282
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Artesunate-Nanoliposome-TPP, a Novel Drug Delivery System That Targets the Mitochondria, Attenuates Cisplatin-Induced Acute Kidney Injury by Suppressing Oxidative Stress and Inflammatory Effects

, , , , , , , & show all
Pages 1385-1408 | Received 11 Oct 2023, Accepted 25 Jan 2024, Published online: 11 Feb 2024

References

  • Bellomo R, Kellum JA, Ronco C. Acute kidney injury. Lancet. 2012;380(9843):756–766. doi:10.1016/s0140-6736(11)61454-2
  • Al-Jaghbeer M, Dealmeida D, Bilderback A, Ambrosino R, Kellum JA. Clinical decision support for in-hospital AKI. J Am Soc Nephrol. 2018;29(2):654–660. doi:10.1681/asn.2017070765
  • Hoste EA, Bagshaw SM, Bellomo R, et al. Epidemiology of acute kidney injury in critically ill patients: the multinational AKI-EPI study. Intensive Care Med. 2015;41(8):1411–1423. doi:10.1007/s00134-015-3934-7
  • Li HD, Meng XM, Huang C, Zhang L, Lv XW, Li J. Application of herbal traditional Chinese medicine in the treatment of acute kidney injury. Front Pharmacol. 2019;10:376. doi:10.3389/fphar.2019.00376
  • Kellum JA, Chawla LS, Keener C, et al. The effects of alternative resuscitation strategies on acute kidney injury in patients with septic shock. Am J Respir Crit Care Med. 2016;193(3):281–287. doi:10.1164/rccm.201505-0995OC
  • Linkermann A. Nonapoptotic cell death in acute kidney injury and transplantation. Kidney Int. 2016;89(1):46–57. doi:10.1016/j.kint.2015.10.008
  • Waikar SS, Liu KD, Chertow GM. Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol. 2008;3(3):844–861. doi:10.2215/cjn.05191107
  • Wang W, Chen J, Hu D, et al. SARS-CoV-2 N protein induces acute kidney injury via Smad3-dependent G1 cell cycle arrest mechanism. Adv Sci. 2022;9(3):e2103248. doi:10.1002/advs.202103248
  • Aloy B, Janus N, Isnard-Bagnis C, Deray G, Launay-Vacher V. Renal toxicity of anticancer drugs. Nephrol Ther. 2021;17(7):553–563. doi:10.1016/j.nephro.2021.09.001
  • Liu S, Zhao J, Wang F. Acute kidney injury in cancer patients. Clin Exp Nephrol. 2022;26(2):103–112. doi:10.1007/s10157-021-02131-7
  • Rosner MH, Perazella MA, Ingelfinger JR. Acute kidney injury in patients with cancer. N Engl J Med. 2017;376(18):1770–1781. doi:10.1056/NEJMra1613984
  • Ghosh S. Cisplatin: the first metal based anticancer drug. Bioorg Chem. 2019;88:102925. doi:10.1016/j.bioorg.2019.102925
  • Ojha S, Venkataraman B, Kurdi A, Mahgoub E, Sadek B, Rajesh M. Plant-derived agents for counteracting cisplatin-induced nephrotoxicity. Oxid Med Cell Longev. 2016;2016:4320374. doi:10.1155/2016/4320374
  • Pabla N, Dong Z. Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int. 2008;73(9):994–1007. doi:10.1038/sj.ki.5002786
  • Fang CY, Lou DY, Zhou LQ . Natural products: potential treatments for cisplatin-induced nephrotoxicity. Acta Pharmacol Sin. 2021;42(12):1951–1969. doi:10.1038/s41401-021-00620-9
  • Li J, Wu Y, Chen C, Zhang, W, Yue, L, Liu, T, et al. A systematic review for prevention of cisplatin-induced nephrotoxicity using different hydration protocols and meta-analysis for magnesium hydrate supplementation. Clin Exp Nephrol. 2024;28(1):1–12. doi:10.1007/s10157-023-02386-2
