Tannic Acid Attenuates Peripheral and Brain Changes in a Preclinical Rat Model of Glioblastoma by Modulating Oxidative Stress and Purinergic Signaling.
Adenosine
/ pharmacology
Adenosine Diphosphate
/ metabolism
Adenosine Monophosphate
/ pharmacology
Adenosine Triphosphate
/ metabolism
Animals
Antioxidants
/ pharmacology
Brain
/ metabolism
Glioblastoma
/ drug therapy
Nitrites
Oxidative Stress
Rats
Reactive Oxygen Species
Superoxide Dismutase
Tannins
/ pharmacology
Thiobarbituric Acid Reactive Substances
Cancer
Ectoenzymes
Glioma
Polyphenols
Redox status
Tannin
Journal
Neurochemical research
ISSN: 1573-6903
Titre abrégé: Neurochem Res
Pays: United States
ID NLM: 7613461
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
11
10
2021
accepted:
02
02
2022
revised:
18
01
2022
pubmed:
19
2
2022
medline:
25
5
2022
entrez:
18
2
2022
Statut:
ppublish
Résumé
Glioblastoma (GB) is a highly aggressive and invasive brain tumor; its treatment remains palliative. Tannic acid (TA) is a polyphenol widely found in foods and possesses antitumor and neuroprotective activities. This study aimed to investigate the effect of TA on oxidative stress parameters and the activity of ectonucleotidases in the serum, platelets, and lymphocytes and/or in the brain of rats with preclinical GB. Rats with GB were treated intragastrically with TA (50 mg/kg/day) for 15 days or with a vehicle. In the platelets of the animals with glioma, the adenosine triphosphate (ATP) and adenosine monophosphate (AMP) hydrolysis and the catalase (CAT) activity decreased. Besides, the adenosine diphosphate (ADP) hydrolysis, adenosine (Ado) deamination, and the reactive oxygen species (ROS) and nitrite levels were increased in glioma animals; however, TA reversed ROS and nitrite levels and AMP hydrolysis alterations. In lymphocytes from animals with glioma, the ATP and ADP hydrolysis, as well as Ado deamination were increased; TA treatment countered this increase. In the brain of the animals with glioma, the ROS, nitrite, and thiobarbituric acid reactive substance (TBARS) levels increased and the thiol (SH) levels and CAT and superoxide dismutase (SOD) activities were decreased; TA treatment decreased the ROS and TBARS levels and restored the SOD activity. In the serum of the animals with glioma, the ATP hydrolysis decreased; TA treatment restored this parameter. Additionally, the ROS levels increased and the SH and SOD activity decreased by glioma implant; TA treatment enhanced nitrite levels and reversed SOD activity. Altogether, our results suggest that TA is an important target in the treatment of GB, as it modulates purinergic and redox systems.
