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Rapid synthesis of novel cerium oxide microtubes and its cytocompatibility study

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Abstract

Microtubes (MT) are one of the emerging biomaterials as they can play an important role as porous conduits, guidance cues, microvascular joining, and places where tissue composition matches microtubular geometry. In this regard, protein- and polymeric-based MT have reported biodegradable protein conduit for nerve repair and silk micro-vasculature-based repair of the blood vessel. Here in this article, we report for the first time the rapid production method of cerium oxide microtubes (CeO2-MT) and their cytocompatibility with C2C12 cells. The microtubes were prepared by precipitating CeO2 in an aqueous solution on the electrospun polycaprolactone (PCL) nanofibers, followed by thermal degradation at 440 °C for 5 h to remove the PCL, thereby obtaining the CeO2-MT. X-ray diffraction, X-ray photoelectron spectroscopy, scanning electron microscopy, Raman spectroscopy, and Brunauer–Emmett–Teller (BET) surface area measurements confirmed the presence of MT with the phase of CeO2, with fiber diameter ≈280 nm and high surface area due to tubular space. MT was cytocompatible with mouse myoblast cell line C2C12 cells and protected the cells from reactive oxygen species (ROS) insult at 100 µM H2Oconcentration. Therefore, the findings demonstrate the potentiality of MT tubular structure as novel biomaterials for scavenging high ROS and as a guided cell cue for potential muscle tissue regeneration.

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The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. C. Mahapatra, R.K. Singh, J.H. Lee, J. Jung, J.K. Hyun, H.W. Kim, Nano-shape varied cerium oxide nanomaterials rescue human dental stem cells from oxidative insult through intracellular or extracellular actions. Acta Biomater. 50, 142–153 (2017). https://doi.org/10.1016/j.actbio.2016.12.014

    Article  CAS  Google Scholar 

  2. M. You, K. Li, Y. Xie, L. Huang, X. Zheng, The effects of cerium valence states at cerium oxide coatings on the responses of bone mesenchymal stem cells and macrophages. Biol. Trace Elem. Res. 179, 259–270 (2017)

    Article  CAS  Google Scholar 

  3. F. Wei, C.J. Neal, T.S. Sakthivel, T. Kean, S. Seal, M.J. Coathup, Multi-functional cerium oxide nanoparticles regulate inflammation and enhance osteogenesis. Mater. Sci. Eng., C 124, 112041 (2021)

    Article  CAS  Google Scholar 

  4. A. Datta, S. Mishra, K. Manna, K.D. Saha, S. Mukherjee, S. Roy, Pro-oxidant therapeutic activities of cerium oxide nanoparticles in colorectal carcinoma cells. ACS Omega 5, 9714–9723 (2020)

    Article  CAS  Google Scholar 

  5. L. Zeng, H. Cheng, Y. Dai, Z. Su, C. Wang, L. Lei, D. Lin, X. Li, H. Chen, K. Fan, S. Shi, In vivo regenerable cerium oxide nanozyme-loaded pH/H2O2-responsive nanovesicle for tumor-targeted photothermal and photodynamic therapies. ACS Appl. Mater. Interfaces. 13, 233–244 (2021)

    Article  CAS  Google Scholar 

  6. B. Córdoba-Jover, A. Arce-Cerezo, J. Ribera, M. Pauta, D. Oró, G. Casals, G. Fernández-Varo, E. Casals, V. Puntes, W. Jiménez, M. Morales-Ruiz, Cerium oxide nanoparticles improve liver regeneration after acetaminophen-induced liver injury and partial hepatectomy in rats. J. Nanobiotechnol. 17, 112 (2019)

    Article  Google Scholar 

  7. J.-W. Kim, C. Mahapatra, J.-Y. Hong, M.S. Kim, K.W. Leong, H.-W. Kim, J.K. Hyun, Functional recovery of contused spinal cord in rat with the injection of optimal-dosed cerium oxide nanoparticles. Adv. Sci. 4, 1700034 (2017)

    Article  Google Scholar 

  8. A. Arya, N.K. Sethy, A. Gangwar, N. Bhargava, A. Dubey, M. Roy, G. Srivastava, S.K. Singh, M. Das, K. Bhargava, Cerium oxide nanozyme modulate the ‘exercise’ redox biology of skeletal muscle. Mater. Res. Express 4, 055401 (2017)

