192
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Capsaicin Attenuates LPS-Induced Acute Lung Injury by Inhibiting Inflammation and Autophagy Through Regulation of the TRPV1/AKT Pathway

ORCID Icon, ORCID Icon, , , ORCID Icon, & show all
Pages 153-170 | Received 16 Oct 2023, Accepted 03 Jan 2024, Published online: 08 Jan 2024

References

  • Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest. 2012;122(8):2731–2740. doi:10.1172/JCI60331
  • Ranieri VM, Rubenfeld GD, Thompson BT, et al. Acute respiratory distress syndrome: the Berlin Definition. JAMA. 2012;307(23):2526–2533. doi:10.1001/jama.2012.5669
  • Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med. 2000;342(18):1334–1349. doi:10.1056/NEJM200005043421806
  • Shi J, Zhao Y, Wang Y, et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature. 2014;514(7521):187–192. doi:10.1038/nature13683
  • Wu Z, Wang Y, Lu S, Yin L, Dai L. SIRT3 alleviates sepsis-induced acute lung injury by inhibiting pyroptosis via regulating the deacetylation of FoxO3a. Pulm Pharmacol Ther. 2023;82:102244. doi:10.1016/j.pupt.2023.102244
  • Li M, Wang C, Xu WT, Zhong X. Sodium houttuyfonate plays a protective role in the asthmatic airway by alleviating the NLRP3-related pyroptosis and Th1/Th2 immune imbalance. Mol Immunol. 2023;160:103–111. doi:10.1016/j.molimm.2023.06.013
  • Song H, Jiang L, Yang W, et al. Cryptotanshinone alleviates lipopolysaccharide and cigarette smoke-induced chronic obstructive pulmonary disease in mice via the Keap1/Nrf2 axis. Biomed Pharmacother. 2023;165:115105. doi:10.1016/j.biopha.2023.115105
  • Liu L, Zhang Y, Wang L, et al. Scutellarein alleviates chronic obstructive pulmonary disease through inhibition of ferroptosis by chelating iron and interacting with arachidonate 15-lipoxygenase. Phytother Res. 2023;2:4.
  • Chapa-Oliver AM, Mejía-Teniente L. Capsaicin: from plants to a cancer-suppressing agent. Molecules. 2016;21(8):931. doi:10.3390/molecules21080931
  • Li Q, Chang M, Lai R, et al. Potential benefits of spicy food consumption on cardiovascular outcomes in patients with diabetes: a cohort study of the China Kadoorie Biobank. Nutrition. 2023;112:112062. doi:10.1016/j.nut.2023.112062
  • Blair HA. Capsaicin 8% dermal patch: a review in peripheral neuropathic pain. Drugs. 2018;78(14):1489–1500. doi:10.1007/s40265-018-0982-7
  • Ghorbanpour A, Salari S, Baluchnejadmojarad T, Roghani M. Capsaicin protects against septic acute liver injury by attenuation of apoptosis and mitochondrial dysfunction. Heliyon. 2023;9(3):e14205. doi:10.1016/j.heliyon.2023.e14205
  • Lian YZ, Chang CC, Chen YS, Tinkov AA, Skalny AV, Chao JC. Lycium barbarum polysaccharides and capsaicin modulate inflammatory cytokines and colonic microbiota in colitis rats induced by dextran sulfate sodium. J Clin Biochem Nutr. 2022;71(3):229–237. doi:10.3164/jcbn.21-174
  • Zheng Y, Chen J, Wu X, et al. Enhanced anti-inflammatory effects of silibinin and capsaicin combination in lipopolysaccharide-induced RAW264.7 cells by inhibiting NF-kappaB and MAPK activation. Front Chem. 2022;10:934541. doi:10.3389/fchem.2022.934541
  • Howard LR, Talcott ST, Brenes CH, Villalon B. Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum species) as influenced by maturity. J Agric Food Chem. 2000;48(5):1713–1720. doi:10.1021/jf990916t
