Copper Oxide Nanoparticle-Induced Acute Inflammatory Response and Injury in Murine Lung Is Ameliorated by Synthetic Secoisolariciresinol Diglucoside (LGM2605)
Abstract
:1. Introduction
2. Results
2.1. Characterization of CuO-NPs and Carbon Black M120
2.2. Kinetics of CuO-NP-Induced Acute Lung Injury in Mice
2.3. LGM2605 Treatment Reduces Lung Injury and Inflammation Following CuO-NP Exposure
2.4. LGM2605 Treatment Reduces Protein Chlorination in Murine Lung Following CuO-NP Exposure
2.5. CuO-NPs Induce ACS Generation by Activation of Myeoloperoxidase (MPO)
2.6. LGM2605 Treatment Mitigates CuO-NP-Induced Acute Lung Inflammation and Injury When Administered Post-CuO-NP Exposure
3. Discussion
4. Materials and Methods
4.1. Nanoparticles
4.2. Dynamic Light Scattering (DLS) and Nanoparticle Tracking Analysis (NTA) for Characterization of Nanoparticles
4.3. Transmission Electron Microscopy (TEM) Characterization of Size/Shape of Nanoparticle Probes
4.4. Mouse Exposure to CuO-NP
4.5. LGM2605 Treatment
4.6. Analytical Evaluation of Lignan Content in Murine Plasma Samples
4.7. Evaluation of Lung Injury
4.8. Analytical Determination of Chlorotyrosine and 3,5-Dichlorotyrosine in Murine Lung
4.9. Determination of BALF Inflammasome-relevant Cytokine Levels
4.10. Western Blot Analysis
4.11. Isolation of Mouse Bone Marrow Neutrophils
4.12. Determination of MPO-Dependent ACS Generation
4.13. Statistical Analysis of the Data
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Conflicts of Interest
References
- Ingle, A.P.; Duran, N.; Rai, M. Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: A review. Appl. Microbiol. Biotechnol. 2014, 98, 1001–1009. [Google Scholar] [CrossRef] [PubMed]
- Akhtar, M.J.; Kumar, S.; Alhadlaq, H.A.; Alrokayan, S.A.; Abu-Salah, K.M.; Ahamed, M. Dose-dependent genotoxicity of copper oxide nanoparticles stimulated by reactive oxygen species in human lung epithelial cells. Toxicol. Ind. Health 2013, 32, 809–821. [Google Scholar] [CrossRef]
- Pandey, A.; Brovelli, S.; Viswanatha, R.; Li, L.; Pietryga, J.M.; Klimov, V.I.; Crooker, S.A. Long-lived photoinduced magnetization in copper-doped ZnSe-CdSe core-shell nanocrystals. Nat. Nanotechnol. 2012, 7, 792–797. [Google Scholar] [CrossRef]
- Ren, X.; Li, J.; Tan, X.; Wang, X. Comparative study of graphene oxide, activated carbon and carbon nanotubes as adsorbents for copper decontamination. Dalton Trans. 2013, 42, 5266–5274. [Google Scholar] [CrossRef]
- Ahamed, M.; Akhtar, M.J.; Alhadlaq, H.A.; Alrokayan, S.A. Assessment of the lung toxicity of copper oxide nanoparticles: Current status. Nanomedicine 2015, 10, 2365–2377. [Google Scholar] [CrossRef] [PubMed]
- Ahamed, M.; Siddiqui, M.A.; Akhtar, M.J.; Ahmad, I.; Pant, A.B.; Alhadlaq, H.A. Genotoxic potential of copper oxide nanoparticles in human lung epithelial cells. Biochem. Biophys. Res. Commun. 2010, 396, 578–583. [Google Scholar] [CrossRef] [PubMed]