    Article  Google Scholar 

  9. G.G. Genchi, A. Degl’Innocenti, A.R. Salgarella, I. Pezzini, A. Marino, A. Menciassi, S. Piccirillo, M. Balsamo, G. Ciofani, Modulation of gene expression in rat muscle cells following treatment with nanoceria in different gravity regimes. Nanomedicine. 13, 2821–2833 (2018)

    Article  CAS  Google Scholar 

  10. I.-S. Park, C. Mahapatra, J.S. Park, K. Dashnyam, J.-W. Kim, J.C. Ahn, P.-S. Chung, D.S. Yoon, N. Mandakhbayar, R.K. Singh, J.-H. Lee, K.W. Leong, H.-W. Kim, Revascularization and limb salvage following critical limb ischemia by nanoceria-induced Ref-1/APE1-dependent angiogenesis. Biomater 242, 119919 (2020)

    Article  CAS  Google Scholar 

  11. A. Jain, M. Behera, C. Mahapatra, N.R. Sundaresan, K. Chatterjee, Nanostructured polymer scaffold decorated with cerium oxide nanoparticles toward engineering an antioxidant and anti-hypertrophic cardiac patch. Mater. Sci. Eng. C 118, 111416 (2021)

    Article  CAS  Google Scholar 

  12. F. Pagliari, C. Mandoli, G. Forte, E. Magnani, S. Pagliari, G. Nardone, S. Licoccia, M. Minieri, P. Di Nardo, E. Traversa, Cerium oxide nanoparticles protect cardiac progenitor cells from oxidative stress. ACS Nano 6, 3767–3775 (2012)

    Article  CAS  Google Scholar 

  13. P.B. Sigler, B.J. Masters, The hydrogen peroxide-induced Ce*(III)-Ce(IV) exchange system1. J. Am. Chem. Soc. 79, 6353–6357 (1957)

    Article  CAS  Google Scholar 

  14. A. Filippi, F. Liu, J. Wilson, S. Lelieveld, K. Korschelt, T. Wang, Y. Wang, T. Reich, U. Pöschl, W. Tremel, H. Tong, Antioxidant activity of cerium dioxide nanoparticles and nanorods in scavenging hydroxyl radicals. RSC Adv. 9, 11077–11081 (2019)

    Article  CAS  Google Scholar 

  15. Y. Yang, Z. Mao, W. Huang, L. Liu, J. Li, J. Li, Q. Wu, Redox enzyme-mimicking activities of CeO2 nanostructures: intrinsic influence of exposed facets. Sci. Rep. 6, 35344 (2016)

    Article  CAS  Google Scholar 

  16. M. Wang, H. He, D. Liu, M. Ma, Y. Zhang, Preparation, characterization and multiple biological properties of peptide-modified cerium oxide nanoparticles. Biomol. 12, 1277 (2022)

    Google Scholar 

  17. T. Naganuma, E. Traversa, The effect of cerium valence states at cerium oxide nanoparticle surfaces on cell proliferation. Biomater. 35, 4441–4453 (2014)

    Article  CAS  Google Scholar 

  18. S.K. Nethi, H.S. Nanda, T.W.J. Steele, C.R. Patra, Functionalized nanoceria exhibit improved angiogenic properties. J. Mater. Chem. B. 5, 9371–9383 (2017)

    Article  CAS  Google Scholar 

  19. S. Das, S. Singh, J.M. Dowding, S. Oommen, A. Kumar, T.X.T. Sayle, S. Saraf, C.R. Patra, N.E. Vlahakis, D.C. Sayle, W.T. Self, S. Seal, The induction of angiogenesis by cerium oxide nanoparticles through the modulation of oxygen in intracellular environments. Biomater. 33, 7746–7755 (2012)

    Article  CAS  Google Scholar 

  20. E. Bazikyan, A. Chunikhin, Morphological and immunohistochemical effect of CeO2 nanoparticles on reparative osteogenesis of the jaw bones, (2021). https://doi.org/10.7324/JAPS.2021.120217

  21. G.-M. Lyu, Y.-J. Wang, X. Huang, H.-Y. Zhang, L.-D. Sun, Y.-J. Liu, C.-H. Yan, Hydrophilic CeO2 nanocubes protect pancreatic β-cell line INS-1 from H2O2-induced oxidative stress. Nanoscale 8, 7923–7932 (2016)

    Article  CAS  Google Scholar 

  22. G.D.O.C. Sathish Ponnurangam, Irina V. Chernyshova, Katherine Wood, Clark Tung-Hui Hung, and Ponisseril Somasundaran, Beneficial effects of cerium oxide nanoparticles in development of chondrocyte-seeded hydrogel constructs and cellular response to interleukin insults. Tissue Engineering Part A 20 (2014) 2908–2919.

