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Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats

Year 2020, Volume: 48 Issue: 4, 341 - 348, 06.07.2020
https://doi.org/10.15671/hjbc.617783

Abstract

Due to lack of self-repair mechanism in neuronal tissue, biomaterials have been widely studied to regenerate damaged nerve tissue. Despite having advantages, nano materials may cause oxidative stress and this could affect the treatment. In the present study, whether PHBV [poly (3-hydroxybutyrate-co-3-hydroxyvalerate)] used for axonal regeneration could lead to lipid peroxidation, protein oxidation in rats or not and also its effects on antioxidant molecules was explored. In the study, PHBV nanofiber membranes were formed by electrospinning and conduits were formed by using the nanofiber membrane. After the formation of a 1 cm gap in the rat peritoneal nerves, PHBV conduits were placed. Animals were sacrificed at 17th week after the operations. Malondialdehyde (MDA), advanced oxidation protein products (AOPP), glutathione (GSH) levels and superoxide dismutase (SOD) activities of livers, as well as surrounding tissues of conduits (muscles) and serums were measured. Compared to control groups, MDA, AOPP and GSH levels and SOD activites in all graft group serums showed a significant increase, while only MDA and AOPP levels in tissues were statistically higher. Therefore, these findings suggest that PHBV nerve graft used for sciatic nerve defects may lead to oxidative stress in rats.

