Orally delivered resveratrol-loaded lipid-core nanocapsules ameliorate LPS-induced acute lung injury via the ERK and PI3K/Akt pathways

References

• Okin D, Medzhitov R. Evolution of inflammatory diseases. Curr Biol. 2012;22(17):R733–R740. doi:10.1016/j.cub.2012.07.02922975004
   PubMed Web of Science ®Google Scholar
• Hunter P. The inflammation theory of disease. The growing realization that chronic inflammation is crucial in many diseases opens new avenues for treatment. EMBO Rep. 2012;13(11):968–970. doi:10.1038/embor.2012.14223044824
   PubMed Web of Science ®Google Scholar
• Chen H, Bai C, Wang X. The value of the lipopolysaccharide-induced acute lung injury model in respiratory medicine. Expert Rev Respir Med. 2010;4(6):773–783. doi:10.1586/ers.10.7121128752
   PubMedGoogle Scholar
• Mirzapoiazova T, Kolosova IA, Moreno L, Sammani S, Garcia JG, Verin AD. Suppression of endotoxin-induced inflammation by taxol. Eur Respir J. 2007;30(3):429–435. doi:10.1183/09031936.0015420617537765
   PubMed Web of Science ®Google Scholar
• Morris M, Li L. Molecular mechanisms and pathological consequences of endotoxin tolerance and priming. Arch Immunol Ther Exp (Warsz). 2012;60(1):13–18. doi:10.1007/s00005-011-0155-922143158
   PubMed Web of Science ®Google Scholar
• Fard N, Saffari A, Emami G, Hofer S, Kauczor HU, Mehrabi A. Acute respiratory distress syndrome induction by pulmonary ischemia-reperfusion injury in large animal models. J Surg Res. 2014;189(2):274–284. doi:10.1016/j.jss.2014.02.03424768138
   PubMed Web of Science ®Google Scholar
• Boyle AJ, McNamee JJ, McAuley DF. Biological therapies in the acute respiratory distress syndrome. Expert Opin Biol Ther. 2014;14(7):969–981. doi:10.1517/14712598.2014.90553624702248
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Cressoni M, Brazzi L. Fluids in ARDS: from onset through recovery. Curr Opin Crit Care. 2014;20(4):373–377. doi:10.1097/MCC.000000000000010524979554
   PubMedGoogle Scholar
• Fanelli V, Vlachou A, Ghannadian S, Simonetti U, Slutsky AS, Zhang H. Acute respiratory distress syndrome: new definition, current and future therapeutic options. J Thorac Dis. 2013;5(3):326–334. doi:10.3978/j.issn.2072-1439.2013.04.0523825769
   PubMed Web of Science ®Google Scholar
• Takaoka M. Resveratrol, a new phenolic compound, from veratrum grandiflorum. J. Chem. Soc. Jpn.. 1939;60:1090–1100.