Identifiants
pubmed: 35178643
doi: 10.1007/s11064-022-03547-7
pii: 10.1007/s11064-022-03547-7
doi:
Substances chimiques
Antioxidants
0
Nitrites
0
Reactive Oxygen Species
0
Tannins
0
Thiobarbituric Acid Reactive Substances
0
Adenosine Monophosphate
415SHH325A
Adenosine Diphosphate
61D2G4IYVH
Adenosine Triphosphate
8L70Q75FXE
Superoxide Dismutase
EC 1.15.1.1
Adenosine
K72T3FS567
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1541-1552Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Tan AC, Ashley DM, López GY, Malinzak M, Friedman HS, Khasraw M (2020) Management of glioblastoma: state of the art and future directions. CA Cancer J Clin 70(4):299–312. https://doi.org/10.3322/caac.21613
doi: 10.3322/caac.21613
pubmed: 32478924
Pande A, Rajaraman N, Sadiya N, Patil S, Pandian S, Adhithyan R, Rajendran B, Jalali R, Ghosh S (2020) Spinal drop metastasis of glioblastoma-two case reports, clinicopathologic features, current modalities of evaluation, and treatment with a review of the literature. World Neurosurg 146:261–269. https://doi.org/10.1016/j.wneu.2020.10.023
doi: 10.1016/j.wneu.2020.10.023
pubmed: 33161132
Ou A, Yung WKA, Majd N (2020) Molecular mechanisms of treatment resistance in glioblastoma. Int J Mol Sci 22(1):351. https://doi.org/10.3390/ijms22010351
doi: 10.3390/ijms22010351
pmcid: 7794986
Olivier C, Oliver L, Lalier L, Vallette FM (2021) Drug resistance in glioblastoma: the two faces of oxidative stress. Front Mol Biosci 7:620677. https://doi.org/10.3389/fmolb.2020.620677
doi: 10.3389/fmolb.2020.620677
pubmed: 33585565
pmcid: 7873048
Pietrobono D, Giacomelli C, Marchetti L, Martini C, Trincavelli ML (2020) High adenosine extracellular levels induce glioblastoma aggressive traits modulating the mesenchymal stromal cell secretome. Int J Mol Sci 21(20):7706. https://doi.org/10.3390/ijms21207706
doi: 10.3390/ijms21207706
pmcid: 7589183
Azambuja JH, Gelsleichter NE, Beckenkamp LR, Iser IC, Fernandes MC, Figueiró F, Battastini AMO, Scholl JN, de Oliveira FH, Spanevello RM, Sévigny J, Wink MR, Stefani MA, Teixeira HF, Braganhol E (2019) CD73 downregulation decreases in vitro and in vivo glioblastoma growth. Mol Neurobiol 56(5):3260–3279. https://doi.org/10.1007/s12035-018-1240-4
doi: 10.1007/s12035-018-1240-4
pubmed: 30117104
Zhou Y, Wang L, Wang C, Wu Y, Chen D, Lee TH (2020) Potential implications of hydrogen peroxide in the pathogenesis and therapeutic strategies of gliomas. Arch Pharm Res 43(2):187–203. https://doi.org/10.1007/s12272-020-01205-6
doi: 10.1007/s12272-020-01205-6
pubmed: 31956964
Idzko M, Ferrari D, Eltzsching HK (2014) Nucleotide signaling during inflammation. Nature 15:310–317. https://doi.org/10.1038/nature13085
doi: 10.1038/nature13085
Di Virgilio F, Adinolfi E (2017) Extracellular purines, purinergic receptors and tumor growth. Oncogene 36:293–303. https://doi.org/10.1038/onc.2016.206
doi: 10.1038/onc.2016.206
pubmed: 27321181
Zimmermann H, Zebisch M, Sträter N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8(1):105–106. https://doi.org/10.1007/s11302-011-9256-5
doi: 10.1007/s11302-011-9256-5
pubmed: 22002166
Linhares P, Carvalho B, Vaz R, Costa BM (2020) Glioblastoma: is there any blood biomarker with true clinical relevance? Int J Mol Sci 21(16):5809. https://doi.org/10.3390/ijms21165809
doi: 10.3390/ijms21165809
pmcid: 7461098