References

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  • 4. V. Witko-Sarsat, M. Friedlander, T.N. Khoa, C. Capeillère-Blandin, A.T. Nguyen, S. Canteloup, J.M. Dayer, P. Jungers, T. Drüeke, B. Descamps-Latscha, Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure, J. Immunol., 161, (1998) 2524-2532.
  • 5. K. Aquilano, S. Baldelli, B. Pagliei, S.M. Cannata, G. Rotilio, M.R. Ciriolo, p53 Orchestrates the PGC-1α-mediated antioxidant response upon mild redox and metabolic imbalance, Antioxid. Redox Signal., 18 (2012) 386-399.
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  • 7. P.A. Mouthuy, S.J.B. Snelling, S.G. Dakin, L. Milković, A.Č. Gašparović, A.J. Carr, N. Žarković, Biocompatibility of implantable materials: an oxidative stress viewpoint, Biomaterials, 109 (2016) 55-68.
  • 8. W. Tao, D. Pan, Z. Gong, X. Peng, Nanoporous platinum electrode grown on anodic aluminum oxide membrane: Fabrication, characterization, electrocatalytic activity toward reactive oxygen and nitrogen species, Anal. Chim. Acta, 1035 (2018) 44-50.
  • 9. W.W. Jiang, S.H. Su, R.C. Eberhart, L. Tang, Phagocyte responses to degradable polymers, J. Biomed. Mater. Res. A, 82 (2007) 492-497.
  • 10. H.H. Chang, M.K. Guo, F.H. Kasten, M.C. Chang, G.F. Huang, Y.L. Wang, R.S. Wang, J.H. Jeng, Stimulation of glutathione depletion, ROS production and cell cycle arrest of dental pulp cells and gingival epithelial cells by HEMA, Biomaterials, 26 (2005) 745-753.
  • 11. W.F. Liu, M. Ma, K.M. Bratlie, T.T. Dang, R. Langer, D.G. Anderson, Real-time in vivo detection of biomaterial-induced reactive oxygen species, Biomaterials, 32 (2011) 1796-1801.
  • 12. M. Demirbilek, M. Sakar, Z. Karahaliloğlu, E. Erdal, E. Yalçın, G. Bozkurt, P. Korkusuz, E. Bilgiç, Ç.M. Temuçin, E.B. Denkbaş, Aligned bacterial PHBV nanofibrous conduit for peripheral nerve regeneration, Artif. Cell. Nanomed. Biotechnol., 43 (2015) 243-251.
  • 13. T. Yoshioka, K. Kawada, T. Shimada, M. Mori, Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood, Am. J. Obstet. Gynecol., 135 (1979) 372-376.
  • 14. Y. Sun, L.W. Oberley, Y. Li, A simple method for clinical assay of superoxide dismutase, Clin. Chem., 34 (1988) 497-500.
  • 15. J. Sedlak, R.H. Lindsay, Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent, Anal. Biochem., 25 (1968) 192-205.
  • 16. O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall, Protein measurements with the folin phenol reagent, J. Biol. Chem., 193 (1951) 265-275.
  • 17. A. Schröfel, G. Kratošová, I. Šafařík, M. Šafaříková, I. Raška,L.M. Shor, Applications of biosynthesized metallic nanoparticles - A review, Acta Biomater., 10 (2014) 4023-4042.
  • 18. H. Shin, S. So, A.G. Mikos, Biomimetic materials for tissue engineering, Biomaterials, 24 (2003) 4353-4364.
  • 19. J.R. Martin, M.K. Gupta, J.M. Page, F. Yu, J.M. Davidson, S.A. Guelcher, C.L. Duvall, A porous tissue engineering scaffold selectively degraded by cell-generated oxygen species, Biomaterials, 35 (2014) 3766-3776.
  • 20. Z.J. Deng, M.T. Liang, M. Monteiro, I. Toth, R.F. Minchin, Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation, Nat. Nanotechnol., 6 (2011) 39-44.
  • 21. R.P. Singh, P. Ramarao, Accumulated polymer degradation products as effector molecules in cytotoxicity of polymeric nanoparticles, Toxicol. Sci., 136 (2013) 131-143.
  • 22. F.A. Cupaioli, F.A. Zucca, D. Boraschi, L. Zecca, Engineered nanoparticles. How brain friendly is this new guest?, Prog. Neurobiol., 119-120 (2014) 20-38.
  • 23. J.D. De Queiroz, A.M. Leal, M. Terada, L.F. Agnez-Lima, I. Costa, N.C. Pinto, S.R. Mediros, Surface modification by argon plasma treatment improves antioxidant defense ability of CHO-k1 cells on titanium surfaces, Toxicol. In Vitro, 28 (2014) 381-387.
  • 24. K. Brieger, S. Schiavone, F.J. Miller, K.H. Krause, Reactive oxygen species: from health to disease, Swiss Med. Wkly., 142 (2012) 13659.
  • 25. M.K. Reddy, L. Wu, W. Kou, A. Ghorpade, V. Labhasetwar, Superoxide dismutase-loaded PLGA nanoparticles protect cultured huöam neurons under oxidative stress, Apply. Biochem. Biotechnol., 151 (2008) 565-577.
  • 26. A.K. Gangwar, N. Kumar, S.D. Khangembam, V. Kumar, R. Singh, Primary chicken embryo fibroblasts seeded acellular dermal matrix (3-D ADM) improve regeneration of full thickness skin wounds in rats, Tissue Cell., 47 (2015) 311-322.
  • 27. S. Xiong, S. George, H. Yu, R. Damoiseaux, B. France, K.W. Ng, J.S. Loo, Size influences the cytotoxicity of poly (lactic-co-glycolic acid) (PLGA) and titanium dioxide (TiO(2)) nanoparticles, Arch. Toxicol., 87 (2013) 1075-1086.
  • 28. M.S. Cartiera, K.M. Johnson, V. Rajendran, M.J. Caplan, W.M. Saltzman, The uptake and intracellular fate of PLGA nanoparticles in epithelial cells, Biomaterials, 30 (2009) 2790-2798.
  • 29. X. Feng, A. Chen, Y. Zhang, J. Wang, L. Shao, L. Wei, Central nervous system toxicity of metallic nanoparticles, Int. J. Nanomedicine, 10 (2015) 4321-4340.
  • 30. J. Lee, S. Giordano, J. Zhang, Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling, Biochem. J., 441 (2012) 523-540.
  • 31. Y.H. Luo, S.B. Wu, Y.H. Wei, Y.C. Chen, M.H. Tsai, C.C. Ho, S.Y. Lin, C.S. Yang, P. Lin, Cadmium-based quantum dot induced autophagy formation for cell survival via oxidative stress, Chem. Res. Toxicol., 26 (2013) 662-673.
  • 32. K.N. Yu, T.J. Yoon, A. Minai-Tehrani, J.E. Kim, S.J. Park, M.S. Jeong, S.W. Ha, J.K. Lee, J.S. Kim, M.H. Cho, Zinc oxide nanoparticle induced autophagic cell death and mitochondrial damage via reactive oxygen species generation, Toxicol. In Vitro, 27 (2013) 1187-1195.
  • 33. K. Fu, D.W. Pack, A.M. Klibanov, R. Langer, Visual evidence of acidic environment within degrading poly(lactic-co-glycolic acid) (PLGA) microspheres, Pharm. Res., 17 (2000) 100-106.
  • 34. T.M. Allen, D.R. Mumbengegwi, G.J. Charrois, Anti-CD19 targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates, Clin. Cancer Res., 11 (2005) 3567-3573.
  • 35. G.J. Charrois, T.M. Allen, Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer, Biochim. Biophys. Acta, 1663 (2004) 167-177.
  • 36. S. Xiong, H. Li, B. Yu, J. Wu, R.J. Lee, Triggering liposomal drug release with a lysosomotropic agent, J. Pharm. Sci., 99 (2010) 5011-5018.
  • 37. M.C. Serrano, R. Pagani, J. Peña, M.T. Portolés MT, Transitory oxidative stress in L929 fibroblasts cultured on poly(epsilon-caprolactone) films, Biomaterials, 26 (2005) 5827-5834.
  • 38. B. Halamdo Kenzaoui, C. Chapuis Bernasconi, S. Guney-Ayra, L. Juillerat-Jeanneret, Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells, Biochem., 441 (2012) 813-821.
Year 2020, Volume: 48 Issue: 4, 341 - 348, 06.07.2020
https://doi.org/10.15671/hjbc.617783

