Benzoylaconine Protects Skeletal Muscle Against Ischemia-Reperfusion Injury Through Activation of IF1-Dependent AMPK/Nrf2 Axis

References

• Morikawa T, Shimasaki M, Ichiseki T, Ueda S, Ueda Y, Takahashi K. The possibility of IPC to prevent ischemic-reperfusion injury in skeletal muscle in a rat. J Clin Med. 2023;12(4):1501. doi:10.3390/jcm12041501
   PubMed Web of Science ®Google Scholar
• Erol K, Sozmen EY, Küçük Ü, Kucuk L. Effect of pheniramine maleate on rat skeletal muscle ischemia-reperfusion injury. Ulus Travma Acil Cerrahi Derg. 2022;28(12):1667–1673. doi:10.14744/tjtes.2021.00312
   PubMed Web of Science ®Google Scholar
• Murray IR, Gonzalez ZN, Baily J, et al. αv integrins on mesenchymal cells regulate skeletal and cardiac muscle fibrosis. Nat Commun. 2017;8(1):1118. doi:10.1038/s41467-017-01097-z
   PubMedGoogle Scholar
• Li Y, Jiang J, Tong L, et al. Bilobalide protects against ischemia/reperfusion-induced oxidative stress and inflammatory responses via the MAPK/NF-κB pathways in rats. BMC Musculoskeletal Dis. 2020;21(1):449. doi:10.1186/s12891-020-03479-9
   PubMed Web of Science ®Google Scholar
• Li B, Liu L. Fibroblast growth factor 21, a stress regulator, inhibits Drp1 activation to alleviate skeletal muscle ischemia/reperfusion injury. Lab Invest. 2022;102(9):979–988. doi:10.1038/s41374-022-00787-7
   PubMed Web of Science ®Google Scholar
• Zhang QQ, Chen FH, Wang F, Di XM, Li W, Zhang H. A novel modulator of the renin-angiotensin system, benzoylaconitine, attenuates hypertension by targeting ACE/ACE2 in enhancing vasodilation and alleviating vascular inflammation. Front Pharm. 2022;13:841435. doi:10.3389/fphar.2022.841435
   PubMed Web of Science ®Google Scholar
• Xu YW, Xu ZD, An R, Zhang H, Wang XH. Revealing the synergistic mechanism of Shenfu Decoction for anti-heart failure through network pharmacology strategy. Chin J Nat Med. 2020;18(7):536–549. doi:10.1016/s1875-5364(20)30064-9
   PubMed Web of Science ®Google Scholar
• Zhou C, Gao J, Ji H, et al. Benzoylaconine modulates LPS-induced responses through inhibition of toLl-like receptor-Mediated NF-κB and MAPK Signaling in RAW264.7 Cells. Inflammation. 2021;44(5):2018–2032. doi:10.1007/s10753-021-01478-z
   PubMed Web of Science ®Google Scholar
• Deng XH, Liu JJ, Sun XJ, Dong JC, Huang JH. Benzoylaconine induces mitochondrial biogenesis in mice via activating AMPK signaling cascade. Acta Pharmacol Sin. 2019;40(5):658–665. doi:10.1038/s41401-018-0174-8
   PubMed Web of Science ®Google Scholar
• Zhang H, Wu Q, Li W, et al. Absorption and metabolism of three monoester-diterpenoid alkaloids in Aconitum carmichaeli after oral administration to rats by HPLC-MS. J Ethnopharmacol. 2014;154(3):645–652. doi:10.1016/j.jep.2014.04.039
   PubMed Web of Science ®Google Scholar
• Zhang H, Liu M, Zhang W, et al. Comparative pharmacokinetics of three monoester-diterpenoid alkaloids after oral administration of Acontium carmichaeli extract and its compatibility with other herbal medicines in Sini Decoction to rats. Biomed Chromatogr. 2015;29(7):1076–1083. doi:10.1002/bmc.3394
   PubMed Web of Science ®Google Scholar
