Zinc Oxide Tetrapods Modulate Wound Healing and Cytokine Release In Vitro—A New Antiproliferative Substance in Glaucoma Filtering Surgery
Abstract
:1. Introduction
2. Materials and Methods
2.1. Preparation of Nano ZnO Tetrapods (ZnO-T)
2.2. Scanning Electron Microscopy (SEM)
2.3. ZnO-T Absorption Spectrum
2.4. Establishment of the Human Tenon’s Fibroblast (HTF) Cultures
2.5. Cell Viability after Incubation with ZnO-Tetrapods
2.6. Ki67, α-SMA and pSMAD Immunostaining
2.7. Quantification of Immunopositive cells
2.8. Cell Migration: Wound Healing Assay
2.9. Culture Supernatant Samples
2.10. Immunoassays
2.11. Statistics
3. Results
3.1. Scanning Electron Microscopy (SEM)
3.2. ZnO-T Absorption Spectrum
3.3. Cytotoxicity of ZnO-Tetrapods
3.4. Ki67, α-SMA and pSMAD Immunostaining
3.5. Cell Migration: Wound Healing Assay
3.6. Cytokine Production: Immunoassays
4. Discussion
5. Patents
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tham, Y.C.; Li, X.; Wong, T.Y.; Quigley, H.A.; Aung, T.; Cheng, C.Y. Global prevalence of glaucoma and projections of glaucoma burden through 2040: A systematic review and meta-analysis. Ophthalmology 2014, 121, 2081–2090. [Google Scholar] [CrossRef] [PubMed]
- Quigley, H.A.; Broman, A.T. The number of people with glaucoma worldwide in 2010 and 2020. Br. J. Ophthalmol. 2006, 90, 262–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- The Advanced Glaucoma Intervention Study (AGIS): 7. The relationship between control of intraocular pressure and visual field deterioration. The AGIS Investigators. Am. J. Ophthalmol. 2000, 130, 429–440. [Google Scholar] [CrossRef]
- Hong, C.H.; Arosemena, A.; Zurakowski, D.; Ayyala, R.S. Glaucoma drainage devices: A systematic literature review and current controversies. Surv. Ophthalmol. 2005, 50, 48–60. [Google Scholar] [CrossRef]
- Tomasek, J.J.; Gabbiani, G.; Hinz, B.; Chaponnier, C.; Brown, R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3, 349–363. [Google Scholar] [CrossRef]
- Lemoinne, S.; Cadoret, A.; El Mourabit, H.; Thabut, D.; Housset, C. Origins and functions of liver myofibroblasts. Biochim. Biophys. Acta 2013, 1832, 948–954. [Google Scholar] [CrossRef] [Green Version]
- Desmoulière, A.; Redard, M.; Darby, I.; Gabbiani, G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am. J. Pathol. 1995, 146, 56–66. [Google Scholar]
- Darby, I.A.; Hewitson, T.D. Fibroblast differentiation in wound healing and fibrosis. Int. Rev. Cytol. 2007, 257, 143–179. [Google Scholar]
- Heckmann, M.; Krieg, T. Biological and pharmacological modulations of fibroblast functions. Skin Pharmacol. 1989, 2, 125–137. [Google Scholar] [CrossRef]
- Kakizaki, H.; Takahashi, Y.; Nakano, T.; Asamoto, K.; Ikeda, H.; Ichinose, A.; Iwaki, M.; Selva, D.; Leibovitch, I. Anatomy of Tenons capsule. Clin. Exp. Ophthalmol. 2011, 40, 611–616. [Google Scholar] [CrossRef]
- Kottler, U.B.; Jünemann, A.G.M.; Aigner, T.; Zenkel, M.; Rummelt, C.; Schlötzer-Schrehardt, U. Comparative effects of TGF-β1 and TGF-β2 on extracellular matrix production, proliferation, migration, and collagen contraction of human Tenon’s capsule fibroblasts in pseudoexfoliation and primary open-angle glaucoma. Exp. Eye Res. 2005, 80, 121–134. [Google Scholar] [CrossRef] [PubMed]