Abstract

References

  • 1. J.L. Gilmore, X. Yi, L. Quan, A.V. Kabanov, Novel nanomaterials for clinical neuroscience, J. Neuroimmune Pharmacol., 3 (2008) 83-94.
  • 2. H. Sies, Oxidative stress: From basic research to clinical application, Am. J. Med., 91 (1991) 31-38.
  • 3. B. Halliwell, J.M.C. Gutteridge, Free radicals in biology and medicine, Development, 134 (2007) 635-646.
  • 4. V. Witko-Sarsat, M. Friedlander, T.N. Khoa, C. Capeillère-Blandin, A.T. Nguyen, S. Canteloup, J.M. Dayer, P. Jungers, T. Drüeke, B. Descamps-Latscha, Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure, J. Immunol., 161, (1998) 2524-2532.
  • 5. K. Aquilano, S. Baldelli, B. Pagliei, S.M. Cannata, G. Rotilio, M.R. Ciriolo, p53 Orchestrates the PGC-1α-mediated antioxidant response upon mild redox and metabolic imbalance, Antioxid. Redox Signal., 18 (2012) 386-399.
  • 6. E. Barone, G. Cenini, F. Di Domenico, T. Noel, C. Wang, M. Perluigi, DK. St Clair, D.A. Butterfield, Basal brain oxidative and nitrative stress levels are finely regulated by the interplay between superoxide dismutase 2 and p53, J. Neurosci. Res., 93 (2015) 1728-1739.
  • 7. P.A. Mouthuy, S.J.B. Snelling, S.G. Dakin, L. Milković, A.Č. Gašparović, A.J. Carr, N. Žarković, Biocompatibility of implantable materials: an oxidative stress viewpoint, Biomaterials, 109 (2016) 55-68.
  • 8. W. Tao, D. Pan, Z. Gong, X. Peng, Nanoporous platinum electrode grown on anodic aluminum oxide membrane: Fabrication, characterization, electrocatalytic activity toward reactive oxygen and nitrogen species, Anal. Chim. Acta, 1035 (2018) 44-50.
  • 9. W.W. Jiang, S.H. Su, R.C. Eberhart, L. Tang, Phagocyte responses to degradable polymers, J. Biomed. Mater. Res. A, 82 (2007) 492-497.
  • 10. H.H. Chang, M.K. Guo, F.H. Kasten, M.C. Chang, G.F. Huang, Y.L. Wang, R.S. Wang, J.H. Jeng, Stimulation of glutathione depletion, ROS production and cell cycle arrest of dental pulp cells and gingival epithelial cells by HEMA, Biomaterials, 26 (2005) 745-753.
  • 11. W.F. Liu, M. Ma, K.M. Bratlie, T.T. Dang, R. Langer, D.G. Anderson, Real-time in vivo detection of biomaterial-induced reactive oxygen species, Biomaterials, 32 (2011) 1796-1801.
  • 12. M. Demirbilek, M. Sakar, Z. Karahaliloğlu, E. Erdal, E. Yalçın, G. Bozkurt, P. Korkusuz, E. Bilgiç, Ç.M. Temuçin, E.B. Denkbaş, Aligned bacterial PHBV nanofibrous conduit for peripheral nerve regeneration, Artif. Cell. Nanomed. Biotechnol., 43 (2015) 243-251.
  • 13. T. Yoshioka, K. Kawada, T. Shimada, M. Mori, Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood, Am. J. Obstet. Gynecol., 135 (1979) 372-376.
  • 14. Y. Sun, L.W. Oberley, Y. Li, A simple method for clinical assay of superoxide dismutase, Clin. Chem., 34 (1988) 497-500.
  • 15. J. Sedlak, R.H. Lindsay, Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent, Anal. Biochem., 25 (1968) 192-205.
  • 16. O.H. Lowry, N.J. Rosebrough, A.L. Farr, R.J. Randall, Protein measurements with the folin phenol reagent, J. Biol. Chem., 193 (1951) 265-275.
  • 17. A. Schröfel, G. Kratošová, I. Šafařík, M. Šafaříková, I. Raška,L.M. Shor, Applications of biosynthesized metallic nanoparticles - A review, Acta Biomater., 10 (2014) 4023-4042.
  • 18. H. Shin, S. So, A.G. Mikos, Biomimetic materials for tissue engineering, Biomaterials, 24 (2003) 4353-4364.
  • 19. J.R. Martin, M.K. Gupta, J.M. Page, F. Yu, J.M. Davidson, S.A. Guelcher, C.L. Duvall, A porous tissue engineering scaffold selectively degraded by cell-generated oxygen species, Biomaterials, 35 (2014) 3766-3776.