   Google Scholar
• Fremont L. Biological effects of resveratrol. Life Sci. 2000;66(8):663–673.10680575
   PubMed Web of Science ®Google Scholar
• Nguyen C, Savouret JF, Widerak M, Corvol MT, Rannou F. Resveratrol, potential therapeutic interest in joint disorders: a critical narrative review. Nutrients. 2017;9(1). doi:10.3390/nu9010045
   Web of Science ®Google Scholar
• Catalgol B, Batirel S, Taga Y, Ozer NK. Resveratrol: French paradox revisited. Front Pharmacol. 2012;3:141. doi:10.3389/fphar.2012.0014122822401
   PubMed Web of Science ®Google Scholar
• Kursvietiene L, Staneviciene I, Mongirdiene A, Bernatoniene J. Multiplicity of effects and health benefits of resveratrol. Medicina (Kaunas). 2016;52(3):148–155. doi:10.1016/j.medici.2016.03.00327496184
   PubMed Web of Science ®Google Scholar
• de Sa Coutinho D, Pacheco MT, Frozza RL, Bernardi A. Anti-inflammatory effects of resveratrol: mechanistic insights. Int J Mol Sci. 2018;19(6). doi:10.3390/ijms19061812
   PubMed Web of Science ®Google Scholar
• Orallo F. Comparative studies of the antioxidant effects of cis- and trans-resveratrol. Curr Med Chem. 2006;13(1):87–98.16457641
   PubMed Web of Science ®Google Scholar
• Augustin MA, Sanguansri L, Lockett T. Nano- and micro-encapsulated systems for enhancing the delivery of resveratrol. Ann N Y Acad Sci. 2013;1290:107–112. doi:10.1111/nyas.1213023855472
   PubMed Web of Science ®Google Scholar
• Trela BC, Waterhouse AL. Resveratrol: isomeric molar absorptivities and stability. J Agric Food Chem. 1996;44(5):1253–1257. doi:10.1021/jf9504576
   Web of Science ®Google Scholar
• Delmas D, Aires V, Limagne E, et al. Transport, stability, and biological activity of resveratrol. Ann N Y Acad Sci. 2011;1215:48–59. doi:10.1111/j.1749-6632.2010.05871.x21261641
   PubMed Web of Science ®Google Scholar
• Pujara N, Jambhrunkar S, Wong KY, McGuckin M, Popat A. Enhanced colloidal stability, solubility and rapid dissolution of resveratrol by nanocomplexation with soy protein isolate. J Colloid Interface Sci. 2017;488:303–308. doi:10.1016/j.jcis.2016.11.01527838554
   PubMed Web of Science ®Google Scholar
• Brittes J, Lucio M, Nunes C, Lima JL, Reis S. Effects of resveratrol on membrane biophysical properties: relevance for its pharmacological effects. Chem Phys Lipids. 2010;163(8):747–754. doi:10.1016/j.chemphyslip.2010.07.00420691168
   PubMedGoogle Scholar
• Pentek T, Newenhouse E, O’Brien B, Chauhan SA. Development of a topical resveratrol formulation for commercial applications using dendrimer nanotechnology. Molecules. 2017;22:1. doi:10.3390/molecules22010137
   Web of Science ®Google Scholar
• Kundu JK, Chun KS, Kim SO, Surh YJ. Resveratrol inhibits phorbol ester-induced cyclooxygenase-2 expression in mouse skin: mAPKs and AP-1 as potential molecular targets. Biofactors. 2004;21(1–4):33–39.15630167
   PubMed Web of Science ®Google Scholar
• Holmes-McNary M, Baldwin AS Jr. Chemopreventive properties of trans-resveratrol are associated with inhibition of activation of the IkappaB kinase. Cancer Res. 2000;60(13):3477–3483.10910059
   PubMed Web of Science ®Google Scholar
• Tung BT, Rodríguez-Bies E, Ballesteros-Simarro M, Motilva V, Navas P, López-Lluch G. Modulation of endogenous antioxidant activity by resveratrol and exercise in mouse liver is age dependent. J Gerontol. 2014;69(4):398–409. doi:10.1093/gerona/glt102
   Google Scholar
• de la Lastra CA, Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem Soc Trans. 2007;35(5):1156–1160. doi:10.1042/BST035115617956300
   PubMed Web of Science ®Google Scholar
• Baxter RA. Anti-aging properties of resveratrol: review and report of a potent new antioxidant skin care formulation. J Cosmet Dermatol. 2008;7(1):2–7. doi:10.1111/j.1473-2165.2008.00354.x18254804
   PubMedGoogle Scholar
• Rauf A, Imran M, Butt MS, Nadeem M, Peters DG, Mubarak MS. Resveratrol as an anticancer agent: a review. Crit Rev Food Sci Nutr. 2018.58:1428–1447.
