional Titanium Carbide (Ti3C2Tx MXene). MXenes (Jenny Stanford Publishing, New York, 2023), pp.415–449. https://doi.org/10.1201/9781003306511-21
- K.S. Novoselov, A.K. Geim, S.V. Morozov, D. Jiang, Y. Zhang et al., Electric field effect in atomically thin carbon films. Science 306, 666–669 (2004). https://doi.org/10.1126/science.1102896
- S.P. Koenig, R.A. Doganov, H. Schmidt, A.H. Castro Neto, B. Özyilmaz, Electric field effect in ultrathin black phosphorus. Appl. Phys. Lett. 104, 103106 (2014). https://doi.org/10.1063/1.4868132
- X. Sang, Y. Xie, M.W. Lin, M. Alhabeb, K.L. Van Aken et al., Atomic defects in monolayer titanium carbide (Ti3C2Tx) MXene. ACS Nano 10, 9193–9200 (2016). https://doi.org/10.1021/acsnano.6b05240
- S.Y. Chae, R. Park, S.W. Hong, Surface-mediated high antioxidant and anti-inflammatory effects of astaxanthin-loaded ultrathin graphene oxide film that inhibits the overproduction of intracellular reactive oxygen species. Biomater. Res. 26, 30 (2022). https://doi.org/10.1186/s40824-022-00276-4
- S.H. Kang, Y.C. Shin, E.Y. Hwang, J.H. Lee, C.-S. Kim et al., Engineered “coffee-rings” of reduced graphene oxide as ultrathin contact guidance to enable patterning of living cells. Mater. Horiz. 6, 1066–1079 (2019). https://doi.org/10.1039/C8MH01381K
- M. Seredych, K. Maleski, T.S. Mathis, Y. Gogotsi, Delamination of MXenes using bovine serum albumin. Colloids Surf. A Physicochem. Eng. Aspects 641, 128580 (2022). https://doi.org/10.1016/j.colsurfa.2022.128580
- J. Sun, Q. Mu, T. Wang, J. Qi, C. Hu, Selective electrosorption of Ca2+ by MXene cathodes coupled with NiAl-LMO anodes through ion intercalation. J. Colloid Interface Sci. 590, 539–547 (2021). https://doi.org/10.1016/j.jcis.2021.01.058
- J. Cao, J. Li, D. Li, Z. Yuan, Y. Zhang et al., Strongly coupled 2D transition metal chalcogenide-MXene-carbonaceous nanoribbon heterostructures with ultrafast ion transport for boosting sodium/potassium ions storage. Nano-Micro Lett. 13, 113 (2021). https://doi.org/10.1007/s40820-021-00623-5
- K. Rasool, M. Helal, A. Ali, C.E. Ren, Y. Gogotsi et al., Antibacterial activity of Ti3C2Tx MXene. ACS Nano 10, 3674–3684 (2016). https://doi.org/10.1021/acsnano.6b00181
- S.H. Ku, C.B. Park, Myoblast differentiation on graphene oxide. Biomaterials 34, 2017–2023 (2013). https://doi.org/10.1016/j.biomaterials.2012.11.052
- J.N. Artaza, S. Bhasin, C. Mallidis, W. Taylor, K. Ma et al., Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells. J. Cell. Physiol. 190, 170–179 (2002). https://doi.org/10.1002/jcp.10044
- A.R. Gillies, R.L. Lieber, Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44, 318–331 (2011). https://doi.org/10.1002/mus.22094
- L. Chen, E. Bonaccurso, Effects of surface wettability and liquid viscosity on the dynamic wetting of individual drops. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 90, 022401 (2014). https://doi.org/10.1103/PhysRevE.90.022401
- J. Pelipenko, P. Kocbek, J. Kristl, Nanofiber diameter as a critical parameter affecting skin cell response. Eur. J. Pharm. Sci. 66, 29–35 (2015). https://doi.org/10.1016/j.ejps.2014.09.022
- J.M. Dang, K.W. Leong, Myogenic induction of aligned mesenchymal stem cell sheets by culture on thermally responsive electrospun nanofibers. Adv. Mater. 19, 2775–2779 (2007). https://doi.org/10.1002/adma.200602159
- K.H. Lee, G.H. Kwon, S.J. Shin, J.Y. Baek, D.K. Han et al., Hydrophilic electrospun polyurethane nanofiber matrices for hMSC culture in a microfluidic cell chip. J. Biomed. Mater. Res. A 90, 619–628 (2009). https://doi.org/10.1002/jbm.a.32059
- I. Sousa, A. Mendes, R.F. Pereira, P.J. Bártolo, Collagen surface modified poly(ε-caprolactone) scaffolds with improved hydrophilicity and cell adhesion properties. Mater. Lett. 134, 263–267 (2014). https://doi.org/10.1016/j.matlet.2014.06.132
- L. Zhang, W. Su, Y. Huang, H. Li, L. Fu et al., In situ high-pressure X-ray diffraction and Raman spectroscopy study of Ti3C2Tx MXene. Nanoscale Res. Lett. 13, 343 (2018). https://doi.org/10.1186/s11671-018-2746-4
- D. Qu, Y. Jian, L. Guo, C. Su, N. Tang et al., An organic solvent-assisted intercalation and collection (OAIC) for Ti3C2Tx MXene with controllable sizes and improved yield. Nano-Micro Lett. 13, 188 (2021). https://doi.org/10.1007/s40820-021-00705-4
- F. Liu, X. Liao, C. Liu, M. Li, Y. Chen et al., Poly(l-lactide-co-caprolactone)/tussah silk fibroin nanofiber vascular scaffolds with small diameter fabricated by core-spun electrospinning technology. J. Mater. Sci. 55, 7106–7119 (2020). https://doi.org/10.1007/s10853-020-04510-z
- K. Garkhal, S. Verma, S. Jonnalagadda, N. Kumar, Fast degradable poly(L-lactide-co-ε-caprolactone) microspheres for tissue engineering: synthesis, characterization, and degradation behavior. J. Polym. Sci. A Polym. Chem. 45, 2755–2764 (2007). https://doi.org/10.1002/pola.22031