Muir M, Gopakumar S, Traylor J, Lee S, Rao G (2020) Glioblastoma multiforme: novel therapeutic targets. Expert Opin Ther Targets 24(7):605–614. https://doi.org/10.1080/14728222.2020.1762568
doi: 10.1080/14728222.2020.1762568
pubmed: 32394767
Deng LJ, Qi M, Li N, Lei YH, Zhang DM, Chen JX (2020) Natural products and their derivatives: promising modulators of tumor immunotherapy. J Leukoc Biol 108(2):493–508. https://doi.org/10.1002/JLB.3MR0320-444R
doi: 10.1002/JLB.3MR0320-444R
pubmed: 32678943
Talib WH, Alsalahat I, Daoud S, Abutayeh RF, Mahmod AI (2020) Plant-derived natural products in cancer research: extraction, mechanism of action, and drug formulation. Molecules 25(22):5319. https://doi.org/10.3390/molecules25225319
doi: 10.3390/molecules25225319
pmcid: 7696819
Li H, Krstin S, Wink M (2018) Modulation of multidrug resistant in cancer cells by EGCG, tannic acid and curcumin. Phytomedicine 50:213–222. https://doi.org/10.1016/j.phymed.2018.09.169
doi: 10.1016/j.phymed.2018.09.169
pubmed: 30466981
Bona NP, Pedra NS, Azambuja JH, Soares MSP, Spohr L, Gelsleichter NE, de Meine MB, Sekine FG, Mendonça LT, de Oliveira FH, Braganhol E, Spanevello RM, da Silveira EF, Stefanello FM (2020) Tannic acid elicits selective antitumoral activity in vitro and inhibits cancer cell growth in a preclinical model of glioblastoma multiforme. Metab Brain Dis 35(2):283–293. https://doi.org/10.1007/s11011-019-00519-9
doi: 10.1007/s11011-019-00519-9
pubmed: 31773434
Nagesh PKB, Chowdhury P, Hatami E, Jain S, Dan N, Kashyap VK, Chauhan SC, Jaggi M, Yallapu MM (2020) Tannic acid inhibits lipid metabolism and induce ROS in prostate cancer cells. Sci Rep 10(1):980. https://doi.org/10.1038/s41598-020-57932-9
doi: 10.1038/s41598-020-57932-9
pubmed: 31969643
pmcid: 6976712
Zhang J, Chen D, Han DM, Cheng YH, Dai C, Wu XJ, Che FY, Heng XY (2018) Tannic acid mediated induction of apoptosis in human glioma Hs 683 cells. Oncol Lett 15(5):6845–6850. https://doi.org/10.3892/ol.2018.8197
doi: 10.3892/ol.2018.8197
pubmed: 29849785
pmcid: 5962853
Gerzson MFB, Pacheco SM, Soares MSP, Bona NP, Oliveira PS, Azambuja JH, da Costa P, Gutierres JM, Carvalho FB, Morsch VM, Spanevello RM, Stefanello FM (2019) Effects of tannic acid in streptozotocin-induced sporadic Alzheimer’s disease: insights into memory, redox status, Na
doi: 10.1080/13813455.2019.1673430
pubmed: 31595805
Gerzson MFB, Bona NP, Soares MSP, Teixeira FC, Rahmeier FL, Carvalho FB, da Cruz FM, Onzi G, Lenz G, Gonçales RA, Spanevello RM, Stefanello FM (2020) Tannic acid ameliorates STZ-induced Alzheimer’s disease-like impairment of memory, neuroinflammation, neuronal death and modulates Akt expression. Neurotox Res 37:1009–1017. https://doi.org/10.1007/s12640-020-00167-3
doi: 10.1007/s12640-020-00167-3
pubmed: 31997154
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
doi: 10.1016/0003-2697(76)90527-3
pubmed: 942051
Böyum A (1968) Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Investig 97:77–89
Jaques JA, Peres JRR, Ruchel JB, Gutierres J, Bairros AV, Gomes ILF, Almeida SCL, Mello CDB, Chitolina MRS, Morsch VM, Leal DB (2011) A method for isolation of rat lymphocyte-rich mononuclear cells from lung tissue useful for determination of nucleoside triphosphate diphosphohydrolase activity. Anal Biochem 410:34–39. https://doi.org/10.1016/j.ab.2010.10.039
doi: 10.1016/j.ab.2010.10.039
pubmed: 21059335