  • Khan FA, Mahmood T, Ali M, Saeed A, Maalik A. Pharmacological importance of an ethnobotanical plant: capsicum annuum L. Nat Prod Res. 2014;28(16):1267–1274. doi:10.1080/14786419.2014.895723
  • Maji AK, Banerji P. Phytochemistry and gastrointestinal benefits of the medicinal spice, Capsicum annuum L. (Chilli): a review. J Complement Integr Med. 2016;13(2):97–122. doi:10.1515/jcim-2015-0037
  • Chen H, Li N, Zhan X, et al. Capsaicin protects against lipopolysaccharide-induced acute lung injury through the HMGB1/NF-κB and PI3K/AKT/mTOR pathways. J Inflamm Res. 2021;14:5291–5304. doi:10.2147/JIR.S309457
  • Srinivasan K. Biological activities of red pepper (Capsicum annuum) and its pungent principle capsaicin: a review. Crit Rev Food Sci Nutr. 2016;56(9):1488–1500. doi:10.1080/10408398.2013.772090
  • Zhang S, Tang C, Wang X. Octreotide activates autophagy to alleviate lipopolysaccharide-induced human pulmonary epithelial cell injury by inhibiting the protein kinase B (AKT)/mammalian target of rapamycin (mTOR) signaling pathway. Bioengineered. 2022;13(1):217–226. doi:10.1080/21655979.2021.2012908
  • Meng Y, Pan M, Zheng B, et al. Autophagy attenuates angiotensin II-induced pulmonary fibrosis by inhibiting redox imbalance-mediated NOD-like receptor family pyrin domain containing 3 inflammasome activation. Antioxid Redox Signal. 2019;30(4):520–541. doi:10.1089/ars.2017.7261
  • Li Y, Yu G, Yuan S, et al. Cigarette smoke-induced pulmonary inflammation and autophagy are attenuated in Ephx2-deficient mice. Inflammation. 2017;40(2):497–510. doi:10.1007/s10753-016-0495-z
  • Chu R, Wang J, Bi Y, Nan G. The kinetics of autophagy in the lung following acute spinal cord injury in rats. Spine J. 2018;18(5):845–856. doi:10.1016/j.spinee.2018.01.001
  • Chang AL, Ulrich A, Suliman HB, Piantadosi CA. Redox regulation of mitophagy in the lung during murine Staphylococcus aureus sepsis. Free Radic Biol Med. 2015;78:179–189. doi:10.1016/j.freeradbiomed.2014.10.582
  • Guo L, Wu X, Zhao S, Zhang X, Qian G, Li S. Autophagy inhibition protects from alveolar barrier dysfunction in LPS-induced ALI mice by targeting alveolar epithelial cells. Respir Physiol Neurobiol. 2021;283:103532. doi:10.1016/j.resp.2020.103532
  • Huang S, Xue Y, Chen W, et al. Fibroblast growth factor 10 alleviates acute lung injury by inhibiting excessive autophagy via Nrf2. J Endocrinol. 2023;259(1). doi:10.1530/JOE-23-0095
  • Sun Q, Zhang H, Du HB, et al. Estrogen Alleviates Posthemorrhagic Shock Mesenteric Lymph-Mediated Lung Injury Through Autophagy Inhibition. Shock. 2023;59(5):754–762. doi:10.1097/SHK.0000000000002102
  • Sun Y, Li C, Shu Y, et al. Inhibition of autophagy ameliorates acute lung injury caused by avian influenza A H5N1 infection. Sci Signal. 2012;5(212):ra16. doi:10.1126/scisignal.2001931
  • Hu R, Chen ZF, Yan J, et al. Complement C5a exacerbates acute lung injury induced through autophagy-mediated alveolar macrophage apoptosis. Cell Death Dis. 2014;5(7):e1330–e1330. doi:10.1038/cddis.2014.274
  • Zhu Q, Wang H, Wang H, et al. Protective effects of ethyl pyruvate on lipopolysaccharide‑induced acute lung injury through inhibition of autophagy in neutrophils. Mol Med Rep. 2017;15(3):1272–1278. doi:10.3892/mmr.2017.6118