   PubMed Web of Science ®Google Scholar
• Das S, Das DK. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Targets. 2007;6(3):168–173.17897053
   PubMedGoogle Scholar
• Hung LM, Chen JK, Huang SS, Lee RS, Su MJ. Cardioprotective effect of resveratrol, a natural antioxidant derived from grapes. Cardiovasc Res. 2000;47(3):549–555. doi:10.1016/s0008-6363(00)00102-410963727
   PubMed Web of Science ®Google Scholar
• Planas JM, Alfaras I, Colom H, Juan ME. The bioavailability and distribution of trans-resveratrol are constrained by ABC transporters. Arch Biochem Biophys. 2012;527(2):67–73. doi:10.1016/j.abb.2012.06.00422750234
   PubMed Web of Science ®Google Scholar
• Vargas JE, Souto AA, Pitrez PM, Stein RT, Porto BN. Modulatory potential of resveratrol during lung inflammatory disease. Med Hypotheses. 2016;96:61–65. doi:10.1016/j.mehy.2016.09.02327959278
   PubMed Web of Science ®Google Scholar
• Karthikeyan S, Rajendra Prasad N, Ganamani A, Balamurugan E. Anticancer activity of resveratrol-loaded gelatin nanoparticles on NCI-H460 non-small cell lung cancer cells. Biomed Preventive Med. 2013;3(1):64–73. doi:10.1016/j.bionut.2012.10.009
   Google Scholar
• Coimbra M, Isacchi B, van Bloois L, et al. Improving solubility and chemical stability of natural compounds for medicinal use by incorporation into liposomes. Int J Pharm. 2011;416(2):433–442. doi:10.1016/j.ijpharm.2011.01.05621291975
   PubMed Web of Science ®Google Scholar
• Teskac K, Kristl J. The evidence for solid lipid nanoparticles mediated cell uptake of resveratrol. Int J Pharm. 2010;390(1):61–69. doi:10.1016/j.ijpharm.2009.10.01119833178
   PubMed Web of Science ®Google Scholar
• Lu X, Ji C, Xu H, et al. Resveratrol-loaded polymeric micelles protect cells from Abeta-induced oxidative stress. Int J Pharm. 2009;375(1–2):89–96. doi:10.1016/j.ijpharm.2009.03.02119481694
   PubMedGoogle Scholar
• Frozza RL, Salbego C, Bernardi A, et al. Incorporation of resveratrol into lipid-core nanocapsules improves its cerebral bioavailability and reduces the Aβ-induced toxicity. Alzheimers Dement. 2011;7(4):S114. doi:10.1016/j.jalz.2011.05.286
   Google Scholar
• Cao Q, Jing C, Tang X, Yin Y, Han X, Wu W. Protective effect of resveratrol on acute lung injury induced by lipopolysaccharide in mice. Anat Rec (Hoboken). 2011;294(3):527–532. doi:10.1002/ar.2133121284090
   PubMedGoogle Scholar
• Szarka RJ, Wang N, Gordon L, Nation PN, Smith RH. A murine model of pulmonary damage induced by lipopolysaccharide via intranasal instillation. J Immunol Methods. 1997;202(1):49–57.9075771
   PubMed Web of Science ®Google Scholar
• Apl D, Pacheco de Oliveira MT, de Souza ET, et al. Alpha-bisabolol-loaded lipid-core nanocapsules reduce lipopolysaccharide-induced pulmonary inflammation in mice. Int J Nanomedicine. 2017;12:4479–4491. doi:10.2147/IJN.S13079828684908
   PubMedGoogle Scholar
• Ferreira TP, de Arantes AC, Do Nascimento CV, et al. IL-13 immunotoxin accelerates resolution of lung pathological changes triggered by silica particles in mice. J Immunol. 2013;191(10):5220–5229. doi:10.4049/jimmunol.120355124133168
   PubMed Web of Science ®Google Scholar
• Kummerle AE, Schmitt M, Cardozo SV, et al. Design, synthesis, and pharmacological evaluation of N-acylhydrazones and novel conformationally constrained compounds as selective and potent orally active phosphodiesterase-4 inhibitors. J Med Chem. 2012;55(17):7525–7545. doi:10.1021/jm300514y22891752
   PubMedGoogle Scholar