- A. Rafieerad, W. Yan, G.L. Sequiera, N. Sareen, E. Abu-El-Rub et al., Application of Ti3C2 MXene quantum dots for immunomodulation and regenerative medicine. Adv. Healthc. Mater. 8, e1900569 (2019). https://doi.org/10.1002/adhm.201900569
- A. Sengupta, B.V. Bhaskara Rao, N. Sharma, S. Parmar, V. Chavan et al., Comparative evaluation of MAX, MXene, NanoMAX, and NanoMAX-derived-MXene for microwave absorption and Li ion battery anode applications. Nanoscale 12, 8466–8476 (2020). https://doi.org/10.1039/c9nr10980c
- M.S. Rizvi, P. Kumar, D.S. Katti, A. Pal, Mathematical model of mechanical behavior of micro/nanofibrous materials designed for extracellular matrix substitutes. Acta Biomater. 8, 4111–4122 (2012). https://doi.org/10.1016/j.actbio.2012.07.025
- S.R. Goodyear, R.M. Aspden, Mechanical properties of bone ex vivo, in Bone Research Protocols. ed. by M.H. Helfrich, S.H. Ralston (Humana Press, Totowa, 2012), pp.555–571. https://doi.org/10.1007/978-1-61779-415-5_35
- M. Akhmanova, E. Osidak, S. Domogatsky, S. Rodin, A. Domogatskaya, Physical, spatial, and molecular aspects of extracellular matrix of in vivo niches and artificial scaffolds relevant to stem cells research. Stem Cells Int. 2015, 167025 (2015). https://doi.org/10.1155/2015/167025
- L. Geddes, L. Carson, E. Themistou, F. Buchanan, A comparison of the increased temperature accelerated degradation of Poly(,-lactide-co-glycolide) and Poly (-lactide-co-glycolide). Polym. Test. 91, 106853 (2020). https://doi.org/10.1016/j.polymertesting.2020.106853
- J. Jokinen, E. Dadu, P. Nykvist, J. Käpylä, D.J. White et al., Integrin-mediated cell adhesion to type I collagen fibrils. J. Biol. Chem. 279, 31956–31963 (2004). https://doi.org/10.1074/jbc.M401409200
- L.T. Denes, L.A. Riley, J.R. Mijares, J.D. Arboleda, K. McKee et al., Culturing C2C12 myotubes on micromolded gelatin hydrogels accelerates myotube maturation. Skelet. Muscle 9, 17 (2019). https://doi.org/10.1186/s13395-019-0203-4
- M.A. Schwartz, R.K. Assoian, Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 114, 2553–2560 (2001). https://doi.org/10.1242/jcs.114.14.2553
- B.M. Sicari, V. Agrawal, B.F. Siu, C.J. Medberry, C.L. Dearth et al., A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng. Part A 18, 1941–1948 (2012). https://doi.org/10.1089/ten.TEA.2012.0475
- N.J. Turner, A.J. Yates Jr., D.J. Weber, I.R. Qureshi, D.B. Stolz et al., Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng. Part A 16, 3309–3317 (2010). https://doi.org/10.1089/ten.TEA.2010.0169
- B.M. Sicari, J.P. Rubin, C.L. Dearth, M.T. Wolf, F. Ambrosio et al., An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6, 234ra58 (2014). https://doi.org/10.1126/scitranslmed.3008085
- V.J. Mase Jr., J.R. Hsu, S.E. Wolf, J.C. Wenke, D.G. Baer et al., Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33, 511 (2010). https://doi.org/10.3928/01477447-20100526-24
- Y. Jin, E.J. Jeon, S. Jeong, S. Min, Y.S. Choi et al., Reconstruction of muscle fascicle-like tissues by anisotropic 3D patterning. Adv. Funct. Mater. 31, 2006227 (2021). https://doi.org/10.1002/adfm.202006227
- Y. Jin, D. Shahriari, E.J. Jeon, S. Park, Y.S. Choi et al., Functional skeletal muscle regeneration with thermally drawn porous fibers and reprogrammed muscle progenitors for volumetric muscle injury. Adv. Mater. 33, e2007946 (2021). https://doi.org/10.1002/adma.202007946
- N.E. Gentile, K.M. Stearns, E.H. Brown, J.P. Rubin, M.L. Boninger et al., Targeted rehabilitation after extracellular matrix scaffold transplantation for the treatment of volumetric muscle loss. Am. J. Phys. Med. Rehabil. 93, S79–S87 (2014). https://doi.org/10.1097/PHM.0000000000000145
- B.N. Brown, J.E. Valentin, A.M. Stewart-Akers, G.P. McCabe, S.F. Badylak, Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30, 1482–1491 (2009). https://doi.org/10.1016/j.biomaterials.2008.11.040
- P. Heher, B. Maleiner, J. Prüller, A.H. Teuschl, J. Kollmitzer et al., A novel bioreactor for the generation of highly aligned 3D skeletal muscle-like constructs through orientation of fibrin via application of static strain. Acta Biomater. 24, 251–265 (2015). https://doi.org/10.1016/j.actbio.2015.06.033
- R. Raman, L. Grant, Y. Seo, C. Cvetkovic, M. Gapinske et al., Damage, healing, and remodeling in optogenetic skeletal muscle bioactuators. Adv. Healthc. Mater. 6, 201700030 (2017). https://doi.org/10.1002/adhm.201700030
- E. Ko, O. Aydin, Z. Li, L. Gapinske, K.-Y. Huang et al., Empowering engineered muscle in biohybrid pump by extending connexin 43 duration with reduced graphene oxides. Biomaterials 287, 121643 (2022). https://doi.org/10.1016/j.biomaterials.2022.121643
- H. Nakazawa, K. Chang, S. Shinozaki, T. Yasukawa, K. Ishimaru et al., iNOS as a driver of inflammation and apoptosis in mouse skeletal muscle after burn injury: possible involvement of Sirt1 S-nitrosylation-mediated acetylation of p65 NF-κB and p53. PLoS ONE 12, e0170391 (2017). https://doi.org/10.1371/journal.pone.0170391
