199
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Neuroprotective effect of canagliflozin against cisplatin-induced cerebral cortex injury is mediated by regulation of HO-1/PPAR-γ, SIRT1/FOXO-3, JNK/AP-1, TLR4/iNOS, and Ang II/Ang 1–7 signals

, , ORCID Icon, , &
Pages 304-316 | Received 01 Apr 2022, Accepted 30 Oct 2022, Published online: 11 Nov 2022

References

  • Brown A, Kumar S, Tchounwou PB. Cisplatin-based chemotherapy of human cancers. J Cancer Sci Ther. 2019;11(4):97.
  • McWhinney SR, Goldberg RM, McLeod HL. Platinum neurotoxicity pharmacogenetics. Mol Cancer Ther. 2009;8(1):10–16.
  • Wolf S, Barton D, Kottschade L, et al. Chemotherapy-induced peripheral neuropathy: prevention and treatment strategies. Eur J Cancer. 2008;44(11):1507–1515.
  • Abdel-Wahab WM, Moussa FI. Neuroprotective effect of N-acetylcysteine against cisplatin-induced toxicity in rat brain by modulation of oxidative stress and inflammation. Drug Des Devel Ther. 2019;13:1155–1162.
  • Zakria M, Ahmad N, Al Kury LT, et al. Melatonin rescues the mice brain against cisplatin-induced neurodegeneration, an insight into antioxidant and anti-inflammatory effects. Neurotoxicology. 2021;87:1–10.
  • Vukovic R, Kumburovic I, Joksimovic Jovic J, et al. N-Acetylcysteine protects against the anxiogenic response to cisplatin in rats. Biomolecules. 2019;9(12):892.
  • Mollman JE. Cisplatin neurotoxicity. Mass Medical Soc. 1990;322:126–127.
  • Barabas K, Milner R, Lurie D, et al. Cisplatin: a review of toxicities and therapeutic applications. Vet Comp Oncol. 2008;6(1):1–18.
  • McDonald ES, Randon KR, Knight A, et al. Cisplatin preferentially binds to DNA in dorsal root ganglion neurons in vitro and in vivo: a potential mechanism for neurotoxicity. Neurobiol Dis. 2005;18(2):305–313.
  • Podratz JL, Lee H, Knorr P, et al. Cisplatin induces mitochondrial deficits in Drosophila larval segmental nerve. Neurobiol Dis. 2017;97(Pt A):60–69.
  • Zhang DD. Mechanistic studies of the Nrf2–Keap1 signaling pathway. Drug Metab Rev. 2006;38(4):769–789.
  • Djordjevic J, Djordjevic A, Adzic M, et al. Alterations in the Nrf2–Keap1 signaling pathway and its downstream target genes in rat brain under stress. Brain Res. 2015;1602:20–31.
  • Zhou YQ, Liu DQ, Chen SP, et al. PPARγ activation mitigates mechanical allodynia in paclitaxel-induced neuropathic pain via induction of Nrf2/HO-1 signaling pathway. Biomed Pharmacother. 2020;129:110356.
  • Martin HL, Mounsey RB, Mustafa S, et al. Pharmacological manipulation of peroxisome proliferator-activated receptor γ (PPARγ) reveals a role for anti-oxidant protection in a model of Parkinson’s disease. Exp Neurol. 2012;235(2):528–538.
  • Nogueiras R, Sabio G. Brain JNK and metabolic disease. Diabetologia. 2021;64(2):265–274.
  • Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell. 2000;103(2):239–252.
  • Zhang F, Yu J, Yang T, et al. A novel c-Jun N-terminal kinase (JNK) signaling complex involved in neuronal migration during brain development. J Biol Chem. 2016;291(22):11466–11475.
  • Yang H, Gu ZT, Maegele LL, et al. SIRT1 plays a neuroprotective role in traumatic brain injury in rats via inhibiting the p38 MAPK pathway. Acta Pharmacol Sin. 2017;38(2):168–181.
  • Khan RS, Dine K, Das Sarma J, et al. SIRT1 activating compounds reduce oxidative stress mediated neuronal loss in viral induced CNS demyelinating disease. Acta Neuropathol Commun. 2014;2:3.
  • Wu Y, Pang Y, Wei W, et al. Resveratrol protects retinal ganglion cell axons through regulation of the SIRT1–JNK pathway. Exp Eye Res. 2020;200:108249.
  • Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol. 2006;147(Suppl. 1):S232–S240.
  • Yang QQ, Zhou JW. Neuroinflammation in the central nervous system: symphony of glial cells. Glia. 2019;67(6):1017–1035.
  • Shi H, Hua X, Kong D, et al. Role of toll-like receptor mediated signaling in traumatic brain injury. Neuropharmacology. 2019;145(Pt B):259–267.