  • 20. Z.J. Deng, M.T. Liang, M. Monteiro, I. Toth, R.F. Minchin, Nanoparticle-induced unfolding of fibrinogen promotes Mac-1 receptor activation and inflammation, Nat. Nanotechnol., 6 (2011) 39-44.
  • 21. R.P. Singh, P. Ramarao, Accumulated polymer degradation products as effector molecules in cytotoxicity of polymeric nanoparticles, Toxicol. Sci., 136 (2013) 131-143.
  • 22. F.A. Cupaioli, F.A. Zucca, D. Boraschi, L. Zecca, Engineered nanoparticles. How brain friendly is this new guest?, Prog. Neurobiol., 119-120 (2014) 20-38.
  • 23. J.D. De Queiroz, A.M. Leal, M. Terada, L.F. Agnez-Lima, I. Costa, N.C. Pinto, S.R. Mediros, Surface modification by argon plasma treatment improves antioxidant defense ability of CHO-k1 cells on titanium surfaces, Toxicol. In Vitro, 28 (2014) 381-387.
  • 24. K. Brieger, S. Schiavone, F.J. Miller, K.H. Krause, Reactive oxygen species: from health to disease, Swiss Med. Wkly., 142 (2012) 13659.
  • 25. M.K. Reddy, L. Wu, W. Kou, A. Ghorpade, V. Labhasetwar, Superoxide dismutase-loaded PLGA nanoparticles protect cultured huöam neurons under oxidative stress, Apply. Biochem. Biotechnol., 151 (2008) 565-577.
  • 26. A.K. Gangwar, N. Kumar, S.D. Khangembam, V. Kumar, R. Singh, Primary chicken embryo fibroblasts seeded acellular dermal matrix (3-D ADM) improve regeneration of full thickness skin wounds in rats, Tissue Cell., 47 (2015) 311-322.
  • 27. S. Xiong, S. George, H. Yu, R. Damoiseaux, B. France, K.W. Ng, J.S. Loo, Size influences the cytotoxicity of poly (lactic-co-glycolic acid) (PLGA) and titanium dioxide (TiO(2)) nanoparticles, Arch. Toxicol., 87 (2013) 1075-1086.
  • 28. M.S. Cartiera, K.M. Johnson, V. Rajendran, M.J. Caplan, W.M. Saltzman, The uptake and intracellular fate of PLGA nanoparticles in epithelial cells, Biomaterials, 30 (2009) 2790-2798.
  • 29. X. Feng, A. Chen, Y. Zhang, J. Wang, L. Shao, L. Wei, Central nervous system toxicity of metallic nanoparticles, Int. J. Nanomedicine, 10 (2015) 4321-4340.
  • 30. J. Lee, S. Giordano, J. Zhang, Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling, Biochem. J., 441 (2012) 523-540.
  • 31. Y.H. Luo, S.B. Wu, Y.H. Wei, Y.C. Chen, M.H. Tsai, C.C. Ho, S.Y. Lin, C.S. Yang, P. Lin, Cadmium-based quantum dot induced autophagy formation for cell survival via oxidative stress, Chem. Res. Toxicol., 26 (2013) 662-673.
  • 32. K.N. Yu, T.J. Yoon, A. Minai-Tehrani, J.E. Kim, S.J. Park, M.S. Jeong, S.W. Ha, J.K. Lee, J.S. Kim, M.H. Cho, Zinc oxide nanoparticle induced autophagic cell death and mitochondrial damage via reactive oxygen species generation, Toxicol. In Vitro, 27 (2013) 1187-1195.
  • 33. K. Fu, D.W. Pack, A.M. Klibanov, R. Langer, Visual evidence of acidic environment within degrading poly(lactic-co-glycolic acid) (PLGA) microspheres, Pharm. Res., 17 (2000) 100-106.
  • 34. T.M. Allen, D.R. Mumbengegwi, G.J. Charrois, Anti-CD19 targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates, Clin. Cancer Res., 11 (2005) 3567-3573.
  • 35. G.J. Charrois, T.M. Allen, Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer, Biochim. Biophys. Acta, 1663 (2004) 167-177.
  • 36. S. Xiong, H. Li, B. Yu, J. Wu, R.J. Lee, Triggering liposomal drug release with a lysosomotropic agent, J. Pharm. Sci., 99 (2010) 5011-5018.
  • 37. M.C. Serrano, R. Pagani, J. Peña, M.T. Portolés MT, Transitory oxidative stress in L929 fibroblasts cultured on poly(epsilon-caprolactone) films, Biomaterials, 26 (2005) 5827-5834.
  • 38. B. Halamdo Kenzaoui, C. Chapuis Bernasconi, S. Guney-Ayra, L. Juillerat-Jeanneret, Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells, Biochem., 441 (2012) 813-821.
There are 38 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Melike Erol Demirbilek 0000-0002-9127-0254