- Ma, P.; Gao, Q.; Wang, Z.; Yu, K. Expression of protein kinase C isoforms in cultured human Tenon’s capsule fibroblast cells. Mol. Med. Rep. 2015, 12, 6025–6030. [Google Scholar] [CrossRef] [PubMed]
- Wei, G.; Xu, Q.; Liu, L.; Zhang, H.; Tan, X.; Zhang, C.; Han, C.; Guo, Y.; Han, G.; Zhang, C. LY2109761 reduces TGF-β1-induced collagen production and contraction in hypertrophic scar fibroblasts. Arch. Dermatol. Res. 2018, 310, 615–623. [Google Scholar] [CrossRef] [PubMed]
- Schafer, M.; Werner, S. Oxidative stress in normal and impaired wound repair. Pharmacol. Res. 2008, 58, 165–171. [Google Scholar] [CrossRef]
- Cunliffe, I.A.; Richardson, P.S.; Rees, R.C.; Rennie, I.G. Effect of TNF, IL-1, and IL-6 on the proliferation of human Tenon’s capsule fibroblasts in tissue culture. Br. J. Ophthalmol. 1995, 79, 590–595. [Google Scholar] [CrossRef] [Green Version]
- Seong, G.J.; Hong, S.; Jung, S.-A.; Lee, J.-J.; Lim, E.; Kim, S.-J.; Lee, J.H. TGF-β-induced interleukin-6 participates in transdifferentiation of human Tenon’s fibroblasts to myofibroblasts. Mol. Vis. 2009, 15, 2123–2128. [Google Scholar]
- Trelford, C.B.; Denstedt, J.T.; Armstrong, J.J.; Hutnik, C.M.L. The Pro-Fibrotic Behavior of Human Tenon’s Capsule Fibroblasts in Medically Treated Glaucoma Patients. Clin. Ophthalmol. 2020, 141, 391–402. [Google Scholar] [CrossRef]
- Fan Gaskin, J.C.; Nguyen, D.Q.; Soon Ang, G.; O’Connor, J.; Crowston, J.G. Wound Healing Modulation in Glaucoma Filtration Surgery-Conventional Practices and New Perspectives: The Role of Antifibrotic Agents (Part I). J. Curr. Glaucoma Pract. 2014, 8, 37–45. [Google Scholar]
- Ponnusamy, T.; Yu, H.; John, V.T.; Ayyala, R.S.; Blake, D.A. A novel antiproliferative drug coating for glaucoma drainage devices. J. Glaucoma 2014, 23, 526–534. [Google Scholar] [CrossRef]
- Greenfield, D.S.; Liebmann, J.M.; Jee, J.; Ritch, R. Late-onset bleb leaks after glaucoma filtering surgery. Arch. Ophthalmol. 1998, 116, 443–447. [Google Scholar] [CrossRef] [Green Version]
- Khaw, P.T.; Doyle, J.W.; Sherwood, M.B.; Grierson, I.; Schultz, G.; McGorray, S. Prolonged localized tissue effects from 5-minute exposures to fluorouracil and mitomycin C. Arch. Ophthalmol. 1993, 111, 263–267. [Google Scholar] [CrossRef]
- Blake, D.A.; Sahiner, N.; John, V.T.; Clinton, A.D.; Galler, K.E.; Walsh, M.; Arosemena, A.; Johnson, P.Y.; Ayyala, R.S. Inhibition of Cell Proliferation by Mitomycin C Incorporated into P(HEMA) Hydrogels. J. Glaucoma 2006, 15, 291–298. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.-D.; Liang, L.; Chen, C.-S.; Lu, B.; Wang, N.-L.; Jiang, F.-G.; Zhang, X.-Z.; Zhuo, R.-X. Peptide Hydrogel as an Intraocular Drug Delivery System for Inhibition of Postoperative Scarring Formation. ACS Appl. Mater. Interfaces 2010, 2, 2663–2671. [Google Scholar] [CrossRef]
- Kim, N.J.; Harris, A.; Gerber, A.; Tobe, L.A.; Amireskandari, A.; Huck, A.; Siesky, B. Nanotechnology and glaucoma: A review of the potential implications of glaucoma nanomedicine. Br. J. Ophthalmol. 2013, 98, 427–431. [Google Scholar] [CrossRef]
- Zarbin, M.A.; Montemagno, C.; Leary, J.F.; Ritch, R. Nanomedicine in ophthalmology: The new frontier. Am. J. Ophthalmol. 2010, 150, 144–162.e2. [Google Scholar] [CrossRef]