- Kwon, J.Y.; Koedrith, P.; Seo, Y.R. Current investigations into the genotoxicity of zinc oxide and silica nanoparticles in mammalian models in vitro and in vivo: Carcinogenic/genotoxic potential, relevant mechanisms and biomarkers, artifacts, and limitations. Int. J. Nanomed. 2014, 9 (Suppl. 2), 271–286. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.; Wadia, C.; Ma, W.; Sadtler, B.; Alivisatos, A.P. Synthesis and photovoltaic application of copper(I) sulfide nanocrystals. Nano Lett. 2008, 8, 2551–2555. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.; Choi, J.R.; Lee, K.J.; Stott, N.E.; Kim, D. Large-scale synthesis of copper nanoparticles by chemically controlled reduction for applications of inkjet-printed electronics. Nanotechnology 2008, 19, 415604. [Google Scholar] [CrossRef]
- Ren, G.; Hu, D.; Cheng, E.W.; Vargas-Reus, M.A.; Reip, P.; Allaker, R.P. Characterisation of copper oxide nanoparticles for antimicrobial applications. Int. J. Antimicrob. Agents 2009, 33, 587–590. [Google Scholar] [CrossRef]
- Maithreepala, R.A.; Doong, R.A. Reductive dechlorination of carbon tetrachloride in aqueous solutions containing ferrous and copper ions. Env. Sci. Technol. 2004, 38, 6676–6684. [Google Scholar] [CrossRef] [PubMed]
- Karlsson, H.L.; Cronholm, P.; Gustafsson, J.; Moller, L. Copper oxide nanoparticles are highly toxic: A comparison between metal oxide nanoparticles and carbon nanotubes. Chem. Res. Toxicol. 2008, 21, 1726–1732. [Google Scholar] [CrossRef] [PubMed]
- Fahmy, B.; Cormier, S.A. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol. Vitr. Int. J. Publ. Assoc. BIBRA 2009, 23, 1365–1371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, R.; Nagesha, D.K. Size-dependent study of pulmonary responses to nano-sized iron and copper oxide nanoparticles. Methods Mol. Biol. 2013, 1028, 247–264. [Google Scholar] [CrossRef]
- Worthington, K.L.; Adamcakova-Dodd, A.; Wongrakpanich, A.; Mudunkotuwa, I.A.; Mapuskar, K.A.; Joshi, V.B.; Allan Guymon, C.; Spitz, D.R.; Grassian, V.H.; Thorne, P.S.; et al. Chitosan coating of copper nanoparticles reduces in vitro toxicity and increases inflammation in the lung. Nanotechnology 2013, 24, 395101. [Google Scholar] [CrossRef] [Green Version]
- Park, J.W.; Lee, I.C.; Shin, N.R.; Jeon, C.M.; Kwon, O.K.; Ko, J.W.; Kim, J.C.; Oh, S.R.; Shin, I.S.; Ahn, K.S. Copper oxide nanoparticles aggravate airway inflammation and mucus production in asthmatic mice via MAPK signaling. Nanotoxicology 2016, 10, 445–452. [Google Scholar] [CrossRef] [PubMed]
- Gosens, I.; Cassee, F.R.; Zanella, M.; Manodori, L.; Brunelli, A.; Costa, A.L.; Bokkers, B.G.; de Jong, W.H.; Brown, D.; Hristozov, D.; et al. Organ burden and pulmonary toxicity of nano-sized copper (II) oxide particles after short-term inhalation exposure. Nanotoxicology 2016, 10, 1084–1095. [Google Scholar] [CrossRef]
- Kim, J.S.; Adamcakova-Dodd, A.; O’Shaughnessy, P.T.; Grassian, V.H.; Thorne, P.S. Effects of copper nanoparticle exposure on host defense in a murine pulmonary infection model. Part. Fibre Toxicol. 2011, 8, 29. [Google Scholar] [CrossRef] [Green Version]
- Adamcakova-Dodd, A.; Monick, M.M.; Powers, L.S.; Gibson-Corley, K.N.; Thorne, P.S. Effects of prenatal inhalation exposure to copper nanoparticles on murine dams and offspring. Part. Fibre Toxicol. 2015, 12, 30. [Google Scholar] [CrossRef] [Green Version]
- Pettibone, J.M.; Adamcakova-Dodd, A.; Thorne, P.S.; O’Shaughnessy, P.T.; Weydert, J.A.; Grassian, V.H. Inflammatory response of mice following inhalation exposure to iron and copper nanoparticles. Nanotoxicology 2008, 2, 189–204. [Google Scholar] [CrossRef]