- S. Schiaffino, C. Mammucari, Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1, 4 (2011). https://doi.org/10.1186/2044-5040-1-4
- E. Andres-Mateos, H. Brinkmeier, T.N. Burks, R. Mejias, D.C. Files et al., Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol. Med. 5, 80–91 (2013). https://doi.org/10.1002/emmm.201201443
- J. Massenet, E. Gardner, B. Chazaud, F.J. Dilworth, Epigenetic regulation of satellite cell fate during skeletal muscle regeneration. Skelet. Muscle 11, 4 (2021). https://doi.org/10.1186/s13395-020-00259-w
- M.K. Tu, J.B. Levin, A.M. Hamilton, L.N. Borodinsky, Calcium signaling in skeletal muscle development, maintenance and regeneration. Cell Calcium 59, 91–97 (2016). https://doi.org/10.1016/j.ceca.2016.02.005
- D.R. Brickley, A.S. Agyeman, R.F. Kopp, B.A. Hall, M.C. Harbeck et al., Serum- and glucocorticoid-induced protein kinase 1 (SGK1) is regulated by store-operated Ca2+ entry and mediates cytoprotection against necrotic cell death. J. Biol. Chem. 288, 32708–32719 (2013). https://doi.org/10.1074/jbc.M113.507210
- J.M. García-Martínez, D.R. Alessi, mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 416, 375–385 (2008). https://doi.org/10.1042/BJ20081668
- E.A. Ivakine, R.D. Cohn, Maintaining skeletal muscle mass: lessons learned from hibernation. Exp. Physiol. 99, 632–637 (2014). https://doi.org/10.1113/expphysiol.2013.074344
- J. Luo, A. Liang, M. Liang, R. Xia, Y. Rizvi et al., Serum glucocorticoid-regulated kinase 1 blocks CKD-induced muscle wasting via inactivation of FoxO3a and Smad2/3. J Am Soc Nephrol 27, 2797–2808 (2016). https://doi.org/10.1681/ASN.2015080867
- Q. Xue, Y. Yan, R. Zhang, H. Xiong, Regulation of iNOS on immune cells and its role in diseases. Int. J. Mol. Sci. 19, 3805 (2018). https://doi.org/10.3390/ijms19123805
- Y. Yu, H. Sun, Q. Lu, J. Sun, P. Zhang et al., Spontaneous formation of MXene-oxidized sono/chemo-dynamic sonosensitizer/nanocatalyst for antibacteria and bone-tissue regeneration. J. Nanobiotechnol. 21, 193 (2023). https://doi.org/10.1186/s12951-023-01933-z
- N.C. Sibisi, C. Snyman, K.H. Myburgh, C.U. Niesler, Evaluating the role of nitric oxide in myogenesis in vitro. Biochimie 196, 216–224 (2022). https://doi.org/10.1016/j.biochi.2021.11.006
- E. Rigamonti, T. Touvier, E. Clementi, A.A. Manfredi, S. Brunelli et al., Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage. J. Immunol. 190, 1767–1777 (2013). https://doi.org/10.4049/jimmunol.1202903
- M. Yamada, Y. Sankoda, R. Tatsumi, W. Mizunoya, Y. Ikeuchi et al., Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int. J. Biochem. Cell Biol. 40, 2183–2191 (2008). https://doi.org/10.1016/j.biocel.2008.02.017
- X. Chen, Y. Li, Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh. Migr. 3, 337–341 (2009). https://doi.org/10.4161/cam.3.4.9338
- S. Hayashi, H. Aso, K. Watanabe, H. Nara, M.T. Rose et al., Sequence of IGF-I, IGF-II, and HGF expression in regenerating skeletal muscle. Histochem. Cell Biol. 122, 427–434 (2004). https://doi.org/10.1007/s00418-004-0704-y
- P. Kaliman, F. Viñals, X. Testar, M. Palacín, A. Zorzano, Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271, 19146–19151 (1996). https://doi.org/10.1074/jbc.271.32.19146
- R. Kornasio, I. Riederer, G. Butler-Browne, V. Mouly, Z. Uni et al., Beta-hydroxy-beta-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim. Biophys. Acta 1793, 755–763 (2009). https://doi.org/10.1016/j.bbamcr.2008.12.017
- M. Ma, X. Wang, X. Chen, R. Cai, F. Chen et al., microRNA-432 targeting E2F3 and P55PIK inhibits myogenesis through PI3K/AKT/mTOR signaling pathway. RNA Biol. 14, 347–360 (2017). https://doi.org/10.1080/15476286.2017.1279786
- J. Kim, M.Y. Park, H.K. Kim, Y. Park, K.Y. Whang, Cortisone and dexamethasone inhibit myogenesis by modulating the AKT/mTOR signaling pathway in C2C12. Biosci. Biotechnol. Biochem. 80, 2093–2099 (2016). https://doi.org/10.1080/09168451.2016.1210502
- Kshitiz, J. Park, P. Kim, W. Helen, A.J. Engler et al., Control of stem cell fate and function by engineering physical microenvironments. Integr. Biol. 4, 1008–1018 (2012). https://doi.org/10.1039/c2ib20080e
- C. Leclech, A.I. Barakat, Is there a universal mechanism of cell alignment in response to substrate topography? Cytoskeleton 78, 284–292 (2021). https://doi.org/10.1002/cm.21661
- M.T. Lam, S. Sim, X. Zhu, S. Takayama, The effect of continuous wavy micropatterns on silicone substrates on the alignment of skeletal muscle myoblasts and myotubes. Biomaterials 27, 4340–4347 (2006). https://doi.org/10.1016/j.biomaterials.2006.04.012
- M.T. Lam, Y.-C. Huang, R.K. Birla, S. Takayama, Microfeature guided skeletal muscle tissue engineering for highly organized 3-dimensional free-standing constructs. Biomaterials 30, 1150–1155 (2009). https://doi.org/10.1016/j.biomaterials.2008.11.014
- D.G. Farwell, K.A. Shera, J.I. Koop, G.A. Bonnet, C.P. Matthews et al., Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am. J. Pathol. 156, 1537–1547 (2000). https://doi.org/10.1016/S0002-9440(10)65025-0