- Ye, H.; Qian, Y.; Lin, M.; Duan, Y.; Sun, X.; Zhuo, Y.; Ge, J. Cationic nano-copolymers mediated IKKβ targeting siRNA to modulate wound healing in a monkey model of glaucoma filtration surgery. Mol. Vis. 2010, 16, 2502–2510. [Google Scholar]
- Shao, T.; Li, X.; Ge, J. Target drug delivery system as a new scarring modulation after glaucoma filtration surgery. Diagn. Pathol. 2011, 6, 64. [Google Scholar] [CrossRef] [Green Version]
- Fan, W.; Li, Q.; Yang, X.; Zhang, L. Zn subcellular distribution in liver of goldfish (carassius auratus) with exposure to zinc oxide nanoparticles and mechanism of hepatic detoxification. PLoS ONE 2013, 8, e78123. [Google Scholar] [CrossRef] [Green Version]
- Shi, L.E.; Li, Z.H.; Zheng, W.; Zhao, Y.F.; Jin, Y.F.; Tang, Z.X. Synthesis, antibacterial activity, antibacterial mechanism and food applications of ZnO nanoparticles: A review. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2014, 31, 173–186. [Google Scholar] [CrossRef]
- Mishra, Y.K.; Adelung, R.; Röhl, C.; Shukla, D.; Spors, F.; Tiwari, V. Virostatic potential of micro-nano filopodia-like ZnO structures against herpes simplex virus-1. Antivir. Res. 2011, 92, 305–312. [Google Scholar] [CrossRef] [Green Version]
- Antoine, T.E.; Mishra, Y.K.; Trigilio, J.; Tiwari, V.; Adelung, R.; Shukla, D. Prophylactic, therapeutic and neutralizing effects of zinc oxide tetrapod structures against herpes simplex virus type-2 infection. Antivir. Res. 2012, 96, 363–375. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.Q.; Yin, L.H.; Tang, M.; Pu, Y.P. ZnO, TiO(2), SiO(2,) and Al(2)O(3) nanoparticles-induced toxic effects on human fetal lung fibroblasts. Biomed. Environ. Sci. 2011, 24, 661–669. [Google Scholar]
- Meyer, K.; Rajanahalli, P.; Ahamed, M.; Rowe, J.J.; Hong, Y. ZnO nanoparticles induce apoptosis in human dermal fibroblasts via p53 and p38 pathways. Toxicol. In Vitro 2011, 25, 1721–1726. [Google Scholar] [CrossRef]
- Akhtar, M.J.; Ahamed, M.; Kumar, S.; Khan, M.M.; Ahmad, J.; Alrokayan, S.A. Zinc oxide nanoparticles selectively induce apoptosis in human cancer cells through reactive oxygen species. Int. J. Nanomed. 2012, 7, 845–857. [Google Scholar]
- Gedamu, D.; Paulowicz, I.; Kaps, S.; Lupan, O.; Wille, S.; Haidarschin, G.; Mishra, Y.K.; Adelung, R. Rapid Fabrication Technique for Interpenetrated ZnO Nanotetrapod Networks for Fast UV Sensors. Adv. Mater. 2013, 26, 1541–1550. [Google Scholar] [CrossRef]
- Papavlassopoulos, H.; Mishra, Y.K.; Kaps, S.; Paulowicz, I.; Abdelaziz, R.; Elbahri, M.; Maser, E.; Adelung, R.; Röhl, C. Toxicity of Functional Nano-Micro Zinc Oxide Tetrapods: Impact of Cell Culture Conditions, Cellular Age and Material Properties. PLoS ONE 2014, 9, e84983. [Google Scholar] [CrossRef] [Green Version]
- Tura, A.; Grisanti, S.K.; Henke-Fahle, S. The Rho-Kinase Inhibitor H-1152P Suppresses the Wound-Healing Activities of Human Tenon’s Capsule Fibroblasts In Vitro. Investig. Ophthalmol. Vis. Sci. 2007, 48, 2152. [Google Scholar] [CrossRef]
- Rasband, W. ImageJ. U S National Institutes of Health, Bethesda, Maryland, USA. 2014. Available online: http://imagej.nih.gov/ij/ (accessed on 15 July 2019).