- Zhang, H.; Ji, Z.; Xia, T.; Meng, H.; Low-Kam, C.; Liu, R.; Pokhrel, S.; Lin, S.; Wang, X.; Liao, Y.P.; et al. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 2012, 6, 4349–4368. [Google Scholar] [CrossRef]
- Mudunkotuwa, I.A.; Pettibone, J.M.; Grassian, V.H. Environmental implications of nanoparticle aging in the processing and fate of copper-based nanomaterials. Environ. Sci. Technol. 2012, 46, 7001–7010. [Google Scholar] [CrossRef]
- Li, Y.; Zhang, W.; Niu, J.; Chen, Y. Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano 2012, 6, 5164–5173. [Google Scholar] [CrossRef]
- Applerot, G.; Lellouche, J.; Lipovsky, A.; Nitzan, Y.; Lubart, R.; Gedanken, A.; Banin, E. Understanding the antibacterial mechanism of CuO nanoparticles: Revealing the route of induced oxidative stress. Small 2012, 8, 3326–3337. [Google Scholar] [CrossRef]
- Gunawan, C.; Teoh, W.Y.; Marquis, C.P.; Amal, R. Cytotoxic origin of copper(II) oxide nanoparticles: Comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano 2011, 5, 7214–7225. [Google Scholar] [CrossRef]
- Studer, A.M.; Limbach, L.K.; Van Duc, L.; Krumeich, F.; Athanassiou, E.K.; Gerber, L.C.; Moch, H.; Stark, W.J. Nanoparticle cytotoxicity depends on intracellular solubility: Comparison of stabilized copper metal and degradable copper oxide nanoparticles. Toxicol. Lett. 2010, 197, 169–174. [Google Scholar] [CrossRef]
- Piret, J.P.; Jacques, D.; Audinot, J.N.; Mejia, J.; Boilan, E.; Noel, F.; Fransolet, M.; Demazy, C.; Lucas, S.; Saout, C.; et al. Copper(II) oxide nanoparticles penetrate into HepG2 cells, exert cytotoxicity via oxidative stress and induce pro-inflammatory response. Nanoscale 2012, 4, 7168–7184. [Google Scholar] [CrossRef] [PubMed]
- Abdelazim, A.M.; Saadeldin, I.M.; Swelum, A.A.; Afifi, M.M.; Alkaladi, A. Oxidative Stress in the Muscles of the Fish Nile Tilapia Caused by Zinc Oxide Nanoparticles and Its Modulation by Vitamins C and E. Oxid. Med. Cell. Longev. 2018, 2018, 6926712. [Google Scholar] [CrossRef] [PubMed]
- Mishra, O.P.; Popov, A.V.; Pietrofesa, R.A.; Christofidou-Solomidou, M. Gamma-irradiation produces active chlorine species (ACS) in physiological solutions: Secoisolariciresinol diglucoside (SDG) scavenges ACS—A novel mechanism of DNA radioprotection. Biochim. Biophys. Acta 2016, 1860, 1884–1897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mishra, O.P.; Popov, A.V.; Pietrofesa, R.A.; Hwang, W.T.; Andrake, M.; Nakamaru-Ogiso, E.; Christofidou-Solomidou, M. Radiation activates myeloperoxidase (MPO) to generate active chlorine species (ACS) via a dephosphorylation mechanism—Inhibitory effect of LGM2605. Biochim. Biophys. Acta Gen. Subj. 2020, 1864, 129548. [Google Scholar] [CrossRef] [PubMed]
- Mishra, O.P.; Popov, A.V.; Pietrofesa, R.A.; Nakamaru-Ogiso, E.; Andrake, M.; Christofidou-Solomidou, M. Synthetic secoisolariciresinol diglucoside (LGM2605) inhibits myeloperoxidase activity in inflammatory cells. Biochim. Biophys. Acta 2018, 1862, 1364–1375. [Google Scholar] [CrossRef]
- Chibber, S.; Shanker, R. Can CuO nanoparticles lead to epigenetic regulation of antioxidant enzyme system? J. Appl. Toxicol. 2017, 37, 84–91. [Google Scholar] [CrossRef] [PubMed]