• Zhang W, Zhang H, Sun S, et al. Comparative pharmacokinetics of hypaconitine after oral administration of pure hypaconitine, Aconitum carmichaelii extract and Sini Decoction to rats. Molecules. 2015;20(1):1560–1570. doi:10.3390/molecules20011560
   PubMed Web of Science ®Google Scholar
• Zhang H, Sun S, Zhang W, et al. Biological activities and pharmacokinetics of aconitine, benzoylaconine, and aconine after oral administration in rats. Drug Test Anal. 2016;8(8):839–846. doi:10.1002/dta.1858
   PubMed Web of Science ®Google Scholar
• Wada K, Nihira M, Hayakawa H, Tomita Y, Hayashida M, Ohno Y. Effects of long-term administrations of aconitine on electrocardiogram and tissue concentrations of aconitine and its metabolites in mice. Forensic Sci Int. 2005;148(1):21–29. doi:10.1016/j.forsciint.2004.04.016
   PubMed Web of Science ®Google Scholar
• Madhavi YV, Gaikwad N, Yerra VG, Kalvala AK, Nanduri S, Kumar A. Targeting AMPK in diabetes and diabetic complications: Energy homeostasis, autophagy and mitochondrial health. Curr Med Chem. 2019;26(27):5207–5229. doi:10.2174/0929867325666180406120051
   PubMed Web of Science ®Google Scholar
• Jia J, Bissa B, Brecht L, et al. AMPK, a regulator of metabolism and autophagy, is activated by lysosomal damage via a novel galectin-directed ubiquitin signal transduction system. Mol Cell. 2020;77(5):951–969.e9. doi:10.1016/j.molcel.2019.12.028
   PubMed Web of Science ®Google Scholar
• Zhao P, Sun X, Chaggan C, et al. An AMPK-caspase-6 axis controls liver damage in nonalcoholic steatohepatitis. Science. 2020;367:(6478):652–660. doi:10.1126/science.aay0542
   PubMed Web of Science ®Google Scholar
• Li C, Chi J, Dai H, et al. Salidroside attenuates cerebral ischemia/reperfusion injury by regulating TSC2-induced autophagy. Exp Brain Res. 2023;241(1):113–125. doi:10.1007/s00221-022-06493-6
   PubMed Web of Science ®Google Scholar
• Yu H, Hong X, Liu L, et al. Cordycepin Decreases Ischemia/Reperfusion Injury in Diabetic Hearts via Upregulating AMPK/Mfn2-dependent mitochondrial fusion. Front Pharmacol. 2021;12:754005. doi:10.3389/fphar.2021.754005
   PubMed Web of Science ®Google Scholar
• Zhao B, G-P L, Peng -J-J, et al. Schizandrin B attenuates hypoxia/reoxygenation injury in H9c2 cells by activating the AMPK/Nrf2 signaling pathway. Exp Ther Med. 2021;21(3):220. doi:10.3892/etm.2021.9651
   PubMed Web of Science ®Google Scholar
• Li J, Zheng X, Ma X, et al. Melatonin protects against chromium(VI)-induced cardiac injury via activating the AMPK/Nrf2 pathway. J Inorg Biochem. 2019;197:110698. doi:10.1016/j.jinorgbio.2019.110698
   PubMed Web of Science ®Google Scholar
• Tang C, Hong J, Hu C, et al. Palmatine Protects against Cerebral Ischemia/Reperfusion Injury by Activation of the AMPK/Nrf2 Pathway. Oxid Med Cell Longev. 2021;2021:1–12. doi:10.1155/2021/6660193
   Web of Science ®Google Scholar
• Jiang W, Song J, Zhang S, Ye Y, Wang J, Zhang Y. CTRP13 Protects H9c2 Cells Against Hypoxia/Reoxygenation (H/R)-Induced Injury Via Regulating the AMPK/Nrf2/ARE Signaling Pathway. Cell Transplant. 2021;30:9636897211033275. doi:10.1177/09636897211033275
   Web of Science ®Google Scholar
• Lee HJ, Moon J, Chung I, et al. ATP synthase inhibitory factor 1 (IF1), a novel myokine, regulates glucose metabolism by AMPK and Akt dual pathways. FASEB J. 2019;33(12):14825–14840. doi:10.1096/fj.201901440RR