• Zhu T, Wang DX, Zhang W, et al. Andrographolide protects against LPS-induced acute lung injury by inactivation of NF-kappaB. PLoS One. 2013;8(2):e56407. doi:10.1371/journal.pone.005640723437127
   PubMed Web of Science ®Google Scholar
• Draper HH, Hadley M. [43] Malondialdehyde determination as index of lipid Peroxidation. Methods Enzymol. 1990;186:421–431. Academic Press.2233309
   PubMed Web of Science ®Google Scholar
• Bannister JV, Calabrese L. Assays for superoxide dismutase. Methods Biochem Anal. 1987;32:279–312.3033431
   PubMedGoogle Scholar
• Britton RG, Kovoor C, Brown K. Direct molecular targets of resveratrol: identifying key interactions to unlock complex mechanisms. Ann N Y Acad Sci. 2015;1348(1):124–133. doi:10.1111/nyas.1279626099829
   PubMedGoogle Scholar
• Chedea VS, Vicas SI, Sticozzi C, et al. Resveratrol: from diet to topical usage. Food Funct. 2017;8(11):3879–3892. doi:10.1039/c7fo01086a29034918
   PubMed Web of Science ®Google Scholar
• Pirola L, Frojdo S. Resveratrol: one molecule, many targets. IUBMB Life. 2008;60(5):323–332. doi:10.1002/iub.4718421779
   PubMed Web of Science ®Google Scholar
• Chen G, Roy I, Yang C, Prasad PN. Nanochemistry and nanomedicine for nanoparticle-based diagnostics and therapy. Chem Rev. 2016;116(5):2826–2885. doi:10.1021/acs.chemrev.5b0014826799741
   PubMed Web of Science ®Google Scholar
• Poletto F, Beck R, Guterres S, Pohlmann A. Polymeric nanocapsules: concepts and applications. In: Beck RCR, Guterres SS, Pohlmann, AR, editors. Nanocosmetics and Nanomedicines: New approaches for skin care. Heidelberg: Springer Verlag; 2011:49–68.
   Google Scholar
• Kothamasu P, Kanumur H, Ravur N, Maddu C, Parasuramrajam R, Thangavel S. Nanocapsules: the weapons for novel drug delivery systems. Bioimpacts. 2012;2(2):71–81. doi:10.5681/bi.2012.01123678444
   PubMedGoogle Scholar
• Diaspro A, Krol S, Cavalleri O, Silvano D, Gliozzi A. Microscopical characterization of nanocapsules templated on ionic crystals and biological cells toward biomedical applications. IEEE Trans Nanobioscience. 2002;1(3):110–115.16696300
   PubMedGoogle Scholar
• Zhang Z, Chen N, Liu JB, et al. Protective effect of resveratrol against acute lung injury induced by lipopolysaccharide via inhibiting the myd88-dependent Toll-like receptor 4 signaling pathway. Mol Med Rep. 2014;10(1):101–106. doi:10.3892/mmr.2014.222624818579
   PubMedGoogle Scholar
• Kamaly N, Yameen B, Wu J, Farokhzad OC. Degradable controlled-release polymers and polymeric nanoparticles: mechanisms of controlling drug release. Chem Rev. 2016;116(4):2602–2663. doi:10.1021/acs.chemrev.5b0034626854975
   PubMed Web of Science ®Google Scholar
• Lee JH, Yeo Y. Controlled drug release from pharmaceutical nanocarriers. Chem Eng Sci. 2015;125:75–84. doi:10.1016/j.ces.2014.08.04625684779
   PubMed Web of Science ®Google Scholar
• Lanz-Landazuri A, Portilla-Arias J, Martinez de Ilarduya A, et al. Nanoparticles of esterified polymalic acid for controlled anticancer drug release. Macromol Biosci. 2014;14(9):1325–1336. doi:10.1002/mabi.20140012424902676
   PubMedGoogle Scholar
• Fujishima S. Pathophysiology and biomarkers of acute respiratory distress syndrome. J Intensive Care. 2014;2(1):32. doi:10.1186/2052-0492-2-3225520844
   PubMedGoogle Scholar
• Williams AE, Chambers RC. The mercurial nature of neutrophils: still an enigma in ARDS? Am J Physiol Lung Cell Mol Physiol. 2014;306(3):L217–230. doi:10.1152/ajplung.00311.201324318116
   PubMed Web of Science ®Google Scholar