  • Licinio J, Prolo P, McCann SM, et al. Brain iNOS: current understanding and clinical implications. Mol Med Today. 1999;5(5):225–232.
  • Patel S, Rauf A, Khan H, et al. Renin–angiotensin–aldosterone (RAAS): the ubiquitous system for homeostasis and pathologies. Biomed Pharmacother. 2017;94:317–325.
  • Mascolo A, Sessa M, Scavone C, et al. New and old roles of the peripheral and brain renin–angiotensin–aldosterone system (RAAS): focus on cardiovascular and neurological diseases. Int J Cardiol. 2017;227:734–742.
  • Varshney V, Garabadu D. Ang (1–7)/mas receptor-axis activation promotes amyloid beta-induced altered mitochondrial bioenergetics in discrete brain regions of Alzheimer’s disease-like rats. Neuropeptides. 2021;86:102122.
  • Deeks ED, Scheen AJ. Canagliflozin: a review in type 2 diabetes. Drugs. 2017;77(14):1577–1592.
  • Hasan R, Lasker S, Hasan A, et al. Canagliflozin attenuates isoprenaline-induced cardiac oxidative stress by stimulating multiple antioxidant and anti-inflammatory signaling pathways. Sci Rep. 2020;10(1):14459.
  • Heerspink HJL, Perco P, Mulder S, et al. Canagliflozin reduces inflammation and fibrosis biomarkers: a potential mechanism of action for beneficial effects of SGLT2 inhibitors in diabetic kidney disease. Diabetologia. 2019;62(7):1154–1166.
  • Hasan R, Lasker S, Hasan A, et al. Canagliflozin ameliorates renal oxidative stress and inflammation by stimulating AMPK–Akt–eNOS pathway in the isoprenaline-induced oxidative stress model. Sci Rep. 2020;10(1):14659.
  • Wang XC, Zhong W, Lei J, et al. Canagliflozin exerts anti-inflammatory effects by inhibiting intracellular glucose metabolism and promoting autophagy in immune cells. Biochem Pharmacol. 2018;152:45–59.
  • Watanabe Y, Nakayama K, Taniuchi N, et al. Beneficial effects of canagliflozin in combination with pioglitazone on insulin sensitivity in rodent models of obese type 2 diabetes. PLOS One. 2015;10(1):e0116851.
  • Ali BH, Al Salam S, Al Suleimani Y, et al. Effects of the SGLT-2 inhibitor canagliflozin on adenine-induced chronic kidney disease in rats. Cell Physiol Biochem. 2019;52(1):27–39.
  • Aydin D, Peker EG, Karakurt MD, et al. Effects of ginkgo biloba extract on brain oxidative condition after cisplatin exposure. Clin Invest Med. 2016;39(6):27511.
  • van den Buuse M, de Jong W. Differential effects of dopaminergic drugs on open-field behavior of spontaneously hypertensive rats and normotensive Wistar-Kyoto rats. J Pharmacol Exp Ther. 1989;248(3):1189–1196.
  • Cryan JF, Valentino RJ, Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev. 2005;29(4–5):547–569.
  • Bancroft JD, Gamble M. Theory and practice of histological techniques. USA: Elsevier Health Sciences; 2008.
  • Montgomery H, Dymock JFJA. Determination of nitrite in water. Cambridge: Royal Society of Chemistry; 1961. p. 414.
  • Krawisz J, Sharon P, Stenson WJG. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity: assessment of inflammation in rat and hamster models. Gastroenterology. 1984;87(6):1344–1350.
  • Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82(1):70–77.
  • Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978;86(1):271–278.
  • Marklund SL. Superoxide dismutase isoenzymes in tissues and plasma from New Zealand black mice, nude mice and normal BALB/c mice. Mutat Res. 1985;148(1–2):129–134.
  • Keen JH, Habig WH, Jakoby WB. Mechanism for the several activities of the glutathione S-transferases. J Biol Chem. 1976;251(20):6183–6188.
  • Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun. 1976;71(4):952–958.
  • Sinha AK. Colorimetric assay of catalase. Anal Biochem. 1972;47(2):389–394.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods. 2001;25(4):402–408.
  • Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem. 1976;72:248–254.
  • Cersosimo RJ. Cisplatin neurotoxicity. Cancer Treat Rev. 1989;16(4):195–211.
  • Jaggi AS, Singh N. Mechanisms in cancer-chemotherapeutic drugs-induced peripheral neuropathy. Toxicology. 2012;291(1–3):1–9.
  • Abdelkader NF, Saad MA, Abdelsalam RM. Neuroprotective effect of nebivolol against cisplatin-associated depressive-like behavior in rats. J Neurochem. 2017;141(3):449–460.