Murat Demirbilek This is me 0000-0001-6990-5607

Ebru Erdal 0000-0001-5384-5961

Mustafa Sakar This is me 0000-0002-8344-4074

Gökhan Bozkurt This is me 0000-0001-5135-1343

Publication Date July 6, 2020
Acceptance Date September 28, 2020
Published in Issue Year 2020 Volume: 48 Issue: 4

Cite

APA Erol Demirbilek, M., Demirbilek, M., Erdal, E., Sakar, M., et al. (2020). Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats. Hacettepe Journal of Biology and Chemistry, 48(4), 341-348. https://doi.org/10.15671/hjbc.617783
AMA Erol Demirbilek M, Demirbilek M, Erdal E, Sakar M, Bozkurt G. Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats. HJBC. July 2020;48(4):341-348. doi:10.15671/hjbc.617783
Chicago Erol Demirbilek, Melike, Murat Demirbilek, Ebru Erdal, Mustafa Sakar, and Gökhan Bozkurt. “Effects of Bacterial PHBV-Conduit Used for Nerve Regeneration on Oxidative Stress Parameters in Rats”. Hacettepe Journal of Biology and Chemistry 48, no. 4 (July 2020): 341-48. https://doi.org/10.15671/hjbc.617783.
EndNote Erol Demirbilek M, Demirbilek M, Erdal E, Sakar M, Bozkurt G (July 1, 2020) Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats. Hacettepe Journal of Biology and Chemistry 48 4 341–348.
IEEE M. Erol Demirbilek, M. Demirbilek, E. Erdal, M. Sakar, and G. Bozkurt, “Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats”, HJBC, vol. 48, no. 4, pp. 341–348, 2020, doi: 10.15671/hjbc.617783.
ISNAD Erol Demirbilek, Melike et al. “Effects of Bacterial PHBV-Conduit Used for Nerve Regeneration on Oxidative Stress Parameters in Rats”. Hacettepe Journal of Biology and Chemistry 48/4 (July 2020), 341-348. https://doi.org/10.15671/hjbc.617783.
JAMA Erol Demirbilek M, Demirbilek M, Erdal E, Sakar M, Bozkurt G. Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats. HJBC. 2020;48:341–348.
MLA Erol Demirbilek, Melike et al. “Effects of Bacterial PHBV-Conduit Used for Nerve Regeneration on Oxidative Stress Parameters in Rats”. Hacettepe Journal of Biology and Chemistry, vol. 48, no. 4, 2020, pp. 341-8, doi:10.15671/hjbc.617783.
Vancouver Erol Demirbilek M, Demirbilek M, Erdal E, Sakar M, Bozkurt G. Effects of bacterial PHBV-conduit used for nerve regeneration on oxidative stress parameters in rats. HJBC. 2020;48(4):341-8.

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