• Uchiba M, Okajima K, Murakami K, Okabe H, Takatsuki K. Endotoxin-induced pulmonary vascular injury is mainly mediated by activated neutrophils in rats. Thromb Res. 1995;78(2):117–125.7482429
   PubMed Web of Science ®Google Scholar
• Chabot F, Mitchell JA, Gutteridge JM, Evans TW. Reactive oxygen species in acute lung injury. Eur Respir J. 1998;11(3):745–757.9596132
   PubMed Web of Science ®Google Scholar
• Dinarello CA. Historical Review of Cytokines. Eur J Immunol. 2007;37(Suppl 1):S34–S45. doi:10.1002/eji.20073777217972343
   PubMedGoogle Scholar
• Goodman RB, Strieter RM, Martin DP, et al. Inflammatory cytokines in patients with persistence of the acute respiratory distress syndrome. Am J Respir Crit Care Med. 1996;154(3 Pt 1):602–611. doi:10.1164/ajrccm.154.3.88105938810593
   PubMedGoogle Scholar
• De Filippo K, Henderson RB, Laschinger M, Hogg N. Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J Immunol. 2008;180(6):4308–4315. doi:10.4049/jimmunol.180.6.430818322244
   PubMed Web of Science ®Google Scholar
• Pan ZZ, Parkyn L, Ray A, Ray P. Inducible lung-specific expression of RANTES: preferential recruitment of neutrophils. Am J Physiol Lung Cell Mol Physiol. 2000;279(4):L658–666. doi:10.1152/ajplung.2000.279.4.L65811000125
   PubMedGoogle Scholar
• Tumpey TM, Fenton R, Molesworth-Kenyon S, Oakes JE, Lausch RN. Role for macrophage inflammatory protein 2 (MIP-2), MIP-1alpha, and interleukin-1alpha in the delayed-type hypersensitivity response to viral antigen. J Virol. 2002;76(16):8050–8057. doi:10.1128/jvi.76.16.8050-8057.200212134010
   PubMedGoogle Scholar
• Balamayooran G, Batra S, Balamayooran T, Cai S, Jeyaseelan S. Monocyte chemoattractant protein 1 regulates pulmonary host defense via neutrophil recruitment during Escherichia coli infection. Infect Immun. 2011;79(7):2567–2577. doi:10.1128/IAI.00067-1121518788
   PubMed Web of Science ®Google Scholar
• Brass DM, Hollingsworth JW, McElvania-Tekippe E, Garantziotis S, Hossain I, Schwartz DA. CD14 is an essential mediator of LPS-induced airway disease. Am J Physiol Lung Cell Mol Physiol. 2007;293(1):L77–L83. doi:10.1152/ajplung.00282.200617384086
   PubMedGoogle Scholar
• Chow CW, Herrera Abreu MT, Suzuki T, Downey GP. Oxidative stress and acute lung injury. Am J Respir Cell Mol Biol. 2003;29(4):427–431. doi:10.1165/rcmb.F27814500253
   PubMed Web of Science ®Google Scholar
• Gertz M, Nguyen GT, Fischer F, et al. A molecular mechanism for direct sirtuin activation by resveratrol. PLoS One. 2012;7(11):e49761. doi:10.1371/journal.pone.004976123185430
   PubMed Web of Science ®Google Scholar
• Held HD, Uhlig S. Mechanisms of endotoxin-induced airway and pulmonary vascular hyperreactivity in mice. Am J Respir Crit Care Med. 2000;162(4 Pt 1):1547–1552. doi:10.1164/ajrccm.162.4.991207911029375
   PubMedGoogle Scholar
• Gattinoni L, Chiumello D, Carlesso E, Valenza F. Bench-to-bedside review: chest wall elastance in acute lung injury/acute respiratory distress syndrome patients. Crit Care. 2004;8(5):350–355. doi:10.1186/cc285415469597
   PubMed Web of Science ®Google Scholar
• Kim EN, Lim JH, Kim MY, et al. Resveratrol, an Nrf2 activator, ameliorates aging-related progressive renal injury. Aging. 2018;10(1):83–99. doi:10.18632/aging.10136129326403
   PubMedGoogle Scholar
• Yasui K, Kobayashi N, Yamazaki T, et al. Superoxide Dismutase (SOD) as a Potential Inhibitory Mediator of Inflammation via Neutrophil Apoptosis. Free Radic. Res.2005;39(7):755–62.