- Mishra, O.P.; Pietrofesa, R.; Christofidou-Solomidou, M. Novel synthetic (S,S) and (R,R)-secoisolariciresinol diglucosides (SDGs) protect naked plasmid and genomic DNA From gamma radiation damage. Radiat. Res. 2014, 182, 102–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietrofesa, R.A.; Chatterjee, S.; Park, K.; Arguiri, E.; Albelda, S.M.; Christofidou-Solomidou, M. Synthetic Lignan Secoisolariciresinol Diglucoside (LGM2605) Reduces Asbestos-Induced Cytotoxicity in an Nrf2-Dependent and -Independent Manner. Antioxidants 2018, 7, 38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietrofesa, R.A.; Velalopoulou, A.; Albelda, S.M.; Christofidou-Solomidou, M. Asbestos Induces Oxidative Stress and Activation of Nrf2 Signaling in Murine Macrophages: Chemopreventive Role of the Synthetic Lignan Secoisolariciresinol Diglucoside (LGM2605). Int. J. Mol. Sci. 2016, 17, 322. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietrofesa, R.A.; Woodruff, P.; Hwang, W.T.; Patel, P.; Chatterjee, S.; Albelda, S.M.; Christofidou-Solomidou, M. The Synthetic Lignan Secoisolariciresinol Diglucoside Prevents Asbestos-Induced NLRP3 Inflammasome Activation in Murine Macrophages. Oxid. Med. Cell. Longev. 2017, 2017, 7395238. [Google Scholar] [CrossRef] [Green Version]
- Velalopoulou, A.; Chatterjee, S.; Pietrofesa, R.A.; Koziol-White, C.; Panettieri, R.A.; Lin, L.; Tuttle, S.; Berman, A.; Koumenis, C.; Christofidou-Solomidou, M. Synthetic Secoisolariciresinol Diglucoside (LGM2605) Protects Human Lung in an Ex Vivo Model of Proton Radiation Damage. Int. J. Mol. Sci. 2017, 18, 2525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Velalopoulou, A.; Tyagi, S.; Pietrofesa, R.A.; Arguiri, E.; Christofidou-Solomidou, M. The Flaxseed-Derived Lignan Phenolic Secoisolariciresinol Diglucoside (SDG) Protects Non-Malignant Lung Cells from Radiation Damage. Int. J. Mol. Sci. 2016, 17, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, W.; von dem Bussche, A.; Yi, X.; Qiu, Y.; Wang, Z.; Weston, P.; Hurt, R.H.; Kane, A.B.; Gao, H. Nanomechanical mechanism for lipid bilayer damage induced by carbon nanotubes confined in intracellular vesicles. Proc. Natl. Acad. Sci. USA 2016, 113, 12374–12379. [Google Scholar] [CrossRef] [Green Version]
- Greenwell, L.L.; Moreno, T.; Jones, T.P.; Richards, R.J. Particle-induced oxidative damage is ameliorated by pulmonary antioxidants. Free Radic. Biol. Med. 2002, 32, 898–905. [Google Scholar] [CrossRef]
- Wang, Z.; von dem Bussche, A.; Kabadi, P.K.; Kane, A.B.; Hurt, R.H. Biological and environmental transformations of copper-based nanomaterials. ACS Nano 2013, 7, 8715–8727. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Christofidou-Solomidou, M.; Pietrofesa, R.A.; Park, K.; Albelda, S.M.; Serve, K.M.; Keil, D.E.; Pfau, J.C. Synthetic secoisolariciresinol diglucoside (LGM2605) inhibits Libby amphibole fiber-induced acute inflammation in mice. Toxicol. Appl. Pharmacol. 2019, 375, 81–93. [Google Scholar] [CrossRef] [PubMed]
- Senapati, V.A.; Kumar, A.; Gupta, G.S.; Pandey, A.K.; Dhawan, A. ZnO nanoparticles induced inflammatory response and genotoxicity in human blood cells: A mechanistic approach. Food Chem. Toxicol. 2015, 85, 61–70. [Google Scholar] [CrossRef] [PubMed]