   PubMed Web of Science ®Google Scholar
• Faccenda D, Gorini G, Jones A, et al. The ATPase Inhibitory Factor 1 (IF1) regulates the expression of the mitochondrial Ca2+ uniporter (MCU) via the AMPK/CREB pathway. Biochim Biophys Acta. 2021;1868(1):118860. doi:10.1016/j.bbamcr.2020.118860
   Web of Science ®Google Scholar
• J-W W, Hu H, J-s H, L-K M. ATPase inhibitory factor 1 protects the heart from acute myocardial ischemia/reperfusion injury through activating AMPK signaling pathway. Int J Biol Sci. 2022;18(2):731–741. doi:10.7150/ijbs.64956
   PubMed Web of Science ®Google Scholar
• Kahancová A, Sklenář F, Ježek P, Dlasková A. Overexpression of native IF1 downregulates glucose-stimulated insulin secretion by pancreatic INS-1E cells. Sci Rep. 2020;10(1):1551. doi:10.1038/s41598-020-58411-x
   PubMed Web of Science ®Google Scholar
• He J, He L, Lu F, Geng B, Xia Y. Low-molecular-weight heparin calcium attenuates the tourniquet-induced ischemia-reperfusion injury in rats. Injury. 2021;52(8):2068–2074. doi:10.1016/j.injury.2021.03.006
   PubMed Web of Science ®Google Scholar
• Zhang M, Zhang M, Wang L, et al. Activation of cannabinoid type 2 receptor protects skeletal muscle from ischemia-reperfusion injury partly via Nrf2 signaling. Life Sci. 2019;230:55–67. doi:10.1016/j.lfs.2019.05.056
   PubMed Web of Science ®Google Scholar
• Huang M, Cheng G, Tan H, et al. Capsaicin protects cortical neurons against ischemia/reperfusion injury via down-regulating NMDA receptors. Exp Neurol. 2017;295:66–76. doi:10.1016/j.expneurol.2017.05.001
   PubMed Web of Science ®Google Scholar
• Bai X, Zhu Y, Jie J, Li D, Song L, Luo J. Maackiain protects against sepsis via activating AMPK/Nrf2/HO-1 pathway. Int Immunopharm. 2022;108:108710. doi:10.1016/j.intimp.2022.108710
   PubMed Web of Science ®Google Scholar
• Sharma A, Anand SK, Singh N, Dwivedi UN, Kakkar P. AMP-activated protein kinase: an energy sensor and survival mechanism in the reinstatement of metabolic homeostasis. Exp Cell Res. 2023;428(1):113614. doi:10.1016/j.yexcr.2023.113614
   PubMed Web of Science ®Google Scholar
• Xue H, Cao H, Xing C, et al. Selenium triggers Nrf2-AMPK crosstalk to alleviate cadmium-induced autophagy in rabbit cerebrum. Toxicology. 2021;459:152855. doi:10.1016/j.tox.2021.152855
   PubMed Web of Science ®Google Scholar
• Kim Y, Kim YS, Kim HY, et al. Early Treatment with Poly(ADP-Ribose) Polymerase-1 Inhibitor (JPI-289) Reduces Infarct Volume and Improves Long-Term Behavior in an Animal Model of Ischemic Stroke. Mol Neurobiol. 2018;55(9):7153–7163. doi:10.1007/s12035-018-0910-6
   PubMed Web of Science ®Google Scholar
• Wu B, Qiu W, Wang P, et al. p53 independent induction of PUMA mediates intestinal apoptosis in response to ischaemia-reperfusion. Gut. 2007;56(5):645–654. doi:10.1136/gut.2006.101683
   PubMed Web of Science ®Google Scholar
• Qiu Z, Lei S, Zhao B, et al. NLRP3 Inflammasome Activation-Mediated Pyroptosis Aggravates Myocardial Ischemia/Reperfusion Injury in Diabetic Rats. Oxid Med Cell Longev. 2017;2017:9743280. doi:10.1155/2017/9743280
   PubMed Web of Science ®Google Scholar