  • Fukushima K, Futatsugi A, Maekawa M, Naito S, Okada A, Sugioka N. Comparison of cisplatin-induced nephrotoxicity between single-dose and split-dose administration to rats. Biomed Pharmacother. 2022;147:112619. doi:10.1016/j.biopha.2022.112619
  • Darwish MA, Abo-Youssef AM, Khalaf MM, Abo-Saif AA, Saleh IG, Abdelghany TM. Resveratrol influences platinum pharmacokinetics: a novel mechanism in protection against cisplatin-induced nephrotoxicity. Toxicol Lett. 2018;290:73–82. doi:10.1016/j.toxlet.2018.03.023
  • Nakamura T, Yonezawa A, Hashimoto S, Katsura T, Inui K. Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity. Biochem Pharmacol. 2010;80(11):1762–1767. doi:10.1016/j.bcp.2010.08.019
  • Kleih M, Böpple K, Dong M, et al. Direct impact of cisplatin on mitochondria induces ROS production that dictates cell fate of ovarian cancer cells. Cell Death Dis. 2019;10(11):851. doi:10.1038/s41419-019-2081-4
  • Brooks C, Wei Q, Cho SG, Dong Z. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J Clin Invest. 2009;119(5):1275–1285. doi:10.1172/jci37829
  • Klayman DL. Qinghaosu (artemisinin): an antimalarial drug from China. Science. 1985;228(4703):1049–1055. doi:10.1126/science.3887571
  • Dentinger CM, Rakotomanga TA, Rakotondrandriana A, et al. Efficacy of artesunate-amodiaquine and artemether-lumefantrine for uncomplicated Plasmodium falciparum malaria in Madagascar, 2018. Malar J. 2021;20(1):432. doi:10.1186/s12936-021-03935-4
  • Visser MT, Zonneveld R, Peto TJ, van Vugt M, Dondorp AM, van der Pluijm RW. Are national treatment guidelines for falciparum malaria in line with WHO recommendations and is antimalarial resistance taken into consideration? - A review of guidelines in non-endemic countries. Trop Med Int Health. 2022;27(2):129–136. doi:10.1111/tmi.13715
  • Hess KM, Goad JA, Arguin PM. Intravenous artesunate for the treatment of severe malaria. Ann Pharmacother. 2010;44(7–8):1250–1258. doi:10.1345/aph.1M732
  • Shah PJ, Koshy J, Everett N, Attia E. Severe Plasmodium falciparum malaria treated with investigational artesunate in the United States. J Pharm Pract. 2020;33(1):108–112. doi:10.1177/0897190018782367
  • Li B, Zhang Z, Fu Y. Anti-inflammatory effects of artesunate on atherosclerosis via miR-16-5p and TXNIP regulation of the NLRP3 inflammasome. Ann Transl Med. 2021;9(20):1558. doi:10.21037/atm-21-4939
  • Ghosh AK, Miller H, Knox K, Kundu M, Henrickson KJ, Arav-Boger R. Inhibition of human coronaviruses by antimalarial peroxides. ACS Infect Dis. 2021;7(7):1985–1995. doi:10.1021/acsinfecdis.1c00053
  • Shakir L, Hussain M, Javeed A, Ashraf M, Riaz A. Artemisinins and immune system. Eur J Pharmacol. 2011;668(1–2):6–14. doi:10.1016/j.ejphar.2011.06.044
  • Efferth T, Dunstan H, Sauerbrey A, Miyachi H, Chitambar CR. The anti-malarial artesunate is also active against cancer. Int J Oncol. 2001;18(4):767–773. doi:10.3892/ijo.18.4.767
  • Lei XY, Tan RZ, Jia J, et al. Artesunate relieves acute kidney injury through inhibiting macrophagic mincle-mediated necroptosis and inflammation to tubular epithelial cell. J Cell Mol Med. 2021;25(18):8775–8788. doi:10.1111/jcmm.16833
  • Shen S, Liu SZ, Du MB, Ge KY, Song LH, Ye ZG. Determination of equilibrium solubility and apparent oil /water partition coefficient of artesunate. Chin J Exp Traditional Med Formulae. 2013;19(19):9–12.
