https://doi.org/10.4081/ejh.2023.3639
Effects of piperlonguminine on lung injury in severe acute pancreatitis via the TLR4/NF-κB pathway
Submitted: 1 January 2023
Accepted: 3 March 2023
Published: 20 March 2023
Accepted: 3 March 2023
Abstract Views: 590
PDF: 417
HTML: 16
HTML: 16
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Acute pancreatitis is an inflammatory response in the pancreas, involving activation of pancreatic enzymes. Severe acute pancreatitis (SAP) often causes systemic complications that affect distant organs, including the lungs. The aim of this study was to explore the therapeutic potential of piperlonguminine on SAP-induced lung injury in rat models. Acute pancreatitis was induced in rats by repetitive injections with 4% sodium taurocholate. Histological examination and biochemical assays were used to assess the severity of lung injury, including tissue damage, and levels of nicotinamide adenine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), nicotinamide adenine dinucleotide phosphate (NADPH) oxidase 4 (NOX4), reactive oxygen species (ROS), and inflammatory cytokines. We found that piperlonguminine significantly ameliorated pulmonary architectural distortion, hemorrhage, interstitial edema, and alveolar thickening in rats with SAP. In addition, NOX2, NOX4, ROS, and inflammatory cytokine levels in pulmonary tissues were notably decreased in piperlonguminine-treated rats. Piperlonguminine also attenuated the expression levels of toll-like receptor 4 (TLR4) and nuclear factor-kappa B (NF-κB). Together, our findings demonstrate for the first time that piperlonguminine can ameliorate acute pancreatitis-induced lung injury via inhibitory modulation of inflammatory responses by suppression of the TLR4/NF-κB signaling pathway.
Dombernowsky T, Kristensen MO, Rysgaard S, Gluud LL, Novovic S. Risk factors for and impact of respiratory failure on mortality in the early phase of acute pancreatitis. Pancreatology 2016;16:756-60.
DOI: https://doi.org/10.1016/j.pan.2016.06.664
Zhou J, Zhou P, Zhang Y, Wang G, Fan Z. Signal pathways and markers involved in acute lung injury induced by acute pancreatitis. Dis Markers 2021;2021:9947047.
DOI: https://doi.org/10.1155/2021/9947047
Fanelli V, Ranieri VM. Mechanisms and clinical consequences of acute lung injury. Ann Am Thorac Soc 2015;12:S3-8.
DOI: https://doi.org/10.1513/AnnalsATS.201407-340MG
Yoval-Sanchez B, Calleja LF, de la Luz Hernandez-Esquivel M, Rodriguez-Zavala JS. Piperlonguminine a new mitochondrial aldehyde dehydrogenase activator protects the heart from ischemia/reperfusion injury. Biochim Biophys Acta Gen Subj 2020;1864:129684.
DOI: https://doi.org/10.1016/j.bbagen.2020.129684
Ginzburg S, Golovine KV, Makhov PB, Uzzo RG, Kutikov A, Kolenko VM. Piperlongumine inhibits NF-kappaB activity and attenuates aggressive growth characteristics of prostate cancer cells. Prostate 2014;74:177-86.
DOI: https://doi.org/10.1002/pros.22739
Liu QR, Liu JM, Chen Y, Xie XQ, Xiong XX, Qiu XY, et al. Piperlongumine inhibits migration of glioblastoma cells via activation of ROS-dependent p38 and JNK signaling pathways. Oxid Med Cell Longev 2014;2014:653732.
DOI: https://doi.org/10.1155/2014/653732
Randhawa H, Kibble K, Zeng H, Moyer MP, Reindl KM. Activation of ERK signaling and induction of colon cancer cell death by piperlongumine. Toxicol In Vitro 2013;27:1626-33.
DOI: https://doi.org/10.1016/j.tiv.2013.04.006
Sriwiriyajan S, Sukpondma Y, Srisawat T, Madla S, Graidist P. (-)-Kusunokinin and piperloguminine from Piper nigrum: An alternative option to treat breast cancer. Biomed Pharmacother 2017;92:732-43.
DOI: https://doi.org/10.1016/j.biopha.2017.05.130
Wang H, Liu J, Gao G, Wu X, Wang X, Yang H. Protection effect of piperine and piperlonguminine from Piper longum L. alkaloids against rotenone-induced neuronal injury. Brain Res 2016;1639:214-27.