  • Qian F, He S, Yang X, Chen X, Zhao S, Wang J. Circular RNA DHTKD1 targets miR‑338‑3p/ETS1 axis to regulate the inflammatory response in human bronchial epithelial cells. Exp Ther Med. 2023;26(1):316. doi:10.3892/etm.2023.12015
  • Miao RF, Tu J. LncRNA CDKN2B-AS1 interacts with LIN28B to exacerbate sepsis-induced acute lung injury by inducing HIF −1α/ NLRP3 -mediated pyroptosis. Kaohsiung J Med Sci. 2023;39(9):883–895. doi:10.1002/kjm2.12697
  • Bouyer PG, Tang X, Weber CR, Shen L, Turner JR, Matthews JB. Capsaicin induces NKCC1 internalization and inhibits chloride secretion in colonic epithelial cells independently of TRPV1. Am J Physiol Gastrointest Liver Physiol. 2013;304(2):G142–156. doi:10.1152/ajpgi.00483.2011
  • Jiao Y, Shen F, Wang Z, et al. Genipin, a natural AKT inhibitor, targets the PH domain to affect downstream signaling and alleviates inflammation. Biochem Pharmacol. 2019;170:113660. doi:10.1016/j.bcp.2019.113660
  • Liu T, Wu B, Wang Y, et al. Particulate matter 2.5 induces autophagy via inhibition of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin kinase signaling pathway in human bronchial epithelial cells. Mol Med Rep. 2015;12(2):1914–1922. doi:10.3892/mmr.2015.3577
  • Wang X, Liu F, Xu M, Wu L. Penehyclidine hydrochloride alleviates lipopolysaccharide‑induced acute respiratory distress syndrome in cells via regulating autophagy‑related pathway. Mol Med Rep. 2021;23:2).
  • Yang N, Shang Y. Ferrostatin-1 and 3-methyladenine ameliorate ferroptosis in OVA-induced asthma model and in IL-13-challenged BEAS-2B cells. Oxid Med Cell Longev. 2022;2022:9657933. doi:10.1155/2022/9657933
  • Zhang Y, Yang S, Qiu Z, et al. Pyrogallol enhances therapeutic effect of human umbilical cord mesenchymal stem cells against LPS-mediated inflammation and lung injury via activation of Nrf2/HO-1 signaling. Free Radic Biol Med. 2022;191:66–81. doi:10.1016/j.freeradbiomed.2022.08.030
  • Xu L, Li X, Wang H, Xie F, Liu H, Xie J. Cigarette smoke triggers inflammation mediated by autophagy in BEAS-2B cells. Ecotoxicol Environ Saf. 2019;184:109617. doi:10.1016/j.ecoenv.2019.109617
  • Liu P, Hao J, Zhao J, et al. Integrated network pharmacology and experimental validation approach to investigate the therapeutic effects of capsaicin on lipopolysaccharide-induced acute lung injury. Mediators Inflamm. 2022;2022:9272896. doi:10.1155/2022/9272896
  • Cabral LD, Giusti-Paiva A. The transient receptor potential vanilloid 1 antagonist capsazepine improves the impaired lung mechanics during endotoxemia. Basic Clin Pharmacol Toxicol. 2016;119(5):421–427. doi:10.1111/bcpt.12605
  • Joffre J, Wong E, Lawton S, et al. N-Oleoyl dopamine induces IL-10 via central nervous system TRPV1 and improves endotoxemia and sepsis outcomes. J Neuroinflammation. 2022;19(1):118. doi:10.1186/s12974-022-02485-z
  • Meng L, Li L, Lu S, et al. The protective effect of dexmedetomidine on LPS-induced acute lung injury through the HMGB1-mediated TLR4/NF-κB and PI3K/Akt/mTOR pathways. Mol Immunol. 2018;94:7–17. doi:10.1016/j.molimm.2017.12.008
  • Li T, Wu YN, Wang H, Ma JY, Zhai SS, Duan J. Dapk1 improves inflammation, oxidative stress and autophagy in LPS-induced acute lung injury via p38MAPK/NF-κB signaling pathway. Mol Immunol. 2020;120:13–22. doi:10.1016/j.molimm.2020.01.014