• Chen L, Yan L, Zhang W. Benzoylaconine improves mitochondrial function in oxygen-glucose deprivation and reperfusion-induced cardiomyocyte injury by activation of the AMPK/PGC-1 axis. Korean J Physiol Pha. 2022;26(5):325–333. doi:10.4196/kjpp.2022.26.5.325
   PubMed Web of Science ®Google Scholar
• Ma J, Chen T, Wang R. Astragaloside IV ameliorates cognitive impairment and protects oligodendrocytes from antioxidative stress via regulation of the SIRT1/Nrf2 signaling pathway. Neurochem Int. 2023;167:105535. doi:10.1016/j.neuint.2023.105535
   PubMed Web of Science ®Google Scholar
• Wani FA, Ibrahim MA, Ameen SH, et al. Platelet Rich Plasma and Adipose-Derived Mesenchymal Stem Cells Mitigate Methotrexate-Induced Nephrotoxicity in Rat via Nrf2/Pparγ/HO-1 and NF-Κb/Keap1/Caspase-3 Signaling Pathways: oxidative Stress and Apoptosis Interplay. Toxics. 2023;11(5):398. doi:10.3390/toxics11050398
   PubMed Web of Science ®Google Scholar
• Guo K, Shang Y, Wang Z, et al. BRG1 alleviates microglial activation by promoting the KEAP1-NRF2/HO-1 signaling pathway and minimizing oxidative damage in cerebral ischemia-reperfusion. Int Immunopharm. 2023;119:110201. doi:10.1016/j.intimp.2023.110201
   PubMed Web of Science ®Google Scholar
• Paskeh MDA, Asadi A, Mirzaei S, et al. Targeting AMPK signaling in ischemic/reperfusion injury: from molecular mechanism to pharmacological interventions. Cell Signal. 2022;94:110323. doi:10.1016/j.cellsig.2022.110323
   PubMed Web of Science ®Google Scholar
• Zhu Y, Wang C, Luo J, et al. The protective role of Zingerone in a murine asthma model via activation of the AMPK/Nrf2/HO-1 pathway. Food Funct. 2021;12(7):3120–3131. doi:10.1039/d0fo01583k
   PubMed Web of Science ®Google Scholar
• Gugliandolo A, Bramanti P, Mazzon E. Activation of Nrf2 by Natural Bioactive Compounds: a Promising Approach for Stroke? Int J Mol Sci. 2020;21(14):4875. doi:10.3390/ijms21144875
   PubMed Web of Science ®Google Scholar
• Yang K, Long Q, Saja K, et al. Knockout of the ATPase inhibitory factor 1 protects the heart from pressure overload-induced cardiac hypertrophy. Sci Rep. 2017;7(1):10501. doi:10.1038/s41598-017-11251-8
   PubMedGoogle Scholar
• Fujikawa M, Imamura H, Nakamura J, Yoshida M. Assessing actual contribution of IF1, inhibitor of mitochondrial FoF1, to ATP homeostasis, cell growth, mitochondrial morphology, and cell viability. J Biol Chem. 2012;287(22):18781–18787. doi:10.1074/jbc.M112.345793
   PubMed Web of Science ®Google Scholar
• Esparza-Moltó PB, Cuezva JM. The Role of Mitochondrial H(+)-ATP Synthase in Cancer. Front Oncol. 2018;8:53. doi:10.3389/fonc.2018.00053
   PubMed Web of Science ®Google Scholar
• Sánchez-Cenizo L, Formentini L, Aldea M, et al. Up-regulation of the ATPase inhibitory factor 1 (IF1) of the mitochondrial H+-ATP synthase in human tumors mediates the metabolic shift of cancer cells to a Warburg phenotype. J Biol Chem. 2010;285(33):25308–25313. doi:10.1074/jbc.M110.146480
   PubMed Web of Science ®Google Scholar
• Kahancová A, Sklenář F, Ježek P, Dlasková A. Regulation of glucose-stimulated insulin secretion by ATPase Inhibitory Factor 1 (IF1). FEBS Lett. 2018;592(6):999–1009. doi:10.1002/1873-3468.12991
   PubMed Web of Science ®Google Scholar