- R. Foulkes, E. Man, J. Thind, S. Yeung, A. Joy et al., The regulation of nanomaterials and nanomedicines for clinical application: current and future perspectives. Biomater. Sci. 8, 4653–4664 (2020). https://doi.org/10.1039/d0bm00558d
References
B.F. Grogan, J.R. Hsu, Volumetric muscle loss. Am. Acad. Orthop. Surg. 19, S35–S37 (2011). https://doi.org/10.5435/00124635-201102001-00007
S. Tamai, S. Komatsu, H. Sakamoto, S. Sano, N. Sasauchi, Free muscle transplants in dogs, with microsurgical neurovascular anastomoses. Plast. Reconstr. Surg. 46, 219–225 (1970). https://doi.org/10.1097/00006534-197009000-00002
K. Doi, Y. Arakawa, Y. Hattori, A.S. Baliarsing, Restoration of elbow flexion with functioning free muscle transfer in arthrogryposis: a report of two cases. J. Bone Joint Surg. Am. 93, e105 (2011). https://doi.org/10.2106/JBJS.J.01846
T.C. Burns, D.J. Stinner, D.R. Possley, A.W. Mack, T.T. Eckel et al., Does the zone of injury in combat-related type III open tibia fractures preclude the use of local soft tissue coverage? J. Orthop. Trauma 24, 697–703 (2010). https://doi.org/10.1097/BOT.0b013e3181d048b8
J.G. Owens, J.A. Blair, J.C. Patzkowski, R.V. Blanck, J.R. Hsu, Return to running and sports participation after limb salvage. J. Trauma Inj. Infect. Crit. Care 71, S120–S124 (2011). https://doi.org/10.1097/ta.0b013e3182219225
J.C. Patzkowski, R.V. Blanck, J.G. Owens, J.M. Wilken, J.A. Blair et al., Can an ankle-foot orthosis change hearts and minds? J. Surg. Orthop. Adv. 20, 8–18 (2011)
S. Ostrovidov, V. Hosseini, S. Ahadian, T. Fujie, S.P. Parthiban et al., Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng. Part B Rev. 20, 403–436 (2014). https://doi.org/10.1089/ten.TEB.2013.0534
R. Yu, H. Zhang, B. Guo, Conductive biomaterials as bioactive wound dressing for wound healing and skin tissue engineering. Nano-Micro Lett. 14, 1 (2021). https://doi.org/10.1007/s40820-021-00751-y
L. Wang, Y. Wu, B. Guo, P.X. Ma, Nanofiber yarn/hydrogel core-shell scaffolds mimicking native skeletal muscle tissue for guiding 3D myoblast alignment, elongation, and differentiation. ACS Nano 9, 9167–9179 (2015). https://doi.org/10.1021/acsnano.5b03644
R. Dong, P.X. Ma, B. Guo, Conductive biomaterials for muscle tissue engineering. Biomaterials 229, 119584 (2020). https://doi.org/10.1016/j.biomaterials.2019.119584
Y. Liang, L. Qiao, B. Qiao, B. Guo, Conductive hydrogels for tissue repair. Chem. Sci. 14, 3091–3116 (2023). https://doi.org/10.1039/d3sc00145h
C. Mao, F. Wang, B. Cao, Controlling nanostructures of mesoporous silica fibers by supramolecular assembly of genetically modifiable bacteriophages. Angew. Chem. Int. Ed. 51, 6411–6415 (2012). https://doi.org/10.1002/anie.201107824
Y. Zhou, Q. Zhao, M. Wang, Biomanufacturing of biomimetic three-dimensional nanofibrous multicellular constructs for tissue regeneration. Colloids Surf. B Biointerfaces 223, 113189 (2023). https://doi.org/10.1016/j.colsurfb.2023.113189
L. Liu, F. Xu, H. Jin, B. Qiu, J. Yang et al., Integrated manufacturing of suspended and aligned nanofibrous scaffold for structural maturation and synchronous contraction of HiPSC-derived cardiomyocytes. Bioengineering 10, 702 (2023). https://doi.org/10.3390/bioengineering10060702
T. Jiang, D. Kai, S. Liu, X. Huang, S. Heng et al., Mechanically cartilage-mimicking poly(PCL-PTHF urethane)/collagen nanofibers induce chondrogenesis by blocking NF-kappa B signaling pathway. Biomaterials 178, 281–292 (2018). https://doi.org/10.1016/j.biomaterials.2018.06.023
B.J. Kwee, D.J. Mooney, Biomaterials for skeletal muscle tissue engineering. Curr. Opin. Biotechnol. 47, 16–22 (2017). https://doi.org/10.1016/j.copbio.2017.05.003
Y. Zheng, X. Hong, J. Wang, L. Feng, T. Fan et al., 2D nanomaterials for tissue engineering and regenerative nanomedicines: recent advances and future challenges. Adv. Healthc. Mater. 10, e2001743 (2021). https://doi.org/10.1002/adhm.202001743
X. Wu, T. Tu, Y. Dai, P. Tang, Y. Zhang et al., Direct ink writing of highly conductive MXene frames for tunable electromagnetic interference shielding and electromagnetic wave-induced thermochromism. Nano-Micro Lett. 13, 148 (2021). https://doi.org/10.1007/s40820-021-00665-9
S. Hao, H. Han, Z. Yang, M. Chen, Y. Jiang et al., Recent advancements on photothermal conversion and antibacterial applications over MXenes-based materials. Nano-Micro Lett. 14, 178 (2022). https://doi.org/10.1007/s40820-022-00901-w
A. Parihar, A. Singhal, N. Kumar, R. Khan, M.A. Khan et al., Next-generation intelligent MXene-based electrochemical aptasensors for point-of-care cancer diagnostics. Nano-Micro Lett. 14, 100 (2022). https://doi.org/10.1007/s40820-022-00845-1