DOI: https://doi.org/10.1016/j.brainres.2015.07.029
Zhu P, Qian J, Xu Z, Meng C, Liu J, Shan W, et al. Piperlonguminine and Piperine analogues as TrxR inhibitors that promote ROS and autophagy and regulate p38 and Akt/mTOR signaling. J Nat Prod 2020;83:3041-9.
DOI: https://doi.org/10.1021/acs.jnatprod.0c00599
Kim N, Do J, Bae JS, Jin HK, Kim JH, Inn KS, et al. Piperlongumine inhibits neuroinflammation via regulating NF-kappaB signaling pathways in lipopolysaccharide-stimulated BV2 microglia cells. J Pharmacol Sci 2018;137:195-201.
DOI: https://doi.org/10.1016/j.jphs.2018.06.004
Ismail EN, Jantan I, Vidyadaran S, Jamal JA, Azmi N. Phyllanthus amarus prevents LPS-mediated BV2 microglial activation via MyD88 and NF-kappaB signaling pathways. BMC Complement Med Ther 2020;20:202.
DOI: https://doi.org/10.1186/s12906-020-02961-0
Zhang Z, Amorosa LF, Petrova A, Coyle S, Macor M, Nair M, et al. TLR4 counteracts BVRA signaling in human leukocytes via differential regulation of AMPK, mTORC1 and mTORC2. Sci Rep 2019;9:7020.
DOI: https://doi.org/10.1038/s41598-019-43347-8
Huang JB, Chen NC, Chen CL, Fu MH, Pan HY, Hsu CY, et al. Serum levels of soluble triggering receptor expressed on myeloid cells-1 associated with the severity and outcome of acute ischemic stroke. J Clin Med 2020;10:61.
DOI: https://doi.org/10.3390/jcm10010061
Xiao Z, Kong B, Yang H, Dai C, Fang J, Qin T, et al. Key player in cardiac hypertrophy, emphasizing the role of toll-like receptor 4. Front Cardiovasc Med 2020;7:579036.
DOI: https://doi.org/10.3389/fcvm.2020.579036
Cao C, Yin C, Shou S, Wang J, Yu L, Li X, et al. Ulinastatin protects against LPS-induced acute lung injury by attenuating TLR4/NF-kappaB pathway activation and reducing inflammatory mediators. Shock 2018;50:595-605.
DOI: https://doi.org/10.1097/SHK.0000000000001104
Tang J, Xu L, Zeng Y, Gong F. Effect of gut microbiota on LPS-induced acute lung injury by regulating the TLR4/NF-kB signaling pathway. Int Immunopharmacol 2021;91:107272.
DOI: https://doi.org/10.1016/j.intimp.2020.107272
Zhang Q, Lenardo MJ, Baltimore D. 30 years of NF-kappaB: A blossoming of relevance to human pathobiology. Cell 2017;168:37-57.
DOI: https://doi.org/10.1016/j.cell.2016.12.012
Ju M, Liu B, He H, Gu Z, Liu Y, Su Y, et al. MicroRNA-27a alleviates LPS-induced acute lung injury in mice via inhibiting in fl ammation and apoptosis through modulating TLR4/MyD88/NF-kappaB pathway. Cell Cycle 2018;17:2001-18.
DOI: https://doi.org/10.1080/15384101.2018.1509635
Chen X, Li SL, Wu T, Liu JD. Proteasome inhibitor ameliorates severe acute pancreatitis and associated lung injury of rats. World J Gastroenterol 2008;14:3249-53.
DOI: https://doi.org/10.3748/wjg.14.3249
Jia W, Wang W, Li R, Zhou Q, Qu Y, Jia Y, et al. Effect of qinbai qingfei concentrated pellets on substance P and neutral endopeptidase of rats with post-infectious cough. BMC Complement Med Ther 2020;20:289.
DOI: https://doi.org/10.1186/s12906-020-03081-5
Galecki P, Talarowska M. Inflammatory theory of depression. Psychiatr Pol 2018;52:437-47.
DOI: https://doi.org/10.12740/PP/76863
Hartman CL, Ford DA. MPO (myeloperoxidase) caused endothelial dysfunction. Arterioscler Thromb Vasc Biol 2018;38:1676-7.
DOI: https://doi.org/10.1161/ATVBAHA.118.311427
Zhou MT, Chen CS, Chen BC, Zhang QY, Andersson R. Acute lung injury and ARDS in acute pancreatitis: mechanisms and potential intervention. World J Gastroenterol 2010;16:2094-9.