  • Fanello C, Hoglund RM, Lee SJ, et al. Pharmacokinetic study of rectal artesunate in children with severe malaria in Africa. Antimicrob Agents Chemother. 2021;65(4). doi:10.1128/aac.02223-20
  • Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev. 2013;65(1):36–48. doi:10.1016/j.addr.2012.09.037
  • Bozzuto G, Molinari A. Liposomes as nanomedical devices. Int J Nanomed. 2015;10:975–999. doi:10.2147/ijn.S68861
  • Amekyeh H, Alkhader E, Sabra R, Billa N. Prospects of curcumin nanoformulations in cancer management. Molecules. 2022;27(2):361. doi:10.3390/molecules27020361
  • Khan S, Hussain A, Attar F, et al. A review of the berberine natural polysaccharide nanostructures as potential anticancer and antibacterial agents. Biomed Pharmacother. 2022;146:112531. doi:10.1016/j.biopha.2021.112531
  • Quijia CR, Chorilli M. Piperine for treating breast cancer: a review of molecular mechanisms, combination with anticancer drugs, and nanosystems. Phytother Res. 2022;36(1):147–163. doi:10.1002/ptr.7291
  • Shen S, Du M, Liu Q, et al. Development of GLUT1-targeting alkyl glucoside-modified dihydroartemisinin liposomes for cancer therapy. Nanoscale. 2020;12(42):21901–21912. doi:10.1039/d0nr05138a
  • Gu L, Zhang J, Liu D, et al. Development of artesunate intelligent prodrug liposomes based on mitochondrial targeting strategy. J Nanobiotechnology. 2022;20(1):376. doi:10.1186/s12951-022-01569-5
  • Deng F, Zhang H, Zhou W, et al. TRPA1 promotes cisplatin-induced acute kidney injury via regulating the endoplasmic reticulum stress-mitochondrial damage. J Transl Med. 2023;21(1):695. doi:10.1186/s12967-023-04351-9
  • Radford MG, Jr., Donadio JV, Jr., Bergstralh EJ, Grande, JP, et al. Predicting renal outcome in IgA nephropathy. J Am Soc Nephrol. 1997;8(2):199–207. doi:10.1681/asn.V82199
  • Xie SB, Wang WM, Chen N. Progression of renal tubulointerstitial fibrosis and expression of α-SMA,TGF-β_1 and VDR in rat UUO models. J Shanghai Jiaotong Univ. 2010;30(7):1.
  • Li W, Xu Q, He YF, et al. Anti-tumor effect of steamed codonopsis lanceolata in H22 tumor-bearing mice and its possible mechanism. Nutrients. 2015;7(10):8294–8307. doi:10.3390/nu7105395
  • Lingaraju MC, Pathak NN, Begum J, et al. Betulinic acid attenuates renal oxidative stress and inflammation in experimental model of murine polymicrobial sepsis. Eur J Pharm Sci. 2015;70:12–21. doi:10.1016/j.ejps.2015.01.001
  • Ozkok A, Ravichandran K, Wang Q, Ljubanovic D, Edelstein CL. NF-κB transcriptional inhibition ameliorates cisplatin-induced acute kidney injury (AKI). Toxicol Lett. 2016;240(1):105–113. doi:10.1016/j.toxlet.2015.10.028
  • Mukhopadhyay P, Rajesh M, Pan H, et al. Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy. Free Radic Biol Med. 2010;48(3 457–467). doi:10.1016/j.freeradbiomed.2009.11.022
  • Hagar H, Medany AE, Salam R, Medany GE, Nayal OA. Betaine supplementation mitigates cisplatin-induced nephrotoxicity by abrogation of oxidative/nitrosative stress and suppression of inflammation and apoptosis in rats. Exp Toxicol Pathol. 2015;67(2):133–141. doi:10.1016/j.etp.2014.11.001