  • Kandeil MA, Gomaa SB, Mahmoud MO. The effect of some natural antioxidants against cisplatin-induced neurotoxicity in rats: behavioral testing. Heliyon. 2020;6(8):e04708.
  • Karavelioglu E, Boyaci MG, Simsek N, et al. Selenium protects cerebral cells by cisplatin induced neurotoxicity. Acta Cir Bras. 2015;30(6):394–400.
  • Yoo KH, Tang JJ, Rashid MA, et al. Nicotinamide mononucleotide prevents cisplatin-induced cognitive impairments. Cancer Res. 2021;81(13):3727–3737.
  • Boukelmoune N, Chiu GS, Kavelaars A, et al. Mitochondrial transfer from mesenchymal stem cells to neural stem cells protects against the neurotoxic effects of cisplatin. Acta Neuropathol Commun. 2018;6(1):139.
  • Chiu GS, Maj MA, Rizvi S, et al. Pifithrin-μ prevents cisplatin-induced chemobrain by preserving neuronal mitochondrial function. Cancer Res. 2017;77(3):742–752.
  • Khasabova IA, Khasabov SG, Olson JK, et al. Pioglitazone, a PPARγ agonist, reduces cisplatin-evoked neuropathic pain by protecting against oxidative stress. Pain. 2019;160(3):688–701.
  • Krönke G, Kadl A, Ikonomu E, et al. Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors. Arterioscler Thromb Vasc Biol. 2007;27(6):1276–1282.
  • Chong ZZ, Shang YC, Wang S, et al. SIRT1: new avenues of discovery for disorders of oxidative stress. Expert Opin Ther Targets. 2012;16(2):167–178.
  • Ali FEM, Hassanein EHM, El-Bahrawy AH, et al. Nephroprotective effect of umbelliferone against cisplatin-induced kidney damage is mediated by regulation of NRF2, cytoglobin, SIRT1/FOXO-3, and NF- kB-p65 signaling pathways. J Biochem Mol Toxicol. 2021;35(5):e22738.
  • Yang X, Liu Q, Li Y, et al. The diabetes medication canagliflozin promotes mitochondrial remodelling of adipocyte via the AMPK–Sirt1–Pgc-1α signalling pathway. Adipocyte. 2020;9(1):484–494.
  • Umino H, Hasegawa K, Minakuchi H, et al. High basolateral glucose increases sodium-glucose cotransporter 2 and reduces sirtuin-1 in renal tubules through glucose transporter-2 detection. Sci Rep. 2018;8(1):6791.
  • Song Z, Zhu J, Wei Q, et al. Canagliflozin reduces cisplatin uptake and activates Akt to protect against cisplatin-induced nephrotoxicity. Am J Physiol Renal Physiol. 2020;318(4):F1041–F1052.
  • Sayed AM, Hassanein EHM, Ali FEM, et al. Regulation of keap-1/Nrf2/AKT and iNOS/NF-κB/TLR4 signals by apocynin abrogated methotrexate-induced testicular toxicity: mechanistic insights and computational pharmacological analysis. Life Sci. 2021;284:119911.
  • Nijboer CH, van der Kooij MA, van Bel F, et al. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic-ischemic brain injury. Brain Behav Immun. 2010;24(5):812–821.
  • Vukic V, Callaghan D, Walker D, et al. Expression of inflammatory genes induced by beta-amyloid peptides in human brain endothelial cells and in Alzheimer’s brain is mediated by the JNK–AP1 signaling pathway. Neurobiol Dis. 2009;34(1):95–106.
  • Antonyak MA, Kenyon LC, Godwin AK, et al. Elevated JNK activation contributes to the pathogenesis of human brain tumors. Oncogene. 2002;21(33):5038–5046.
  • Nunes-Silva A, Rocha GC, Magalhaes DM, et al. Physical exercise and ACE2–angiotensin-(1–7)–Mas receptor axis of the renin angiotensin system. Protein Pept Lett. 2017;24(9):809–816.
  • Santos RAS, Sampaio WO, Alzamora AC, et al. The ACE2/angiotensin-(1–7)/MAS axis of the renin–angiotensin system: focus on angiotensin-(1–7). Physiol Rev. 2018;98(1):505–553.
  • Okui S, Yamamoto H, Li W, et al. Cisplatin-induced acute renal failure in mice is mediated by chymase-activated angiotensin–aldosterone system and interleukin-18. Eur J Pharmacol. 2012;685(1–3):149–155.
  • Zhang J, Rudemiller NP, Patel MB, et al. Competing actions of type 1 angiotensin II receptors expressed on T lymphocytes and kidney epithelium during cisplatin-induced AKI. J Am Soc Nephrol. 2016;27(8):2257–2264.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.