- Green, E.; Wilkins, M.; Bunce, C.; Wormald, R. 5-Fluorouracil for glaucoma surgery. Cochrane Database Syst. Rev. 2014, 2, CD001132. [Google Scholar] [CrossRef]
- Mietz, H.; Krieglstein, G.K. Postoperative application of mitomycin c improves the complete success rate of primary trabeculectomy: A prospective, randomized trial. Graefe’s archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv für klinische und experimentelle. Ophthalmologie 2006, 244, 1429–1436. [Google Scholar]
- Skuta, G.L.; Beeson, C.C.; Higginbotham, E.J.; Lichter, P.R.; Musch, D.; Bergstrom, T.J.; Klein, T.B.; Falck, F.Y. Intraoperative Mitomycin versus Postoperative 5-Fluorouracil in High-risk Glaucoma Filtering Surgery. Ophthalmology 1992, 99, 438–444. [Google Scholar] [CrossRef]
- Chen, C.W.; Huang, H.T.; Bair, J.S.; Lee, C.C. Trabeculectomy with simultaneous topical application of mitomycin-C in refractory glaucoma. J. Ocul. Pharmacol. 1990, 6, 175–182. [Google Scholar] [CrossRef]
- Crowston, J.G.; Akbar, A.N.; Constable, P.H.; Occleston, N.L.; Daniels, J.T.; Khaw, P.T. Antimetabolite-induced apoptosis in Tenon’s capsule fibroblasts. Investig. Ophthalmol. Vis. Sci. 1998, 39, 449–454. [Google Scholar]
- Khaw, P.T.; Migdal, C.S. Current techniques in wound healing modulation in glaucoma surgery. Curr. Opin. Ophthalmol. 1996, 7, 24–33. [Google Scholar] [CrossRef]
- Turgut, B.; Eren, K.; Akin, M.M.; Bilir Can, N.; Demir, T. Impact of trastuzumab on wound healing in experimental glaucoma surgery. Clin. Exp. Ophthalmol. 2014, 43, 67–76. [Google Scholar] [CrossRef]
- Grisanti, S.; Szurman, P.; Warga, M.; Kaczmarek, R.; Ziemssen, F.; Tatar, O.; Bartz-Schmidt, K.U. Decorin Modulates Wound Healing in Experimental Glaucoma Filtration Surgery: A Pilot Study. Investig. Ophtalmol. Vis. Sci. 2005, 46, 191–196. [Google Scholar] [CrossRef] [Green Version]
- Nassar, K.; Tura, A.; Lüke, J.; Lüke, M.; Grisanti, S.; Grisanti, S. A p38 MAPK Inhibitor Improves Outcome After Glaucoma Filtration Surgery. J. Glaucoma 2014. [Google Scholar] [CrossRef]
- Siddique, S.; Shah, Z.H.; Shahid, S.; Yasmin, F. Preparation, characterization and antibacterial activity of ZnO nanoparticles on broad spectrum of microorganisms. Acta Chim. Slov. 2013, 60, 660–665. [Google Scholar]
- Choi, S.J.; Choy, J.H. Biokinetics of zinc oxide nanoparticles: Toxicokinetics, biological fates, and protein interaction. Int. J. Nanomed. 2014, 9, 261–269. [Google Scholar]
- Gogos, A.; Thalmann, B.A.; Kaegi, R. Sulfidation kinetics of copper oxide nanoparticles. Env. Sci Nano 2017, 4, 1733–1741. [Google Scholar] [CrossRef]
- Lowry, G.V.; Gregory, K.B.; Apte, S.C.; Lead, J.R. Transformations of Nanomaterials in the Environment. Environ. Sci. Technol. 2012, 46, 6893–6899. [Google Scholar] [CrossRef]
- Ma, R.; Stegemeier, J.; Levard, C.; Dale, J.G.; Noack, C.W.; Yang, T.; Brown, G.E.; Lowry, G.V. Sulfidation of copper oxide nanoparticles and properties of resulting copper sulfide. Environ. Sci. Nano 2014, 1, 347–357. [Google Scholar] [CrossRef]
- Wang, M.; Yang, Q.; Long, J.; Ding, Y.; Zou, X.; Liao, G.; Cao, Y. A comparative study of toxicity of TiO2, ZnO, and Ag nanoparticles to human aortic smooth-muscle cells. Int. J. Nanomed. 2018, 13, 8037–8049. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.; Sigmund, W. ZnO nanocrystals synthesized by physical vapor deposition. J. Nanosci. Nanotechnol. 2004, 4, 275–278. [Google Scholar] [CrossRef]
- Mishra, Y.K.; Modi, G.; Cretu, V.; Postica, V.; Lupan, O.; Reimer, T.; Paulowicz, I.; Hrkac, V.; Benecke, W.; Kienle, L.; et al. Direct Growth of Freestanding ZnO Tetrapod Networks for Multifunctional Applications in Photocatalysis, UV Photodetection, and Gas Sensing. ACS Appl. Mater. Interfaces 2015, 7, 14303–14316. [Google Scholar] [CrossRef] [PubMed]
