1,2,3,4,6-O-Pentagalloylglucose Protects against Acute Lung Injury by Activating the AMPK/PI3K/Akt/Nrf2 Pathway
Abstract
:1. Introduction
2. Results
2.1. PGG Exerts Protective Effects against ALI in Rats
2.2. PGG Alleviates LPS-Induced Pathological Changes in Lung Tissues
2.3. Western Blot Analysis
2.4. Effect of PGG on Expression of AMPK, PI3K, Akt, and Nrf2 in Lung Tissues by Immunohistochemical Analysis
2.5. Immunofluorescence Assay
3. Discussion
4. Materials and Methods
4.1. Compound
4.2. Animals
4.3. Experimental Design
4.4. Measurement of Cell Counts in BALF
4.5. Lung Wet/Dry (W/D) Ratio
4.6. Evaluation of Oxidative Stress in BALF
4.7. Measurement of Cytokine Levels in BALF
4.8. Histological Examination
4.9. Western Blot Analysis
4.10. Immunohistochemistry for Detection of PI3K, Akt, Nrf2, and AMPK
4.11. Immunofluorescence
4.12. Data Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ware, L.B.; Matthay, M.A. The acute respiratory distress syndrome. N. Engl. J. Med. 2000, 342, 1334–1349. [Google Scholar] [CrossRef] [PubMed]
- Frutos-Vivar, F.; Nin, N.; Esteban, A. Epidemiology of acute lung injury and acute respiratory distress syndrome. Curr. Opin. Crit. Care 2004, 10, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Calfee, C.S.; Delucchi, K.L.; Sinha, P.; Matthay, M.A.; Hackett, J.; Shankar-Hari, M.; McDowell, C.; Laffey, J.G.; O’Kane, C.M.; McAuley, D.F.; et al. Acute respiratory distress syndrome subphenotypes and differential response to simvastatin: Secondary analysis of a randomised controlled trial. Lancet Respir. Med. 2018, 6, 691–698. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.-D.; Zhang, Z.-Y.; Wei, X.-J.; Cai, Y.-Q.; Yao, W.-Z.; Wang, M.-H.; Huang, Q.-F.; Zhang, X.-B. Association between cytokine profiles and lung injury in COVID-19 pneumonia. Respir. Res. 2020, 21, 201. [Google Scholar] [CrossRef]
- Sweeney, R.M.; Griffiths, M.; McAuley, D. Treatment of acute lung injury: Current and emerging pharmacological therapies. Semin. Respir. Crit. Care Med. 2013, 34, 487–498. [Google Scholar] [CrossRef] [PubMed]
- Impellizzeri, D.; Bruschetta, G.; Esposito, E.; Cuzzocrea, S. Emerging drugs for acute lung injury. Expert. Opin. Emerg. Drugs 2015, 20, 75–89. [Google Scholar] [CrossRef]
- Hussain, M.; Xu, C.; Ahmad, M.; Majeed, A.; Lu, M.; Wu, X.; Tang, L.; Wu, X. Acute respiratory distress syndrome: Bench-to-bedside approaches to improve drug development. Clin. Pharmacol. Ther. 2018, 104, 484–494. [Google Scholar] [CrossRef] [PubMed]
- Boukhenouna, S.; Wilson, M.A.; Bahmed, K.; Kosmider, B. Reactive Oxygen species in chronic obstructive pulmonary disease. Oxid. Med. Cell. Longev. 2018, 2018, 5730395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sohrabi, F.; Dianat, M.; Badavi, M.; Radan, M.; Mard, S.A. Gallic acid suppresses inflammation and oxidative stress through modulating Nrf2-HO-1-NF-κB signaling pathways in elastase-induced emphysema in rats. Environ. Sci. Pollut. Res. Int. 2021, 28, 56822–56834. [Google Scholar] [CrossRef] [PubMed]
- Mahmoud, M.; Nabil, M.; Hasan, R.; El Sahzly, A.; El-Ansari, M.; Sobeh, M. Pentagalloyl glucose, a major compound in mango seed kernel, exhibits distinct gastroprotective effects in indomethacin-induced gastropathy in rats via modulating the NO/eNOS/iNOS signaling pathway. Front. Pharmacol. 2022, 13, 800986. [Google Scholar] [CrossRef] [PubMed]
- Patnaik, S.S.; Simionescu, D.T.; Goergen, C.J.; Hoyt, K.; Sirsi, S.; Finol, E.A. Pentagalloyl glucose and its functional role in vascular health: Biomechanics and drug-delivery characteristics. Ann. Biomed. Eng. 2019, 47, 39–59. [Google Scholar] [CrossRef]
- Torres-León, C.; Ventura-Sobrevilla, J.; Serna-Cock, L.; Ascacio-Valdés, J.A.; Contreras-Esquivel, J.; Aguilar, C.N. Pentagalloylglucose (PGG): A valuable phenolic compound with functional properties. J. Funct. Foods 2017, 37, 176–189. [Google Scholar] [CrossRef]