T. Xu, Q. Song, K. Liu, H. Liu, J. Pan et al., Nanocellulose-assisted construction of multifunctional MXene-based aerogels with engineering biomimetic texture for pressure sensor and compressible electrode. Nano-Micro Lett. 15, 98 (2023). https://doi.org/10.1007/s40820-023-01073-x
E. Mostafavi, S. Iravani, MXene-graphene composites: a perspective on biomedical potentials. Nano-Micro Lett. 14, 130 (2022). https://doi.org/10.1007/s40820-022-00880-y
J. Yin, S. Pan, X. Guo, Y. Gao, D. Zhu et al., Nb2C MXene-functionalized scaffolds enables osteosarcoma phototherapy and angiogenesis/osteogenesis of bone defects. Nano-Micro Lett. 13, 30 (2021). https://doi.org/10.1007/s40820-020-00547-6
S. Umrao, R. Tabassian, J. Kim, V.H. Nguyen, Q. Zhou et al., MXene artificial muscles based on ionically cross-linked Ti3C2Tx electrode for kinetic soft robotics. Sci. Robot. 4, eaaw7797 (2019). https://doi.org/10.1126/scirobotics.aaw7797
P. Xue, Y. Chen, Y. Xu, C. Valenzuela, X. Zhang et al., Bioinspired MXene-based soft actuators exhibiting angle-independent structural color. Nano-Micro Lett. 15, 1 (2022). https://doi.org/10.1007/s40820-022-00977-4
M. Soleymaniha, M.A. Shahbazi, A.R. Rafieerad, A. Maleki, A. Amiri, Promoting role of MXene nanosheets in biomedical sciences: therapeutic and biosensing innovations. Adv. Healthc. Mater. 8, e1801137 (2019). https://doi.org/10.1002/adhm.201801137
T. Li, J. Ma, W. Wang, B. Lei, Bioactive MXene promoting angiogenesis and skeletal muscle regeneration through regulating M2 polarization and oxidation stress. Adv. Healthc. Mater. 12, e2201862 (2023). https://doi.org/10.1002/adhm.202201862
S. Boularaoui, A. Shanti, M. Lanotte, S. Luo, S. Bawazir et al., Nanocomposite conductive bioinks based on low-concentration GelMA and MXene nanosheets/gold nanops providing enhanced printability of functional skeletal muscle tissues. ACS Biomater. Sci. Eng. 7, 5810–5822 (2021). https://doi.org/10.1021/acsbiomaterials.1c01193
M. Khazaei, A. Ranjbar, M. Arai, S. Yunoki, Topological insulators in the ordered double transition metals M2′M′′C2MXenes (M′=Mo, W;M′′=Ti, Zr, Hf). Phys. Rev. B 94, 125152 (2016). https://doi.org/10.1103/physrevb.94.125152
Z.-Q. Huang, M.-L. Xu, G. Macam, C.-H. Hsu, F.-C. Chuang, Large-gap topological insulators in functionalized ordered double transition metal carbide MXenes. Phys. Rev. B 102, 075306 (2020). https://doi.org/10.1103/physrevb.102.075306
I. Persson, L.-Å. Näslund, J. Halim, M.W. Barsoum, V. Darakchieva et al., On the organization and thermal behavior of functional groups on Ti3C2 MXene surfaces in vacuum. 2D Mater. 5, 015002 (2017). https://doi.org/10.1088/2053-1583/aa89cd
N.C. Osti, M. Naguib, A. Ostadhossein, Y. Xie, P.R. Kent et al., Effect of metal ion intercalation on the structure of MXene and water dynamics on its internal surfaces. ACS Appl. Mater. Interfaces 8, 8859–8863 (2016). https://doi.org/10.1021/acsami.6b01490
S. Goodwin, J.D. McPherson, W.R. McCombie, Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333–351 (2016). https://doi.org/10.1038/nrg.2016.49
S.C. Schuster, Next-generation sequencing transforms today’s biology. Nat. Methods 5, 16–18 (2008). https://doi.org/10.1038/nmeth1156
S.H. Lee, S. Jeon, X. Qu, M.S. Kang, J.H. Lee et al., Ternary MXene-loaded PLCL/collagen nanofibrous scaffolds that promote spontaneous osteogenic differentiation. Nano Converg. 9, 38 (2022). https://doi.org/10.1186/s40580-022-00329-3
Y.B. Lee, S.-J. Song, Y.C. Shin, Y.J. Jung, B. Kim et al., Ternary nanofiber matrices composed of PCL/black phosphorus/collagen to enhance osteodifferentiation. J. Ind. Eng. Chem. 80, 802–810 (2019). https://doi.org/10.1016/j.jiec.2019.06.055
D. Szklarczyk, A.L. Gable, D. Lyon, A. Junge, S. Wyder et al., STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019). https://doi.org/10.1093/nar/gky1131
P. Shannon, A. Markiel, O. Ozier, N.S. Baliga, J.T. Wang et al., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003). https://doi.org/10.1101/gr.1239303
T. Wu, E. Hu, S. Xu, M. Chen, P. Guo et al., clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation 2, 100141 (2021). https://doi.org/10.1016/j.xinn.2021.100141
S. Iravani, R.S. Varma, MXene-based composites as nanozymes in biomedicine: a perspective. Nano-Micro Lett. 14, 213 (2022). https://doi.org/10.1007/s40820-022-00958-7
G. Wang, X. Shen, B. Wang, J. Yao, J. Park, Synthesis and characterisation of hydrophilic and organophilic graphene nanosheets. Carbon 47, 1359–1364 (2009). https://doi.org/10.1016/j.carbon.2009.01.027
M. Alhabeb, K. Maleski, B. Anasori, P. Lelyukh, L. Clark et al., Guidelines for Synthesis and Processing of Two-Dimensional Titanium Carbide (Ti3C2Tx MXene). MXenes (Jenny Stanford Publishing, New York, 2023), pp.415–449. https://doi.org/10.1201/9781003306511-21
K.S. Novoselov, A.K. Geim, S.V. Morozov, D. Jiang, Y. Zhang et al., Electric field effect in atomically thin carbon films. Science 306, 666–669 (2004). https://doi.org/10.1126/science.1102896