DOI: https://doi.org/10.3748/wjg.v16.i17.2094
Sharma V, Rana SS, Sharma RK, Kang M, Gupta R, Bhasin DK. A study of radiological scoring system evaluating extrapancreatic inflammation with conventional radiological and clinical scores in predicting outcomes in acute pancreatitis. Ann Gastroenterol 2015;28:399-404.
Wu P, Li L, Sun W. Efficacy comparisons of enteral nutrition and parenteral nutrition in patients with severe acute pancreatitis: a meta-analysis from randomized controlled trials. Biosci Rep 2018;38:BSR20181515.
DOI: https://doi.org/10.1042/BSR20181515
Silva-Vaz P, Abrantes AM, Castelo-Branco M, Gouveia A, Botelho MF, Tralhao JG. Multifactorial scores and biomarkers of prognosis of acute pancreatitis: Applications to research and practice. Int J Mol Sci 2020;21:338.
DOI: https://doi.org/10.3390/ijms21010338
Huang CH, Wang SC, Chen IC, Chen YT, Liu PL, Fang SH, et al. Protective effect of piplartine against LPS-induced sepsis through attenuating the MAPKs/NF-kappaB signaling pathway and NLRP3 inflammasome activation. Pharmaceuticals (Basel) 2021;14:588.
DOI: https://doi.org/10.3390/ph14060588
Tang Y, Zhang W, Wu L, Bai B, Zheng B, Li M, et al. Piperlongumine mitigates LPS-induced inflammation and lung injury via targeting MD2/TLR4. Biochem Biophys Res Commun 2023;642:118-27.
DOI: https://doi.org/10.1016/j.bbrc.2022.11.092
Ashino TEB, Sant Ana ML, Yoshikawa AH, Possebon L, de Souza Costa S, Iyomasa-Pilon MM, et al. Protective effects of piperlongumin in the prevention of inflammatory damage caused by pulmonary exposure to benzopyrene carcinogen. Int Immunopharmacol 2021;101:108285.
DOI: https://doi.org/10.1016/j.intimp.2021.108285
Awasthee N, Shekher A, Rai V, Verma SS, Mishra S, Dhasmana A, et al. Piperlongumine, a piper alkaloid, enhances the efficacy of doxorubicin in breast cancer: involvement of glucose import, ROS, NF-kappaB and lncRNAs. Apoptosis 2022;27:261-82.
DOI: https://doi.org/10.1007/s10495-022-01711-6
Zheng L, Fang S, Chen A, Chen W, Qiao E, Chen M, et al. Piperlongumine synergistically enhances the antitumour activity of sorafenib by mediating ROS-AMPK activation and targeting CPSF7 in liver cancer. Pharmacol Res 2022;177:106140.
DOI: https://doi.org/10.1016/j.phrs.2022.106140
Wang XY, Tang QQ, Zhang JL, Fang MY, Li YX. Effect of SB203580 on pathologic change of pancreatic tissue and expression of TNF-alpha and IL-1beta in rats with severe acute pancreatitis. Eur Rev Med Pharmacol Sci 2014;18:338-43.
Motegi SI, Sekiguchi A, Uchiyama A, Uehara A, Fujiwara C, Yamazaki S, et al. Protective effect of mesenchymal stem cells on the pressure ulcer formation by the regulation of oxidative and endoplasmic reticulum stress. Sci Rep 2017;7:17186.
DOI: https://doi.org/10.1038/s41598-017-17630-5
Cheng D, Chen L, Tu W, Wang H, Wang Q, Meng L, et al. Protective effects of valsartan administration on doxorubicin‑induced myocardial injury in rats and the role of oxidative stress and NOX2/NOX4 signaling. Mol Med Rep 2020;22:4151-62.
DOI: https://doi.org/10.3892/mmr.2020.11521
Escalada FJ. [The physiology of glucagon-like peptide-1 and its role in the pathophysiology of type 2 diabetes mellitus].[Article in Spanish]. Med Clin (Barc) 2014;143:S2-7.
Merza M, Hartman H, Rahman M, Hwaiz R, Zhang E, Renstrom E, et al. Neutrophil extracellular traps induce trypsin activation, inflammation, and tissue damage in mice with severe acute pancreatitis. Gastroenterology 2015;149:1920-31-e8.
DOI: https://doi.org/10.1053/j.gastro.2015.08.026
Yang ZW, Meng XX, Xu P. Central role of neutrophil in the pathogenesis of severe acute pancreatitis. J Cell Mol Med 2015;19:2513-20.