- Mishra, Y.K.; Adelung, R. ZnO tetrapod materials for functional applications. Mater. Today 2018, 21, 631–651. [Google Scholar] [CrossRef]
- Msaki, A.; Sanchez, A.M.; Koh, L.F.; Barré, B.; Rocha, S.; Perkins, N.D.; Johnson, R.F. The role of RelA (p65) threonine 505 phosphorylation in the regulation of cell growth, survival, and migration. Mol. Biol. Cell 2011, 22, 3032–3040. [Google Scholar] [CrossRef] [Green Version]
- Kole, T.P.; Tseng, Y.; Jiang, I.; Katz, J.L.; Wirtz, D. Intracellular mechanics of migrating fibroblasts. Mol. Biol. Cell 2005, 16, 328–338. [Google Scholar] [CrossRef]
- Raffa, V.; Taccola, L.; Riggio, C.; Vittorio, O.; Iorio, M.C.; Pietrabissa, A.; Cuschieri, A. Zinc oxide nanoparticles as selective killers of proliferating cells. Int. J. Nanomed. 2011, 6, 1129–1140. [Google Scholar] [CrossRef] [Green Version]
- Nakamura, T.; Mizuno, S. The discovery of hepatocyte growth factor (HGF) and its significance for cell biology, life sciences and clinical medicine. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. Jan. 2010, 86, 588–610. [Google Scholar] [CrossRef] [Green Version]
- Sehgal, P.B. Interleukin-6: Molecular pathophysiology. J. Investig. Dermatol. 1990, 94, 2S–6S. [Google Scholar] [CrossRef] [Green Version]
- Huang, Z.; Zheng, X.; Yan, D.; Yin, G.; Liao, X.; Kang, Y.; Yao, Y.; Huang, D.; Hao, B. Toxicological Effect of ZnO Nanoparticles Based on Bacteria. Langmuir 2008, 24, 4140–4144. [Google Scholar] [CrossRef]
- Reddy, K.M.; Feris, K.; Bell, J.; Wingett, D.G.; Hanley, C.; Punnoose, A. Selective toxicity of zinc oxide nanoparticles to prokaryotic and eukaryotic systems. Appl. Phys. Lett. 2007, 90, 2139021–2139023. [Google Scholar] [CrossRef] [Green Version]
- Yamamoto, T. Bleb-related infection: Clinical features and management. Taiwan J. Ophthalmol. 2012, 2, 2–5. [Google Scholar] [CrossRef] [Green Version]
- Ba′arah, B.T.; Smiddy, W.E. Bleb-related Endophthalmitis: Clinical Presentation, Isolates, Treatment and Visual Outcome of Culture-proven Cases. Middle East Afr. J. Ophthalmol. 2009, 16, 20–24. [Google Scholar] [CrossRef] [Green Version]
- Rajput, V.; Minkina, T.; Sushkova, S.; Behal, A.; Maksimov, A.; Blicharska, E.; Ghazaryan, K.; Movsesyan, H.; Barsova, N. ZnO and CuO nanoparticles: A threat to soil organisms, plants, and human health. Environ. Geochem. Health 2019, 42, 147–158. [Google Scholar] [CrossRef]
- Cousins, S.W.; McCabe, M.M.; Danielpour, D.; Streilein, J.W. Identification of transforming growth factor-beta as an immunosuppressive factor in aqueous humor. Invest. Ophthalmol. Vis. Sci. 1991, 32, 2201–2211. [Google Scholar]
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Sonntag, S.R.; Gniesmer, S.; Gapeeva, A.; Adelung, R.; Cojocaru, A.; Mishra, Y.K.; Kaps, S.; Tura, A.; Grisanti, S.; Grisanti, S.; et al. Zinc Oxide Tetrapods Modulate Wound Healing and Cytokine Release In Vitro—A New Antiproliferative Substance in Glaucoma Filtering Surgery. Life 2022, 12, 1691. https://doi.org/10.3390/life12111691
Sonntag SR, Gniesmer S, Gapeeva A, Adelung R, Cojocaru A, Mishra YK, Kaps S, Tura A, Grisanti S, Grisanti S, et al. Zinc Oxide Tetrapods Modulate Wound Healing and Cytokine Release In Vitro—A New Antiproliferative Substance in Glaucoma Filtering Surgery. Life. 2022; 12(11):1691. https://doi.org/10.3390/life12111691
Chicago/Turabian StyleSonntag, Svenja Rebecca, Stefanie Gniesmer, Anna Gapeeva, Rainer Adelung, Ala Cojocaru, Yogendra Kumar Mishra, Sören Kaps, Aysegül Tura, Swaantje Grisanti, Salvatore Grisanti, and et al. 2022. "Zinc Oxide Tetrapods Modulate Wound Healing and Cytokine Release In Vitro—A New Antiproliferative Substance in Glaucoma Filtering Surgery" Life 12, no. 11: 1691. https://doi.org/10.3390/life12111691