S.P. Koenig, R.A. Doganov, H. Schmidt, A.H. Castro Neto, B. Özyilmaz, Electric field effect in ultrathin black phosphorus. Appl. Phys. Lett. 104, 103106 (2014). https://doi.org/10.1063/1.4868132
X. Sang, Y. Xie, M.W. Lin, M. Alhabeb, K.L. Van Aken et al., Atomic defects in monolayer titanium carbide (Ti3C2Tx) MXene. ACS Nano 10, 9193–9200 (2016). https://doi.org/10.1021/acsnano.6b05240
S.Y. Chae, R. Park, S.W. Hong, Surface-mediated high antioxidant and anti-inflammatory effects of astaxanthin-loaded ultrathin graphene oxide film that inhibits the overproduction of intracellular reactive oxygen species. Biomater. Res. 26, 30 (2022). https://doi.org/10.1186/s40824-022-00276-4
S.H. Kang, Y.C. Shin, E.Y. Hwang, J.H. Lee, C.-S. Kim et al., Engineered “coffee-rings” of reduced graphene oxide as ultrathin contact guidance to enable patterning of living cells. Mater. Horiz. 6, 1066–1079 (2019). https://doi.org/10.1039/C8MH01381K
M. Seredych, K. Maleski, T.S. Mathis, Y. Gogotsi, Delamination of MXenes using bovine serum albumin. Colloids Surf. A Physicochem. Eng. Aspects 641, 128580 (2022). https://doi.org/10.1016/j.colsurfa.2022.128580
J. Sun, Q. Mu, T. Wang, J. Qi, C. Hu, Selective electrosorption of Ca2+ by MXene cathodes coupled with NiAl-LMO anodes through ion intercalation. J. Colloid Interface Sci. 590, 539–547 (2021). https://doi.org/10.1016/j.jcis.2021.01.058
J. Cao, J. Li, D. Li, Z. Yuan, Y. Zhang et al., Strongly coupled 2D transition metal chalcogenide-MXene-carbonaceous nanoribbon heterostructures with ultrafast ion transport for boosting sodium/potassium ions storage. Nano-Micro Lett. 13, 113 (2021). https://doi.org/10.1007/s40820-021-00623-5
K. Rasool, M. Helal, A. Ali, C.E. Ren, Y. Gogotsi et al., Antibacterial activity of Ti3C2Tx MXene. ACS Nano 10, 3674–3684 (2016). https://doi.org/10.1021/acsnano.6b00181
S.H. Ku, C.B. Park, Myoblast differentiation on graphene oxide. Biomaterials 34, 2017–2023 (2013). https://doi.org/10.1016/j.biomaterials.2012.11.052
J.N. Artaza, S. Bhasin, C. Mallidis, W. Taylor, K. Ma et al., Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells. J. Cell. Physiol. 190, 170–179 (2002). https://doi.org/10.1002/jcp.10044
A.R. Gillies, R.L. Lieber, Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 44, 318–331 (2011). https://doi.org/10.1002/mus.22094
L. Chen, E. Bonaccurso, Effects of surface wettability and liquid viscosity on the dynamic wetting of individual drops. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 90, 022401 (2014). https://doi.org/10.1103/PhysRevE.90.022401
J. Pelipenko, P. Kocbek, J. Kristl, Nanofiber diameter as a critical parameter affecting skin cell response. Eur. J. Pharm. Sci. 66, 29–35 (2015). https://doi.org/10.1016/j.ejps.2014.09.022
J.M. Dang, K.W. Leong, Myogenic induction of aligned mesenchymal stem cell sheets by culture on thermally responsive electrospun nanofibers. Adv. Mater. 19, 2775–2779 (2007). https://doi.org/10.1002/adma.200602159
K.H. Lee, G.H. Kwon, S.J. Shin, J.Y. Baek, D.K. Han et al., Hydrophilic electrospun polyurethane nanofiber matrices for hMSC culture in a microfluidic cell chip. J. Biomed. Mater. Res. A 90, 619–628 (2009). https://doi.org/10.1002/jbm.a.32059
I. Sousa, A. Mendes, R.F. Pereira, P.J. Bártolo, Collagen surface modified poly(ε-caprolactone) scaffolds with improved hydrophilicity and cell adhesion properties. Mater. Lett. 134, 263–267 (2014). https://doi.org/10.1016/j.matlet.2014.06.132
L. Zhang, W. Su, Y. Huang, H. Li, L. Fu et al., In situ high-pressure X-ray diffraction and Raman spectroscopy study of Ti3C2Tx MXene. Nanoscale Res. Lett. 13, 343 (2018). https://doi.org/10.1186/s11671-018-2746-4
D. Qu, Y. Jian, L. Guo, C. Su, N. Tang et al., An organic solvent-assisted intercalation and collection (OAIC) for Ti3C2Tx MXene with controllable sizes and improved yield. Nano-Micro Lett. 13, 188 (2021). https://doi.org/10.1007/s40820-021-00705-4
F. Liu, X. Liao, C. Liu, M. Li, Y. Chen et al., Poly(l-lactide-co-caprolactone)/tussah silk fibroin nanofiber vascular scaffolds with small diameter fabricated by core-spun electrospinning technology. J. Mater. Sci. 55, 7106–7119 (2020). https://doi.org/10.1007/s10853-020-04510-z
K. Garkhal, S. Verma, S. Jonnalagadda, N. Kumar, Fast degradable poly(L-lactide-co-ε-caprolactone) microspheres for tissue engineering: synthesis, characterization, and degradation behavior. J. Polym. Sci. A Polym. Chem. 45, 2755–2764 (2007). https://doi.org/10.1002/pola.22031
A. Rafieerad, W. Yan, G.L. Sequiera, N. Sareen, E. Abu-El-Rub et al., Application of Ti3C2 MXene quantum dots for immunomodulation and regenerative medicine. Adv. Healthc. Mater. 8, e1900569 (2019). https://doi.org/10.1002/adhm.201900569
A. Sengupta, B.V. Bhaskara Rao, N. Sharma, S. Parmar, V. Chavan et al., Comparative evaluation of MAX, MXene, NanoMAX, and NanoMAX-derived-MXene for microwave absorption and Li ion battery anode applications. Nanoscale 12, 8466–8476 (2020). https://doi.org/10.1039/c9nr10980c