- Chen, R.H.; Yang, L.J.; Hamdoun, S.; Chung, S.K.; Lam, C.W.-k.; Zhang, K.X.; Guo, X.; Xia, C.; Law, B.Y.K.; Wong, V.K.W. 1,2,3,4,6-Pentagalloyl glucose, a RBD-ACE2 binding inhibitor to prevent SARS-CoV-2 infection. Front. Pharmacol. 2021, 12, 634176. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Lei, H.-M.; Wang, P.-L.; Ma, Z.-Q.; Zhang, Y.; Wu, J.-J.; Nie, J.; Chen, S.-J.; Han, W.-J.; Wang, Q.; et al. Bioactive components from Qingwen Baidu Decoction against LPS-induced acute lung injury in rats. Molecules 2017, 22, 692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Q.; Nie, J.; Chen, S.J.; Li, Q. Protective effects of ethyl gallate and pentagalloylglucose, the active components of Qingwen Baidu Decoction, against lipopolysaccharide-induced acute lung injury in rats. Drug. Des. Devel. Ther. 2019, 13, 71–77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, K.; Guo, S.; Yang, C.; Yang, J.; Chen, Y.; Shaukat, A.; Zhao, G.; Wu, H.; Deng, G. Barbaloin protects against lipopolysaccharide (LPS)-induced acute lung injury by inhibiting the ROS-mediated PI3K/AKT/NF-κB pathway. Int. Immunopharmacol. 2018, 64, 140–150. [Google Scholar] [CrossRef]
- Meng, L.; Li, L.; Lu, S.; Li, K.; Su, Z.; Wang, Y.; Fan, X.; Li, X.; Zhao, G. 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. [Google Scholar] [CrossRef] [PubMed]
- Wu, G.; Du, L.; Zhao, L.; Shang, R.; Liu, D.; Jing, Q.; Liang, J.; Ren, Y. The total alkaloids of Aconitum tanguticum protect against lipopolysaccharide-induced acute lung injury in rats. J. Ethnopharmacol. 2014, 155, 1483–1491. [Google Scholar] [CrossRef]
- Monnet, X.; Anguel, N.; Osman, D.; Hamzaoui, O.; Richard, C.; Teboul, J.-L. Assessing pulmonary permeability by transpulmonary thermodilution allows differentiation of hydrostatic pulmonary edema from ALI/ARDS. Intensive Care Med. 2007, 33, 448–453. [Google Scholar] [CrossRef]
- Jiang, W.; Luo, F.; Lu, Q.; Liu, J.; Li, P.; Wang, X.; Fu, Y.; Hao, K.; Yan, T.; Ding, X. The protective effect of Trillin LPS-induced acute lung injury by the regulations of inflammation and oxidative state. Chem. Biol. Interact. 2016, 243, 127–134. [Google Scholar] [CrossRef]
- Chen, T.; Wang, R.; Jiang, W.; Wang, H.; Xu, A.; Lu, G.; Ren, Y.; Xu, Y.; Song, Y.; Yong, S.; et al. Protective Effect of astragaloside IV against paraquat-induced lung injury in mice by suppressing Rho signaling. Inflammation 2016, 39, 483–492. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Lv, H.; Li, H.; Ci, X.; Peng, L. Oridonin protects LPS-induced acute lung injury by modulating Nrf2-mediated oxidative stress and Nrf2-independent NLRP3 and NF-κB pathways. Cell Commun. Signal. 2019, 17, 62. [Google Scholar] [CrossRef] [Green Version]
- Grahame Hardie, D. AMP-activated protein kinase: A key regulator of energy balance with many roles in human disease. J. Intern. Med. 2014, 276, 543–559. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Cheng, X.; Yue, L.; Cui, W.; Zhou, W.; Gao, J.; Yao, H. Molecular pathogenesis in chronic obstructive pulmonary disease and therapeutic potential by targeting AMP-activated protein kinase. J. Cell Physiol. 2018, 233, 1999–2006. [Google Scholar] [CrossRef] [PubMed]
- Cheng, X.Y.; Li, Y.Y.; Huang, C.; Li, J.; Yao, H.W. AMP-activated protein kinase reduces inflammatory responses and cellular senescence in pulmonary emphysema. Oncotarget 2017, 8, 22513–22523. [Google Scholar] [CrossRef] [Green Version]