  • Gu H, Gwon MG, Kim JH, Leem J, Lee SJ, Ahmed M. Oridonin attenuates cisplatin-induced acute kidney injury via inhibiting oxidative stress, apoptosis, and inflammation in mice. Biomed Res Int. 2022;2022:3002962. doi:10.1155/2022/3002962
  • Zaaba NE, Beegam S, Elzaki O, et al. The nephroprotective effects of α-bisabolol in cisplatin-induced acute kidney injury in mice. Biomedicines. 2022;10(4):842. doi:10.3390/biomedicines10040842
  • Yan X, Tan XY, Li YX, et al. A stepwise targeting curcumin derivative, Ser@TPP@CUR, for acute kidney injury. ACS Med Chem Lett. 2022;13(4):554–559. doi:10.1021/acsmedchemlett.1c00585
  • Hao Q, Xiao X, Zhen J, et al. Resveratrol attenuates acute kidney injury by inhibiting death receptor‑mediated apoptotic pathways in a cisplatin‑induced rat model. Mol Med Rep. 2016;14(4):3683–3689. doi:10.3892/mmr.2016.5714
  • Zhou L, Yu P, Wang TT, et al. Polydatin attenuates cisplatin-induced acute kidney injury by inhibiting ferroptosis. Oxid Med Cell Longev. 2022;2022:9947191. doi:10.1155/2022/9947191
  • Dang WZ, Li H, Jiang B, et al. Therapeutic effects of artesunate on lupus-prone MRL/lpr mice are dependent on T follicular helper cell differentiation and activation of JAK2-STAT3 signaling pathway. Phytomedicine. 2019;62:152965. doi:10.1016/j.phymed.2019.152965
  • Chen Q, Wang Z, Lv J, et al. Efficacy and safety of artesunate for patients with IgA nephropathy: a study protocol for a multicenter, double-blind, randomized, placebo-controlled trial. Trials. 2022;23(1):444. doi:10.1186/s13063-022-06336-3
  • Sun Z, Ma Y, Chen F, Wang S, Chen B, Shi J. Artesunate ameliorates high glucose-induced rat glomerular mesangial cell injury by suppressing the TLR4/NF-κB/NLRP3 inflammasome pathway. Chem Biol Interact. 2018;293:11–19. doi:10.1016/j.cbi.2018.07.011
  • Patra JK, Das G, Fraceto LF, et al. Nano based drug delivery systems: recent developments and future prospects. J Nanobiotechnology. 2018;16(1):71. doi:10.1186/s12951-018-0392-8
  • Lammers T, Ferrari M. The success of nanomedicine. Nano Today. 2020;31. doi:10.1016/j.nantod.2020.100853
  • Chang HI, Yeh MK. Clinical development of liposome-based drugs: formulation, characterization, and therapeutic efficacy. Int J Nanomed. 2012;7:49–60. doi:10.2147/ijn.S26766
  • Hu C, Liang K, An R, Wang XH, You LS. Tissue distribution of TPGS modified artesunate liposome and its metabolites in rats. Zhongguo Zhong Yao Za Zhi. 2018;43(2):325–331. doi:10.19540/j.cnki.cjcmm.20171023.006
  • Karim N, Shishir MRI, Rashwan AK, Ke H, Chen W. Suppression of palmitic acid-induced hepatic oxidative injury by neohesperidin-loaded pectin-chitosan decorated nanoliposomes. Int J Biol Macromol. 2021;183:908–917. doi:10.1016/j.ijbiomac.2021.05.010
  • Li Y, Xu F, Li X, et al. Development of curcumin-loaded composite phospholipid ethosomes for enhanced skin permeability and vesicle stability. Int J Pharm. 2021;592:119936. doi:10.1016/j.ijpharm.2020.119936
  • Ramesh G, Reeves WB. TNF-alpha mediates chemokine and cytokine expression and renal injury in cisplatin nephrotoxicity. J Clin Invest. 2002;110(6):835–842. doi:10.1172/jci15606