  23. M.J. Akhtar, M. Ahamed, H. Alhadlaq, Anti-inflammatory CeO2 nanoparticles prevented cytotoxicity due to exogenous nitric oxide donors via induction rather than inhibition of superoxide/nitric oxide in HUVE cells. Mol. 26, 5416 (2021)

    Article  CAS  Google Scholar 

  24. M.B. Kolli, N.D.P.K. Manne, R. Para, S.K. Nalabotu, G. Nandyala, T. Shokuhfar, K. He, A. Hamlekhan, J.Y. Ma, P.S. Wehner, L. Dornon, R. Arvapalli, K.M. Rice, E.R. Blough, Cerium oxide nanoparticles attenuate monocrotaline induced right ventricular hypertrophy following pulmonary arterial hypertension. Biomater. 35, 9951–9962 (2014)

    Article  CAS  Google Scholar 

  25. S.S. El Shaer, T.A. Salaheldin, N.M. Saied, S.M. Abdelazim, In vivo ameliorative effect of cerium oxide nanoparticles in isoproterenol-induced cardiac toxicity. Exp. Toxicol. Pathol. 69, 435–441 (2017)

    Article  Google Scholar 

  26. G.G. Genchi, A. Degl’Innocenti, C. Martinelli, M. Battaglini, D. De Pasquale, M. Prato, S. Marras, G. Pugliese, F. Drago, A. Mariani, M. Balsamo, V. Zolesi, G. Ciofani, Cerium Oxide Nanoparticle Administration to Skeletal Muscle Cells under Different Gravity and Radiation Conditions. ACS Appl Mater Interfaces. 13(34), 40200–40213 (2021). https://doi.org/10.1021/acsami.1c14176

    Article  CAS  Google Scholar 

  27. D. Lian, M.-M. Chen, H. Wu, S. Deng, X. Hu, The role of oxidative stress in skeletal muscle myogenesis and muscle disease. Antioxid. 11, 755 (2022)

    Article  CAS  Google Scholar 

  28. M.-C. Chen, Y.-C. Sun, Y.-H. Chen, Electrically conductive nanofibers with highly oriented structures and their potential application in skeletal muscle tissue engineering. Acta Biomater. 9, 5562–5572 (2013)

    Article  CAS  Google Scholar 

  29. M. Suhaeri, R. Subbiah, S.-H. Kim, C.-H. Kim, S.J. Oh, S.-H. Kim, K. Park, Novel platform of cardiomyocyte culture and coculture via fibroblast-derived matrix-coupled aligned electrospun nanofiber. ACS Appl. Mater. Interfaces. 9, 224–235 (2017)

    Article  CAS  Google Scholar 

  30. H. Gao, J. Xiao, Y. Wei, H. Wang, H. Wan, S. Liu, Regulation of myogenic differentiation by topologically microgrooved surfaces for skeletal muscle tissue engineering. ACS Omega 6, 20931–20940 (2021)

    Article  CAS  Google Scholar 

  31. K. Chun et al., An array of hollow microcapillaries for the controlled injection of genetic materials into animal/plant cells, Technical Digest. IEEE International MEMS 99 Conference. Twelfth IEEE International Conference on Micro Electro Mechanical Systems (Cat. No.99CH36291), Orlando, FL, USA, 1999, pp. 406–411. https://doi.org/10.1109/MEMSYS.1999.746863

  32. J. Li, Z. Liu, G. Huang, Z. An, G. Chen, J. Zhang, M. Li, R. Liu, Y. Mei, Hierarchical nanoporous microtubes for high-speed catalytic microengines. NPG Asia Mater. 6, e94–e94 (2014)

    Article  CAS  Google Scholar 

  33. M. Lovett, C. Cannizzaro, L. Daheron, B. Messmer, G. Vunjak-Novakovic, D.L. Kaplan, Silk fibroin microtubes for blood vessel engineering. Biomater. 28, 5271–5279 (2007)

    Article  CAS  Google Scholar 

  34. D. Sooriyaarachchi, Y. Zhou, S. Maharubin, G.Z. Tan, Microtube-embedded microfluidic devices for potential applications in blood brain barrier research. Procedia Manuf. 48, 294–301 (2020)