- Cui, W.; Zhang, Z.; Zhang, P.; Qu, J.; Zheng, C.; Mo, X.; Zhou, W.; Xu, L.; Yao, H.; Gao, J. Nrf2 attenuates inflammatory response in COPD/emphysema: Crosstalk with Wnt3a/β-catenin and AMPK pathways. J. Cell Mol. Med. 2018, 22, 3514–3525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wen, Z.; Hou, W.; Wu, W.; Zhao, Y.; Dong, X.; Bai, X.; Peng, L.; Song, L. 6′-O-Galloylpaeoniflorin attenuates cerebral ischemia reperfusion-induced neuroinflammation and oxidative stress via PI3K/Akt/Nrf2 activation. Oxid. Med. Cell Longev. 2018, 2018, 8678267. [Google Scholar] [CrossRef] [Green Version]
- Brasil, F.B.; de Almeida, F.J.S.; Luckachaki, M.D.; Dall’Oglio, E.L.; de Oliveira, M.R. The C-glucosyl flavone isoorientin pretreatment attenuates the methylglyoxal-induced mitochondrial dysfunction in the human neuroblastoma SH-SY5Y cells: Role for the AMPK-PI3K/Akt/Nrf2/γ-GCL/GSH axis. Metab. Brain Dis. 2022. [Google Scholar] [CrossRef] [PubMed]
- Tu, L.; Wang, Y.; Chen, D.; Xiang, P.; Shen, J.; Li, Y.; Wang, S. Protective Effects of notoginsenoside R1 via regulation of the PI3K-Akt-mTOR/JNK pathway in neonatal cerebral hypoxic–ischemic brain injury. Neurochem. Res. 2018, 43, 1210–1226. [Google Scholar] [CrossRef] [Green Version]
- Torrealba, N.; Rodriguez-Berriguete, G.; Fraile, B.; Olmedilla, G.; Martínez-Onsurbe, P.; Sánchez-Chapado, M.; Paniagua, R.; Royuela, M. PI3K pathway and Bcl-2 family. Clinicopathological features in prostate cancer. Aging Male 2018, 21, 211–222. [Google Scholar] [CrossRef]
- Zhang, W.; Zhang, J.-Q.; Meng, F.-M.; Xue, F.-S. Dexmedetomidine protects against lung ischemia–reperfusion injury by the PI3K/Akt/HIF-1α signaling pathway. J. Anesth. 2016, 30, 826–833. [Google Scholar] [CrossRef]
- Wu, X.-T.; Ansari, A.R.; Pang, X.-X.; Li, H.-Z.; Zhang, Z.-W.; Luo, Y.; Arshad, M.; Song, H. Visfatin plays a significant role in alleviating lipopolysaccharide-induced apoptosis and autophagy through PI3K/AKT signaling pathway during acute lung injury in mice. Arch. Immunol. Ther. Exp. 2019, 67, 249–261. [Google Scholar] [CrossRef]
- Nguyen, T.; Sherratt, P.J.; Huang, H.C.; Yang, C.S.; Pickett, C.B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J. Biol. Chem. 2003, 278, 4536–4541. [Google Scholar] [CrossRef] [Green Version]
- Tkachev, V.O.; Menshchikova, E.B.; Zenkov, N.K. Mechanism of the Nrf2/Keap1/ARE signaling system. Biochemistry 2011, 76, 407–422. [Google Scholar] [CrossRef]
- Kensler, T.W.; Wakabayashi, N.; Biswal, S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 89–116. [Google Scholar] [CrossRef] [PubMed]
- Kirkby, K.A.; Adin, C.A. Products of heme oxygenase and their potential therapeutic applications. Am. J. Physiol. Renal. Physiol. 2006, 290, 563–571. [Google Scholar] [CrossRef] [Green Version]
- Tomazini, B.M.; Maia, I.S.; Cavalcanti, A.B.; Berwanger, O.; Rosa, R.G.; Veiga, V.C.; Avezum, A.; Lopes, R.D.; Bueno, F.R.; Silva, M.V.A.O.; et al. Effect of dexamethasone on days alive and ventilator-free in patients with moderate or severe acute respiratory distress syndrome and COVID-19 the CoDEX randomized clinical trial. JAMA 2020, 324, 1307–1316. [Google Scholar] [CrossRef]
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Zhang, Q.; Cheng, S.; Xin, Z.; Deng, H.; Wang, Y.; Li, Q.; Wu, G.; Chen, W. 1,2,3,4,6-O-Pentagalloylglucose Protects against Acute Lung Injury by Activating the AMPK/PI3K/Akt/Nrf2 Pathway. Int. J. Mol. Sci. 2022, 23, 14423. https://doi.org/10.3390/ijms232214423
Zhang Q, Cheng S, Xin Z, Deng H, Wang Y, Li Q, Wu G, Chen W. 1,2,3,4,6-O-Pentagalloylglucose Protects against Acute Lung Injury by Activating the AMPK/PI3K/Akt/Nrf2 Pathway. International Journal of Molecular Sciences. 2022; 23(22):14423. https://doi.org/10.3390/ijms232214423
Chicago/Turabian StyleZhang, Qi, Sai Cheng, Zhiming Xin, Haohua Deng, Ying Wang, Qiang Li, Gangwei Wu, and Wei Chen. 2022. "1,2,3,4,6-O-Pentagalloylglucose Protects against Acute Lung Injury by Activating the AMPK/PI3K/Akt/Nrf2 Pathway" International Journal of Molecular Sciences 23, no. 22: 14423. https://doi.org/10.3390/ijms232214423