DOI: https://doi.org/10.1111/jcmm.12639
Gu SM, Lee HP, Ham YW, Son DJ, Kim HY, Oh KW, et al. Piperlongumine improves lipopolysaccharide-induced amyloidogenesis by suppressing NF-kappaB pathway. Neuromolecular Med 2018;20:312-27.
DOI: https://doi.org/10.1007/s12017-018-8495-9
Ethics Approval
The experimental protocols were approved by the Institutional Animal Care and Use Committee of the Second Affiliated Hospital of Nanchang University, Nanchang, ChinaHow to Cite
Hu, Q. ., Tao, R. ., Hu, X. ., Wu, H. ., & Xu, J. (2023). Effects of piperlonguminine on lung injury in severe acute pancreatitis <em>via</em> the TLR4/NF-κB pathway. European Journal of Histochemistry, 67(2). https://doi.org/10.4081/ejh.2023.3639
Copyright (c) 2023 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
Similar Articles
- F. Merigo, F. Boschi, C. Lasconi, D. Benati, A. Sbarbati, Molecules implicated in glucose homeostasis are differentially expressed in the trachea of lean and obese Zucker rats , European Journal of Histochemistry: Vol. 60 No. 1 (2016)
- Simone Carotti, Giuseppe Perrone, Michelina Amato, Umberto Vespasiani Gentilucci, Daniela Righi, Maria Francesconi, Claudio Pellegrini, Francesca Zalfa, Maria Zingariello, Antonio Picardi, Andrea Onetti Muda, Sergio Morini, Reelin expression in human liver of patients with chronic hepatitis C infection , European Journal of Histochemistry: Vol. 61 No. 1 (2017)
- E. Tarantola, V. Bertone, G. Milanesi, C. Gruppi, A. Ferrigno, M. Vairetti, S. Barni, I. Freitas, Dipeptidylpeptidase-IV activity and expression reveal decreased damage to the intrahepatic biliary tree in fatty livers submitted to subnormothermic machine-perfusion respect to conventional cold storage , European Journal of Histochemistry: Vol. 58 No. 3 (2014)
- M. Ferreira Júnior, S.A. Batista, P.V.T. Vidigal, A.A.C. Cordeiro, F.M.S. Oliveira, L.O. Prata, A.E.T. Diniz, C.M. Barral, R.C. Barbuto, A.D. Gomes, I.D. Araújo, D.M.M. Queiroz, M.V. Caliari, Infection with CagA-positive Helicobacter pylori strain containing three EPIYA C phosphorylation sites is associated with more severe gastric lesions in experimentally infected Mongolian gerbils (Meriones unguiculatus) , European Journal of Histochemistry: Vol. 59 No. 2 (2015)
- Gong Cheng, Fengmin An, Zhilin Cao, Mingdi Zheng, Zhongyuan Zhao, Hao Wu, DPY30 promotes the growth and survival of osteosarcoma cell by regulating the PI3K/AKT signal pathway , European Journal of Histochemistry: Vol. 67 No. 1 (2023)
- Rong Tian, Gengsheng Mao, Ghrelin reduces cerebral ischemic injury in rats by reducing M1 microglia/macrophages , European Journal of Histochemistry: Vol. 66 No. 1 (2022)
- E. Lacunza, V. Ferretti, C. Barbeito, A. Segal-Eiras, M. V. Croce, Immunohistochemical evidence of Muc1 expression during rat embryonic development , European Journal of Histochemistry: Vol. 54 No. 4 (2010)
- J. Feng, S. Ge, L. Zhang, H. Che, C. Liang, Aortic dissection is associated with reduced polycystin-1 expression, an abnormality that leads to increased ERK phosphorylation in vascular smooth muscle cells , European Journal of Histochemistry: Vol. 60 No. 4 (2016)
- Roberta Sferra, Simona Pompili, Claudio Festuccia, Francesco Marampon, Giovanni L. Gravina, Luca Ventura, Ernesto Di Cesare, Sara Cicchinelli, Eugenio Gaudio, Antonella Vetuschi, The possible prognostic role of histone deacetylase and transforming growth factor β/Smad signaling in high grade gliomas treated by radio-chemotherapy: a preliminary immunohistochemical study , European Journal of Histochemistry: Vol. 61 No. 2 (2017)
- A. Rus, M.L. Del Moral, F. Molina, M.A. Peinado, Upregulation of cardiac NO/NOS system during short-term hypoxia and the subsequent reoxygenation period , European Journal of Histochemistry: Vol. 55 No. 2 (2011)
<< < 2 3 4 5 6 7 8 9 10 11 > >>
You may also start an advanced similarity search for this article.