    Article  Google Scholar 

  35. A. Oyane, K. Onuma, A. Ito, H.-M. Kim, T. Kokubo, T. Nakamura, Formation and growth of clusters in conventional and new kinds of simulated body fluids. J. Biomed. Mater. Res., Part A 64A, 339–348 (2003)

    Article  CAS  Google Scholar 

  36. Y. Polyak, Z. Bastl, XPS and factor analysis study of initial stages of cerium oxide growth on polycrystalline tungsten. Surf. Interface Anal. 47, 663–671 (2015)

    Article  CAS  Google Scholar 

  37. M. Comet, L. Schreyeck-Reinert, C. Louis, H. Fuzellier, Synthesis and characterization of high surface area aluminium and alumina microtubes from carbonaceous materials. J. Mater. Chem. 12, 754–757 (2002)

    Article  CAS  Google Scholar 

  38. C. Schilling, A. Hofmann, C. Hess, M.V. Ganduglia-Pirovano, Raman spectra of polycrystalline CeO2: a density functional theory study. J. Phys. Chem. C 121, 20834–20849 (2017)

    Article  CAS  Google Scholar 

  39. K. Li, Y. Xie, M. You, L. Huang, X. Zheng, Cerium oxide-incorporated calcium silicate coating protects MC3T3-E1 osteoblastic cells from H2O2-induced oxidative stress. Biol. Trace Elem. Res. 174, 198–207 (2016)

    Article  CAS  Google Scholar 

  40. Y. Feng, Z. Xu, C. Peng, H. Huang, J. Hu, A facile route to obtain binary micro-nano roughness on composite coating surface. Eur. Phys. J. Appl. Phys. 82, 21302 (2018)

    Article  CAS  Google Scholar 

  41. M. Aguirre, E. Johansson Salazar-Sandoval, M. Johansson, A. Ahniyaz, M. Paulis, J.R. Leiza, Hybrid acrylic/CeO2 nanocomposites using hydrophilic, spherical and high aspect ratio CeO2 nanoparticles. Journal of Materials Chemistry A. 2, 20280–20287 (2014). https://doi.org/10.1039/c4ta03620d

  42. S. Polaka, P. Katare, B. Pawar, N. Vasdev, T. Gupta, K. Rajpoot, P. Sengupta, R.K. Tekade, Emerging ROS-modulating technologies for augmentation of the wound healing process. ACS. Omega. 7, 30657–30672 (2022)

    Article  CAS  Google Scholar 

  43. H. Sadidi, S. Hooshmand, A. Ahmadabadi, S. Javad Hosseini, F. Baino, M. Vatanpour, S. Kargozar, Cerium Oxide Nanoparticles (Nanoceria): Hopes in Soft Tissue Engineering. Molecules. 25(19):4559 (2020 ). https://doi.org/10.3390/molecules25194559

  44. K. Min, O.-S. Kwon, A.J. Smuder, M.P. Wiggs, K.J. Sollanek, D.D. Christou, J.-K. Yoo, M.-H. Hwang, H.H. Szeto, A.N. Kavazis, S.K. Powers, Increased mitochondrial emission of reactive oxygen species and calpain activation are required for doxorubicin-induced cardiac and skeletal muscle myopathy. J. Physiol. 593, 2017–2036 (2015)

    Article  CAS  Google Scholar 

  45. S.A. Dogan, G. Giacchin, E. Zito, C. Viscomi, Redox signaling and stress in inherited myopathies. Antioxid Redox Signal. 37(4–6), 301–323 (2022). https://doi.org/10.1089/ars.2021.0266

    Article  CAS  Google Scholar 

  46. S.K. Powers, A.J. Smuder, A.R. Judge, Oxidative stress and disuse muscle atrophy: cause or consequence? Current Opinion in Clinical Nutrition & Metabolic Care 15 (2012).