  • Slavin SA, Leonard A, Grose V, Fazal F, Rahman A. Autophagy inhibitor 3-methyladenine protects against endothelial cell barrier dysfunction in acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2018;314(3):L388–L396. doi:10.1152/ajplung.00555.2016
  • Kong L, Deng J, Zhou X, et al. Sitagliptin activates the p62-Keap1-Nrf2 signalling pathway to alleviate oxidative stress and excessive autophagy in severe acute pancreatitis-related acute lung injury. Cell Death Dis. 2021;12(10):928. doi:10.1038/s41419-021-04227-0
  • Fanelli V, Ranieri VM. Mechanisms and clinical consequences of acute lung injury. Ann Am Thorac Soc. 2015;12(Suppl 1):S3–8. doi:10.1513/AnnalsATS.201407-340MG
  • Seki H, Tasaka S, Fukunaga K, et al. Effect of Toll-like receptor 4 inhibitor on LPS-induced lung injury. Inflamm Res. 2010;59(10):837–845. doi:10.1007/s00011-010-0195-3
  • Patel BV, Wilson MR, O’Dea KP, Takata M. TNF-induced death signaling triggers alveolar epithelial dysfunction in acute lung injury. J Immunol. 2013;190(8):4274–4282. doi:10.4049/jimmunol.1202437
  • Pierrakos C, Karanikolas M, Scolletta S, Karamouzos V, Velissaris D. Acute respiratory distress syndrome: pathophysiology and therapeutic options. J Clin Med Res. 2012;4(1):7–16. doi:10.4021/jocmr761w
  • Ward PA, Grailer JJ. Acute lung injury and the role of histones. Transl Respir Med. 2014;2(1):1. doi:10.1186/2213-0802-2-1
  • Alonso-Villegas R, González-Amaro RM, Figueroa-Hernández CY, Rodríguez-Buenfil IM. The genus capsicum: a review of bioactive properties of its polyphenolic and capsaicinoid composition. Molecules. 2023;28(10):4239. doi:10.3390/molecules28104239
  • Fernandes ES, Cerqueira AR, Soares AG, Costa SK. Capsaicin and its role in chronic diseases. Adv Exp Med Biol. 2016;929:91–125. doi:10.1007/978-3-319-41342-6_5
  • Zhan X, Zhang J, Chen H, et al. Capsaicin alleviates Acetaminophen-induced acute liver injury in mice. Clin Immunol. 2020;220:108578.
  • Adhikari R, Jung J, Shiwakoti S, et al. Capsaicin inhibits aortic valvular interstitial cell calcification via the redox-sensitive NFκB/AKT/ERK1/2 pathway. Biochem Pharmacol. 2023;212:115530. doi:10.1016/j.bcp.2023.115530
  • Shi S, Huang D, Wu Y, et al. Salidroside pretreatment alleviates PM(2.5) caused lung injury via inhibition of apoptosis and pyroptosis through regulating NLRP3 Inflammasome. Food Chem Toxicol. 2023;177:113858. doi:10.1016/j.fct.2023.113858
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147(4):728–741. doi:10.1016/j.cell.2011.10.026
  • Khandia R, Dadar M, Munjal A, et al. A comprehensive review of autophagy and its various roles in infectious, non-infectious, and lifestyle diseases: current knowledge and prospects for disease prevention, novel drug design, and therapy. Cells. 2019;8(7):674. doi:10.3390/cells8070674
  • Ma Y, Xu H, Chen G, et al. Uncovering the active constituents and mechanisms of Rujin Jiedu powder for ameliorating LPS-induced acute lung injury using network pharmacology and experimental investigations. Front Pharmacol. 2023;14:1186699. doi:10.3389/fphar.2023.1186699
  • Wang L, Jiang S, Li X, Lin T, Qin T. Astringin protects LPS-induced toxicity by suppressing oxidative stress and inflammation via suppression of PI3K/AKT/NF-κB pathway for pediatric acute lung injury. Naunyn Schmiedebergs Arch Pharmacol. 2023;396(10):2369–2377. doi:10.1007/s00210-023-02439-z