  • Holditch SJ, Brown CN, Lombardi AM, Nguyen KN, Edelstein CL. Recent advances in models, mechanisms, biomarkers, and interventions in cisplatin-induced acute kidney injury. Int J Mol Sci. 2019;20(12):3011. doi:10.3390/ijms20123011
  • Kim DU, Kim DG, Choi JW, et al. Loganin attenuates the severity of acute kidney injury induced by cisplatin through the inhibition of ERK activation in mice. Int J Mol Sci. 2021;22(3). doi:10.3390/ijms22031421
  • Faubel S, Lewis EC, Reznikov L, et al. Cisplatin-induced acute renal failure is associated with an increase in the cytokines interleukin (IL)-1beta, IL-18, IL-6, and neutrophil infiltration in the kidney. J Pharmacol Exp Ther. 2007;322(1):8–15. doi:10.1124/jpet.107.119792
  • Ramesh G, Reeves WB. Salicylate reduces cisplatin nephrotoxicity by inhibition of tumor necrosis factor-alpha. Kidney Int. 2004;65(2):490–499. doi:10.1111/j.1523-1755.2004.00413.x
  • Zeng L, Lin L, Xiao W, Li Y. L-theanine protects rat kidney from D-galactose-induced injury via inhibition of the AGEs/RAGE signaling pathway. Eur J Pharmacol. 2022;927:175072. doi:10.1016/j.ejphar.2022.175072
  • Shen C, Ma Y, Zeng Z, Yin Q, Hong Y, Hou X and Liu X. (2017). RAGE-Specific Inhibitor FPS-ZM1 Attenuates AGEs-Induced Neuroinflammation and Oxidative Stress in Rat Primary Microglia. Neurochem Res, 42(10), 2902–2911. 10.1007/s11064-017-2321-x
  • Giridharan VV, Thandavarayan RA, Bhilwade HN. Schisandrin B, attenuates cisplatin-induced oxidative stress, genotoxicity and neurotoxicity through modulating NF-κB pathway in mice. Free Radic Res. 2012;46(1):50–60. doi:10.3109/10715762.2011.638291
  • Gao X, Wang J, Wang Y . Fucoidan-ferulic acid nanoparticles alleviate cisplatin-induced acute kidney injury by inhibiting the cGAS-STING pathway. Int J Biol Macromol. 2022;223(Pt A):1083–1093. doi:10.1016/j.ijbiomac.2022.11.062
  • Peiro G, Alary J, Cravedi JP, Rathahao E, Steghens JP, Guéraud F. Dihydroxynonene mercapturic acid, a urinary metabolite of 4-hydroxynonenal, as a biomarker of lipid peroxidation. Biofactors. 2005;24(1–4):89–96. doi:10.1002/biof.5520240110
  • Ansari MA. Sinapic acid modulates Nrf2/HO-1 signaling pathway in cisplatin-induced nephrotoxicity in rats. Biomed Pharmacother. 2017;93:646–653. doi:10.1016/j.biopha.2017.06.085
  • Zhao W, Li J, Li Y, Chen Y, Jin H. Preventive effect of collagen peptides from acaudina molpadioides on acute kidney injury through attenuation of oxidative stress and inflammation. Oxid Med Cell Longev. 2022;2022:8186838. doi:10.1155/2022/8186838
  • Diao C, Chen Z, Qiu T, et al. Inhibition of PRMT5 attenuates oxidative stress-induced pyroptosis via activation of the Nrf2/HO-1 signal pathway in a mouse model of renal ischemia-reperfusion injury. Oxid Med Cell Longev. 2019;2019:2345658. doi:10.1155/2019/2345658
  • Tran MT, Zsengeller ZK, Berg AH, et al. PGC1α drives NAD biosynthesis linking oxidative metabolism to renal protection. Nature. 2016;531(7595):528–532. doi:10.1038/nature17184