  47. M.C. Gomez-Cabrera, C. Arc-Chagnaud, A. Salvador-Pascual, T. Brioche, A. Chopard, G. Olaso-Gonzalez, J. Viña, Redox modulation of muscle mass and function. Redox Biol. 35, 101531 (2020)

    Article  CAS  Google Scholar 

  48. J. Kruk, B.H. Aboul-Enein, E. Duchnik, M. Marchlewicz, Antioxidative properties of phenolic compounds and their effect on oxidative stress induced by severe physical exercise. J. Physiol. Sci. 72, 19 (2022)

    Article  CAS  Google Scholar 

  49. H. Wu, H. Liao, F. Li, J. Lee, P. Hu, W. Shao, X. Li, D. Ling, Bioactive ROS-scavenging nanozymes for regenerative medicine: reestablishing the antioxidant firewall. Nano. Select. 1, 285–297 (2020)

    Article  Google Scholar 

  50. F.M. Filetti, D.V. Vassallo, M. Fioresi, M.R. Simões, Reactive oxygen species impair the excitation-contraction coupling of papillary muscles after acute exposure to a high copper concentration. Toxicol. In Vitro 51, 106–113 (2018)

    Article  CAS  Google Scholar 

  51. J.-W. Cao, S.-Y. Duan, H.-X. Zhang, Y. Chen, M. Guo, Zinc deficiency promoted fibrosis via ROS and TIMP/MMPs in the myocardium of mice. Biol. Trace Elem. Res. 196, 145–152 (2020)

    Article  Google Scholar 

  52. J.-G. Lee, W.-J. Noh, H. Kim, M.-Y. Lee, Generation of reactive oxygen species contributes to the development of carbon black cytotoxicity to vascular cells Toxicological Research. Korean. Soc. Toxicol. 27, 161–166 (2011)

    CAS  Google Scholar 

  53. H.K. Choi, C.-H. Kim, S.N. Lee, T.-H. Kim, B.-K. Oh, Nano-sized graphene oxide coated nanopillars on microgroove polymer arrays that enhance skeletal muscle cell differentiation. Nano Convergence 8, 40 (2021)

    Article  CAS  Google Scholar 

  54. C. Eren Cimenci, G. Uzunalli, O. Uysal, F. Yergoz, E. Karaca Umay, M.O. Guler, A.B. Tekinay, Laminin mimetic peptide nanofibers regenerate acute muscle defect. Acta Biomaterialia 60 , 190–200 (2017)

  55. A. Cheesbrough, F. Sciscione, F. Riccio, P. Harley, L. R’Bibo, G. Ziakas, A. Darbyshire, I. Lieberam, W. Song, Biobased elastomer nanofibers guide light-controlled human-iPSC-derived skeletal myofibers. Adv. Mater. 34, 2110441 (2022)

    Article  CAS  Google Scholar 

  56. M. Goldberg, R. Langer, X. Jia, Nanostructured materials for applications in drug delivery and tissue engineering. J. Biomater. Sci. Polym. Ed. 18, 241–268 (2007)

    Article  CAS  Google Scholar 

  57. L.D. Ghosh, A. Jain, N.R. Sundaresan, K. Chatterjee, Elucidating molecular events underlying topography mediated cardiomyogenesis of stem cells on 3D nanofibrous scaffolds. Mat Sci Eng C-Mater 88, 104–114 (2018)

    Article  Google Scholar 

  58. N. Hanib, F. Hamzah, Z. Omar, I. Subuki, Surface characterization on alkali-heat-treatment on titanium alloy. Malays. J. Anal. Sci. 20, 1429–1436 (2016)

    Article  Google Scholar 

  59. F. Gentile, Time dependent adhesion of cells on nanorough surfaces. J. Biomech. 129, 110814 (2021)

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are thankful to the National Institute of Technology, Raipur (Chhattisgarh), India, and (CeNSE- MNCF) IISc Bangalore for providing support for this work. CM acknowledges the National Institute of Technology Raipur for the Seed Grant, Project No: NITRR/Seed Grant/2021-22/30. CM also gratefully acknowledged research support from the Department of Science and Technology, India, Science and Engineering Research Board (SERB), Sanction Order No SRG/2022/000348.

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C.M. conceived and designed the study. D.C. performed the experiments. A.K. and C.M analyzed the data and wrote first draft of the manuscript. All the authors reviewed the manuscript. C.M. prepared the final draft of the manuscript.

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Correspondence to Chinmaya Mahapatra.

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Highlights

1. Unique method for rapid production of cerium microtubes is reported.

2. Cerium oxide microtubes are cytocompatible with C2C12 cells.

3. Cerium oxide microtubes could provide directional cue to the C2C12 cells.

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Chandra, D.K., Kumar, A. & Mahapatra, C. Rapid synthesis of novel cerium oxide microtubes and its cytocompatibility study. emergent mater. 6, 595–603 (2023). https://doi.org/10.1007/s42247-023-00498-9

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