M.S. Rizvi, P. Kumar, D.S. Katti, A. Pal, Mathematical model of mechanical behavior of micro/nanofibrous materials designed for extracellular matrix substitutes. Acta Biomater. 8, 4111–4122 (2012). https://doi.org/10.1016/j.actbio.2012.07.025
S.R. Goodyear, R.M. Aspden, Mechanical properties of bone ex vivo, in Bone Research Protocols. ed. by M.H. Helfrich, S.H. Ralston (Humana Press, Totowa, 2012), pp.555–571. https://doi.org/10.1007/978-1-61779-415-5_35
M. Akhmanova, E. Osidak, S. Domogatsky, S. Rodin, A. Domogatskaya, Physical, spatial, and molecular aspects of extracellular matrix of in vivo niches and artificial scaffolds relevant to stem cells research. Stem Cells Int. 2015, 167025 (2015). https://doi.org/10.1155/2015/167025
L. Geddes, L. Carson, E. Themistou, F. Buchanan, A comparison of the increased temperature accelerated degradation of Poly(,-lactide-co-glycolide) and Poly (-lactide-co-glycolide). Polym. Test. 91, 106853 (2020). https://doi.org/10.1016/j.polymertesting.2020.106853
J. Jokinen, E. Dadu, P. Nykvist, J. Käpylä, D.J. White et al., Integrin-mediated cell adhesion to type I collagen fibrils. J. Biol. Chem. 279, 31956–31963 (2004). https://doi.org/10.1074/jbc.M401409200
L.T. Denes, L.A. Riley, J.R. Mijares, J.D. Arboleda, K. McKee et al., Culturing C2C12 myotubes on micromolded gelatin hydrogels accelerates myotube maturation. Skelet. Muscle 9, 17 (2019). https://doi.org/10.1186/s13395-019-0203-4
M.A. Schwartz, R.K. Assoian, Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 114, 2553–2560 (2001). https://doi.org/10.1242/jcs.114.14.2553
B.M. Sicari, V. Agrawal, B.F. Siu, C.J. Medberry, C.L. Dearth et al., A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng. Part A 18, 1941–1948 (2012). https://doi.org/10.1089/ten.TEA.2012.0475
N.J. Turner, A.J. Yates Jr., D.J. Weber, I.R. Qureshi, D.B. Stolz et al., Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng. Part A 16, 3309–3317 (2010). https://doi.org/10.1089/ten.TEA.2010.0169
B.M. Sicari, J.P. Rubin, C.L. Dearth, M.T. Wolf, F. Ambrosio et al., An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6, 234ra58 (2014). https://doi.org/10.1126/scitranslmed.3008085
V.J. Mase Jr., J.R. Hsu, S.E. Wolf, J.C. Wenke, D.G. Baer et al., Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33, 511 (2010). https://doi.org/10.3928/01477447-20100526-24
Y. Jin, E.J. Jeon, S. Jeong, S. Min, Y.S. Choi et al., Reconstruction of muscle fascicle-like tissues by anisotropic 3D patterning. Adv. Funct. Mater. 31, 2006227 (2021). https://doi.org/10.1002/adfm.202006227
Y. Jin, D. Shahriari, E.J. Jeon, S. Park, Y.S. Choi et al., Functional skeletal muscle regeneration with thermally drawn porous fibers and reprogrammed muscle progenitors for volumetric muscle injury. Adv. Mater. 33, e2007946 (2021). https://doi.org/10.1002/adma.202007946
N.E. Gentile, K.M. Stearns, E.H. Brown, J.P. Rubin, M.L. Boninger et al., Targeted rehabilitation after extracellular matrix scaffold transplantation for the treatment of volumetric muscle loss. Am. J. Phys. Med. Rehabil. 93, S79–S87 (2014). https://doi.org/10.1097/PHM.0000000000000145
B.N. Brown, J.E. Valentin, A.M. Stewart-Akers, G.P. McCabe, S.F. Badylak, Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30, 1482–1491 (2009). https://doi.org/10.1016/j.biomaterials.2008.11.040
P. Heher, B. Maleiner, J. Prüller, A.H. Teuschl, J. Kollmitzer et al., A novel bioreactor for the generation of highly aligned 3D skeletal muscle-like constructs through orientation of fibrin via application of static strain. Acta Biomater. 24, 251–265 (2015). https://doi.org/10.1016/j.actbio.2015.06.033
R. Raman, L. Grant, Y. Seo, C. Cvetkovic, M. Gapinske et al., Damage, healing, and remodeling in optogenetic skeletal muscle bioactuators. Adv. Healthc. Mater. 6, 201700030 (2017). https://doi.org/10.1002/adhm.201700030
E. Ko, O. Aydin, Z. Li, L. Gapinske, K.-Y. Huang et al., Empowering engineered muscle in biohybrid pump by extending connexin 43 duration with reduced graphene oxides. Biomaterials 287, 121643 (2022). https://doi.org/10.1016/j.biomaterials.2022.121643
H. Nakazawa, K. Chang, S. Shinozaki, T. Yasukawa, K. Ishimaru et al., iNOS as a driver of inflammation and apoptosis in mouse skeletal muscle after burn injury: possible involvement of Sirt1 S-nitrosylation-mediated acetylation of p65 NF-κB and p53. PLoS ONE 12, e0170391 (2017). https://doi.org/10.1371/journal.pone.0170391
S. Schiaffino, C. Mammucari, Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1, 4 (2011). https://doi.org/10.1186/2044-5040-1-4
E. Andres-Mateos, H. Brinkmeier, T.N. Burks, R. Mejias, D.C. Files et al., Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol. Med. 5, 80–91 (2013). https://doi.org/10.1002/emmm.201201443
J. Massenet, E. Gardner, B. Chazaud, F.J. Dilworth, Epigenetic regulation of satellite cell fate during skeletal muscle regeneration. Skelet. Muscle 11, 4 (2021). https://doi.org/10.1186/s13395-020-00259-w