- Crow, B.S.; Quinones-Gonzalez, J.; Pantazides, B.G.; Perez, J.W.; Winkeljohn, W.R.; Garton, J.W.; Thomas, J.D.; Blake, T.A.; Johnson, R.C. Simultaneous Measurement of 3-Chlorotyrosine and 3,5-Dichlorotyrosine in Whole Blood, Serum and Plasma by Isotope Dilution HPLC-MS-MS. J. Anal. Toxicol. 2016, 40, 264–271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chatterjee, S.; Pietrofesa, R.A.; Park, K.; Tao, J.Q.; Carabe-Fernandez, A.; Berman, A.T.; Koumenis, C.; Sielecki, T.; Christofidou-Solomidou, M. LGM2605 Reduces Space Radiation-Induced NLRP3 Inflammasome Activation and Damage in In Vitro Lung Vascular Networks. Int. J. Mol. Sci. 2019, 20, 176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietrofesa, R.A.; Velalopoulou, A.; Arguiri, E.; Menges, C.W.; Testa, J.R.; Hwang, W.T.; Albelda, S.M.; Christofidou-Solomidou, M. Flaxseed lignans enriched in secoisolariciresinol diglucoside prevent acute asbestos-induced peritoneal inflammation in mice. Carcinogenesis 2016, 37, 177–187. [Google Scholar] [CrossRef] [Green Version]
- Larson, T.C.; Lewin, M.; Gottschall, E.B.; Antao, V.C.; Kapil, V.; Rose, C.S. Associations between radiographic findings and spirometry in a community exposed to Libby amphibole. Occup. Environ. Med. 2012, 69, 361–366. [Google Scholar] [CrossRef] [PubMed]
- Miller, A.; Szeinuk, J.; Noonan, C.W.; Henschke, C.I.; Pfau, J.; Black, B.; Yankelevitz, D.F.; Liang, M.; Liu, Y.; Yip, R.; et al. Libby Amphibole Disease: Pulmonary Function and CT Abnormalities in Vermiculite Miners. J. Occup. Environ. Med. 2018, 60, 167–173. [Google Scholar] [CrossRef]
- Whitehouse, A.C.; Black, C.B.; Heppe, M.S.; Ruckdeschel, J.; Levin, S.M. Environmental exposure to Libby Asbestos and mesotheliomas. Am. J. Ind. Med. 2008, 51, 877–880. [Google Scholar] [CrossRef]
- Szeinuk, J.; Noonan, C.W.; Henschke, C.I.; Pfau, J.; Black, B.; Miller, A.; Yankelevitz, D.F.; Liang, M.; Liu, Y.; Yip, R.; et al. Pulmonary abnormalities as a result of exposure to Libby amphibole during childhood and adolescence-The Pre-Adult Latency Study (PALS). Am. J. Ind. Med. 2017, 60, 20–34. [Google Scholar] [CrossRef]
- Diegel, R.; Black, B.; Pfau, J.C.; McNew, T.; Noonan, C.; Flores, R. Case series: Rheumatological manifestations attributed to exposure to Libby Asbestiform Amphiboles. J. Toxicol. Environ. Health A 2018, 81, 734–747. [Google Scholar] [CrossRef] [Green Version]
- Yang, E.J.; Kim, S.; Kim, J.S.; Choi, I.H. Inflammasome formation and IL-1beta release by human blood monocytes in response to silver nanoparticles. Biomaterials 2012, 33, 6858–6867. [Google Scholar] [CrossRef]
- Simard, J.C.; Vallieres, F.; de Liz, R.; Lavastre, V.; Girard, D. Silver nanoparticles induce degradation of the endoplasmic reticulum stress sensor activating transcription factor-6 leading to activation of the NLRP-3 inflammasome. J. Biol. Chem. 2015, 290, 5926–5939. [Google Scholar] [CrossRef] [Green Version]
- Sager, T.M.; Wolfarth, M.; Leonard, S.S.; Morris, A.M.; Porter, D.W.; Castranova, V.; Holian, A. Role of engineered metal oxide nanoparticle agglomeration in reactive oxygen species generation and cathepsin B release in NLRP3 inflammasome activation and pulmonary toxicity. Inhal. Toxicol. 2016, 28, 686–697. [Google Scholar] [CrossRef]
- Minigalieva, I.A.; Katsnelson, B.A.; Panov, V.G.; Privalova, L.I.; Varaksin, A.N.; Gurvich, V.B.; Sutunkova, M.P.; Shur, V.Y.; Shishkina, E.V.; Valamina, I.E.; et al. In vivo toxicity of copper oxide, lead oxide and zinc oxide nanoparticles acting in different combinations and its attenuation with a complex of innocuous bio-protectors. Toxicology 2017, 380, 72–93. [Google Scholar] [CrossRef] [PubMed]