   Google Scholar
• Wang Y, Wang X, Zhang L, Zhang R. Alleviation of acute lung injury in rats with sepsis by resveratrol via the phosphatidylinositol 3-kinase/nuclear factor-erythroid 2 related factor 2/Heme Oxygenase-1 (PI3K/Nrf2/HO-1) pathway. Med Sci Monit. 2018;24:3604–3611. doi:10.12659/MSM.91024529844304
   PubMedGoogle Scholar
• Spanier G, Xu H, Xia N, et al. Resveratrol reduces endothelial oxidative stress by modulating the gene expression of superoxide dismutase 1 (SOD1), glutathione peroxidase 1 (GPx1) and NADPH oxidase subunit (Nox4). J Physiol Pharmacol. 2009;60(Suppl 4):111–116.
   PubMed Web of Science ®Google Scholar
• Sadi G, Konat D. Resveratrol regulates oxidative biomarkers and antioxidant enzymes in the brain of streptozotocin-induced diabetic rats. Pharm Biol. 2016;54(7):1156–1163. doi:10.3109/13880209.2015.105631126079852
   PubMed Web of Science ®Google Scholar
• Kulkarni SS, Canto C. The molecular targets of resveratrol. Biochim Biophys Acta. 2015;1852(6):1114–1123. doi:10.1016/j.bbadis.2014.10.00525315298
   PubMed Web of Science ®Google Scholar
• Qin X, Jiang X, Wang Y, et al. Micheliolide inhibits LPS-induced inflammatory response and protects mice from LPS challenge. Sci Rep. 2016;6:23240. doi:10.1038/srep2324026984741
   PubMedGoogle Scholar
• Wang X, Quinn PJ, Yan A. Kdo2 -lipid A: structural diversity and impact on immunopharmacology. Biol Rev Camb Philos Soc. 2015;90(2):408–427. doi:10.1111/brv.1211424838025
   PubMedGoogle Scholar
• Wang G, Hu Z, Fu Q, et al. Resveratrol mitigates lipopolysaccharide-mediated acute inflammation in rats by inhibiting the TLR4/NF-kappaBp65/MAPKs signaling cascade. Sci Rep. 2017;7:45006. doi:10.1038/srep4500628322346
   PubMed Web of Science ®Google Scholar
• Berman AY, Motechin RA, Wiesenfeld MY, Holz MK. The therapeutic potential of resveratrol: a review of clinical trials. NPJ Precis Oncol. 2017;1:35.
   Web of Science ®Google Scholar
• Zhang HX, Duan GL, Wang CN, Zhang YQ, Zhu XY, Liu YJ. Protective effect of resveratrol against endotoxemia-induced lung injury involves the reduction of oxidative/nitrative stress. Pulm Pharmacol Ther. 2014;27(2):150–155. doi:10.1016/j.pupt.2013.07.00723921197
   PubMedGoogle Scholar
• Jiang L, Zhang L, Kang K, et al. Resveratrol ameliorates LPS-induced acute lung injury via NLRP3 inflammasome modulation. Biomed Pharmacother. 2016;84:130–138. doi:10.1016/j.biopha.2016.09.02027643555
   PubMed Web of Science ®Google Scholar