M.K. Tu, J.B. Levin, A.M. Hamilton, L.N. Borodinsky, Calcium signaling in skeletal muscle development, maintenance and regeneration. Cell Calcium 59, 91–97 (2016). https://doi.org/10.1016/j.ceca.2016.02.005
D.R. Brickley, A.S. Agyeman, R.F. Kopp, B.A. Hall, M.C. Harbeck et al., Serum- and glucocorticoid-induced protein kinase 1 (SGK1) is regulated by store-operated Ca2+ entry and mediates cytoprotection against necrotic cell death. J. Biol. Chem. 288, 32708–32719 (2013). https://doi.org/10.1074/jbc.M113.507210
J.M. García-Martínez, D.R. Alessi, mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 416, 375–385 (2008). https://doi.org/10.1042/BJ20081668
E.A. Ivakine, R.D. Cohn, Maintaining skeletal muscle mass: lessons learned from hibernation. Exp. Physiol. 99, 632–637 (2014). https://doi.org/10.1113/expphysiol.2013.074344
J. Luo, A. Liang, M. Liang, R. Xia, Y. Rizvi et al., Serum glucocorticoid-regulated kinase 1 blocks CKD-induced muscle wasting via inactivation of FoxO3a and Smad2/3. J Am Soc Nephrol 27, 2797–2808 (2016). https://doi.org/10.1681/ASN.2015080867
Q. Xue, Y. Yan, R. Zhang, H. Xiong, Regulation of iNOS on immune cells and its role in diseases. Int. J. Mol. Sci. 19, 3805 (2018). https://doi.org/10.3390/ijms19123805
Y. Yu, H. Sun, Q. Lu, J. Sun, P. Zhang et al., Spontaneous formation of MXene-oxidized sono/chemo-dynamic sonosensitizer/nanocatalyst for antibacteria and bone-tissue regeneration. J. Nanobiotechnol. 21, 193 (2023). https://doi.org/10.1186/s12951-023-01933-z
N.C. Sibisi, C. Snyman, K.H. Myburgh, C.U. Niesler, Evaluating the role of nitric oxide in myogenesis in vitro. Biochimie 196, 216–224 (2022). https://doi.org/10.1016/j.biochi.2021.11.006
E. Rigamonti, T. Touvier, E. Clementi, A.A. Manfredi, S. Brunelli et al., Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage. J. Immunol. 190, 1767–1777 (2013). https://doi.org/10.4049/jimmunol.1202903
M. Yamada, Y. Sankoda, R. Tatsumi, W. Mizunoya, Y. Ikeuchi et al., Matrix metalloproteinase-2 mediates stretch-induced activation of skeletal muscle satellite cells in a nitric oxide-dependent manner. Int. J. Biochem. Cell Biol. 40, 2183–2191 (2008). https://doi.org/10.1016/j.biocel.2008.02.017
X. Chen, Y. Li, Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adh. Migr. 3, 337–341 (2009). https://doi.org/10.4161/cam.3.4.9338
S. Hayashi, H. Aso, K. Watanabe, H. Nara, M.T. Rose et al., Sequence of IGF-I, IGF-II, and HGF expression in regenerating skeletal muscle. Histochem. Cell Biol. 122, 427–434 (2004). https://doi.org/10.1007/s00418-004-0704-y
P. Kaliman, F. Viñals, X. Testar, M. Palacín, A. Zorzano, Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271, 19146–19151 (1996). https://doi.org/10.1074/jbc.271.32.19146
R. Kornasio, I. Riederer, G. Butler-Browne, V. Mouly, Z. Uni et al., Beta-hydroxy-beta-methylbutyrate (HMB) stimulates myogenic cell proliferation, differentiation and survival via the MAPK/ERK and PI3K/Akt pathways. Biochim. Biophys. Acta 1793, 755–763 (2009). https://doi.org/10.1016/j.bbamcr.2008.12.017
M. Ma, X. Wang, X. Chen, R. Cai, F. Chen et al., microRNA-432 targeting E2F3 and P55PIK inhibits myogenesis through PI3K/AKT/mTOR signaling pathway. RNA Biol. 14, 347–360 (2017). https://doi.org/10.1080/15476286.2017.1279786
J. Kim, M.Y. Park, H.K. Kim, Y. Park, K.Y. Whang, Cortisone and dexamethasone inhibit myogenesis by modulating the AKT/mTOR signaling pathway in C2C12. Biosci. Biotechnol. Biochem. 80, 2093–2099 (2016). https://doi.org/10.1080/09168451.2016.1210502
Kshitiz, J. Park, P. Kim, W. Helen, A.J. Engler et al., Control of stem cell fate and function by engineering physical microenvironments. Integr. Biol. 4, 1008–1018 (2012). https://doi.org/10.1039/c2ib20080e
C. Leclech, A.I. Barakat, Is there a universal mechanism of cell alignment in response to substrate topography? Cytoskeleton 78, 284–292 (2021). https://doi.org/10.1002/cm.21661
M.T. Lam, S. Sim, X. Zhu, S. Takayama, The effect of continuous wavy micropatterns on silicone substrates on the alignment of skeletal muscle myoblasts and myotubes. Biomaterials 27, 4340–4347 (2006). https://doi.org/10.1016/j.biomaterials.2006.04.012
M.T. Lam, Y.-C. Huang, R.K. Birla, S. Takayama, Microfeature guided skeletal muscle tissue engineering for highly organized 3-dimensional free-standing constructs. Biomaterials 30, 1150–1155 (2009). https://doi.org/10.1016/j.biomaterials.2008.11.014
D.G. Farwell, K.A. Shera, J.I. Koop, G.A. Bonnet, C.P. Matthews et al., Genetic and epigenetic changes in human epithelial cells immortalized by telomerase. Am. J. Pathol. 156, 1537–1547 (2000). https://doi.org/10.1016/S0002-9440(10)65025-0
R. Foulkes, E. Man, J. Thind, S. Yeung, A. Joy et al., The regulation of nanomaterials and nanomedicines for clinical application: current and future perspectives. Biomater. Sci. 8, 4653–4664 (2020). https://doi.org/10.1039/d0bm00558d