- Jeong, J.; Kim, J.; Seok, S.H.; Cho, W.S. Indium oxide (In2O3) nanoparticles induce progressive lung injury distinct from lung injuries by copper oxide (CuO) and nickel oxide (NiO) nanoparticles. Arch. Toxicol. 2016, 90, 817–828. [Google Scholar] [CrossRef] [PubMed]
- Jeitner, T.; Lawrence, D. Pulmonary autoimmunity and inflammation. In Pulmonary Immunotoxicology; Cohen, M.D., Zelikoff, J.T., Schlesinger, R.B., Eds.; Kluwer Academic Publishers: New York, NY, USA, 2000; pp. 153–179. [Google Scholar]
- Malle, E.; Furtmuller, P.G.; Sattler, W.; Obinger, C. Myeloperoxidase: A target for new drug development? Br. J. Pharmacol. 2007, 152, 838–854. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nauseef, W.M. Myeloperoxidase in human neutrophil host defence. Cell. Microbiol. 2014, 16, 1146–1155. [Google Scholar] [CrossRef] [Green Version]
- Hawkins, C.L.; Davies, M.J. Hypochlorite-Induced Damage to DNA, RNA, and Polynucleotides: Formation of Chloramines and Nitrogen-Centered Radicals. Chem. Res. Toxicol. 2002, 15, 83–92. [Google Scholar] [CrossRef]
- Hawkins, C.L.; Pattison, D.I.; Davies, M.J. Hypochlorite-induced oxidation of amino acids, peptides and proteins. Amino. Acids 2003, 25, 259–274. [Google Scholar] [CrossRef]
- Cadet, J.; Wagner, J.R. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb. Perspect. Biol. 2013, 5, A012559/012551–A012559/012518. [Google Scholar] [CrossRef]
- Jeitner, T.M.; Xu, H.; Gibson, G.E. Inhibition of the α-ketoglutarate dehydrogenase complex by the myeloperoxidase products, hypochlorous acid and mono-N-chloramine. J. Neurochem. 2005, 92, 302–310. [Google Scholar] [CrossRef]
- Masuda, M.; Suzuki, T.; Friesen, M.D.; Ravanat, J.-L.; Cadet, J.; Pignatelli, B.; Nishino, H.; Ohshima, H. Chlorination of guanosine and other nucleosides by hypochlorous acid and myeloperoxidase of activated human neutrophils: Catalysis by nicotine and trimethylamine. J. Biol. Chem. 2001, 276, 40486–40496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Badouard, C.; Masuda, M.; Nishino, H.; Cadet, J.; Favier, A.; Ravanat, J.-L. Detection of chlorinated DNA and RNA nucleosides by HPLC coupled to tandem mass spectrometry as potential biomarkers of inflammation. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2005, 827, 26–31. [Google Scholar] [CrossRef] [PubMed]
- Southam, D.S.; Dolovich, M.; O’Byrne, P.M.; Inman, M.D. Distribution of intranasal instillations in mice: Effects of volume, time, body position, and anesthesia. Am. J. Physiology. Lung Cell. Mol. Physiol. 2002, 282, L833–L839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lai, X.; Zhao, H.; Zhang, Y.; Guo, K.; Xu, Y.; Chen, S.; Zhang, J. Intranasal Delivery of Copper Oxide Nanoparticles Induces Pulmonary Toxicity and Fibrosis in C57BL/6 mice. Sci. Rep. 2018, 8, 4499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mishra, O.P.; Simmons, N.; Tyagi, S.; Pietrofesa, R.; Shuvaev, V.V.; Valiulin, R.A.; Heretsch, P.; Nicolaou, K.C.; Christofidou-Solomidou, M. Synthesis and antioxidant evaluation of (S,S)- and (R,R)-secoisolariciresinol diglucosides (SDGs). Bioorg. Med. Chem. Lett. 2013, 23, 5325–5328. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.C.; Kinniry, P.A.; Arguiri, E.; Serota, M.; Kanterakis, S.; Chatterjee, S.; Solomides, C.C.; Javvadi, P.; Koumenis, C.; Cengel, K.A.; et al. Dietary curcumin increases antioxidant defenses in lung, ameliorates radiation-induced pulmonary fibrosis, and improves survival in mice. Radiat. Res. 2010, 173, 590–601. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.C.; Krochak, R.; Blouin, A.; Kanterakis, S.; Chatterjee, S.; Arguiri, E.; Vachani, A.; Solomides, C.C.; Cengel, K.A.; Christofidou-Solomidou, M. Dietary flaxseed prevents radiation-induced oxidative lung damage, inflammation and fibrosis in a mouse model of thoracic radiation injury. Cancer Biol. 2009, 8, 47–53. [Google Scholar] [CrossRef] [Green Version]
- Chikara, S.; Mamidi, S.; Sreedasyam, A.; Chittem, K.; Pietrofesa, R.; Zuppa, A.; Moorthy, G.; Dyer, N.; Christofidou-Solomidou, M.; Reindl, K.M. Flaxseed Consumption Inhibits Chemically Induced Lung Tumorigenesis and Modulates Expression of Phase II Enzymes and Inflammatory Cytokines in A/J Mice. Cancer Prev. Res. 2018, 11, 27–37. [Google Scholar] [CrossRef] [Green Version]
- Pietrofesa, R.A.; Solomides, C.C.; Christofidou-Solomidou, M. Flaxseed Mitigates Acute Oxidative Lung Damage in a Mouse Model of Repeated Radiation and Hyperoxia Exposure Associated with Space Exploration. J. Pulm. Respir. Med. 2014, 4, 1000215. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.C.; Bhora, F.; Sun, J.; Cheng, G.; Arguiri, E.; Solomides, C.C.; Chatterjee, S.; Christofidou-Solomidou, M. Dietary flaxseed enhances antioxidant defenses and is protective in a mouse model of lung ischemia-reperfusion injury. Am. J. Physiology. Lung Cell. Mol. Physiol. 2008, 294, L255–L265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swamydas, M.; Lionakis, M.S. Isolation, purification and labeling of mouse bone marrow neutrophils for functional studies and adoptive transfer experiments. J. Vis. Exp. 2013, 77, e50586. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pietrofesa, R.A.; Park, K.; Mishra, O.P.; Johnson-McDaniel, D.; Myerson, J.W.; Shuvaev, V.V.; Arguiri, E.; Chatterjee, S.; Moorthy, G.S.; Zuppa, A.; et al. Copper Oxide Nanoparticle-Induced Acute Inflammatory Response and Injury in Murine Lung Is Ameliorated by Synthetic Secoisolariciresinol Diglucoside (LGM2605). Int. J. Mol. Sci. 2021, 22, 9477. https://doi.org/10.3390/ijms22179477
Pietrofesa RA, Park K, Mishra OP, Johnson-McDaniel D, Myerson JW, Shuvaev VV, Arguiri E, Chatterjee S, Moorthy GS, Zuppa A, et al. Copper Oxide Nanoparticle-Induced Acute Inflammatory Response and Injury in Murine Lung Is Ameliorated by Synthetic Secoisolariciresinol Diglucoside (LGM2605). International Journal of Molecular Sciences. 2021; 22(17):9477. https://doi.org/10.3390/ijms22179477
Chicago/Turabian StylePietrofesa, Ralph A., Kyewon Park, Om P. Mishra, Darrah Johnson-McDaniel, Jacob W. Myerson, Vladimir V. Shuvaev, Evguenia Arguiri, Shampa Chatterjee, Ganesh S. Moorthy, Athena Zuppa, and et al. 2021. "Copper Oxide Nanoparticle-Induced Acute Inflammatory Response and Injury in Murine Lung Is Ameliorated by Synthetic Secoisolariciresinol Diglucoside (LGM2605)" International Journal of Molecular Sciences 22, no. 17: 9477. https://doi.org/10.3390/ijms22179477