Lunkes GIL, Lunkes DS, Morsch VM et al (2004) NTPDase and 5′- nucleotidase activities in rats with alloxan-induced diabetes. Diabetes Res Clin Pract 65:1–6. https://doi.org/10.1016/j.diabres.2003.11.016
doi: 10.1016/j.diabres.2003.11.016
pubmed: 15163471
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
doi: 10.1016/S0021-9258(19)52451-6
Fürstenau CR, Trentin DS, Gossenheimer AN et al (2008) Ectonucleotidase activities are altered in serum and platelets of L-NAME-treated rats. Blood Cells Mol Dis 41:223–229. https://doi.org/10.1016/j.bcmd.2008.04.009
doi: 10.1016/j.bcmd.2008.04.009
pubmed: 18559295
Chan K, Delfert D, Junger KD (1986) A direct colorimetric assay for Ca
doi: 10.1016/0003-2697(86)90640-8
pubmed: 2946250
Leal DB, Streher CA, Neu TN, Bittencourt FP, Leal CA, da Silva JE, Morsch VM, Schetinger MR (2005) Characterization of NTPDase (NTPDase 1: ectoapyrase; ectodiphosphohydrolase; CD39; E.C. 3.6.1.5) activity in human lymphocytes. Biochim Biophys Acta 1721:9–11. https://doi.org/10.1016/j.bbagen.2004.09.006
doi: 10.1016/j.bbagen.2004.09.006
pubmed: 15652174
Pilla C, Emanuelli T, Frassetto SS, Battastini AMO, Dias RD, Sarkis JJF (1996) ATP diphosphohydrolase activity (apyrase E.C. 3.6.1.5) in human blood platelets. Platelets 7:225–230. https://doi.org/10.3109/09537109609023582
doi: 10.3109/09537109609023582
pubmed: 21043691
Giusti G, Galanti B (1984) Colorimetric method. Adenosine deaminase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 3rd edn. Wiley, Weinheim, pp 315–3233
Ali SF, LeBel CP, Bondy SC (1992) Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13:637–648
pubmed: 1475065
Stuehr DJ, Nathan CF (1989) Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med 169:1543–1555. https://doi.org/10.1084/jem.169.5.1543
doi: 10.1084/jem.169.5.1543
pubmed: 2497225
Aksenov MY, Markesbery WR (2001) Changes in thiol content and expression of glutathione redox system genes in the hippocampus and cerebellum in Alzheimer’s disease. Neurosci Lett 302:141–145. https://doi.org/10.1016/S0304-3940(01)01636-6
doi: 10.1016/S0304-3940(01)01636-6
pubmed: 11290407
Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421. https://doi.org/10.1016/0076-6879(90)86134-H
doi: 10.1016/0076-6879(90)86134-H
pubmed: 2233308
Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175
doi: 10.1016/S0021-9258(19)45228-9
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
doi: 10.1016/S0076-6879(84)05016-3
pubmed: 6727660
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
doi: 10.1016/S0021-9258(19)42083-8
Marx S, Splittstöhser M, Kinnen F, Moritz E, Joseph C, Paul S, Paland H, Seifert C, Marx M, Böhm A, Schwedhelm E, Holzer K, Singer S, Ritter CA, Bien-Möller S, Schroeder HWS, Rauch BH (2018) Platelet activation parameters and platelet-leucocyte-conjugate formation in glioblastoma multiforme patients. Oncotarget 9(40):25860–25876. https://doi.org/10.18632/oncotarget.25395
doi: 10.18632/oncotarget.25395
pubmed: 29899827
pmcid: 5995223
Yersal Ö, Odabaşi E, Özdemir Ö, Kemal Y (2018) Prognostic significance of pre-treatment neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio in patients with glioblastoma. Mol Clin Oncol 9(4):453–458. https://doi.org/10.3892/mco.2018.1695
doi: 10.3892/mco.2018.1695
pubmed: 30233797
pmcid: 6142303
Sol N, In’t Veld SGJG, Vancura A, Tjerkstra M, Leurs C, Rustenburg F, Schellen P, Verschueren H, Post E, Zwaan K, Ramaker J, Wedekind LE, Tannous J, Ylstra B, Killestein J, Mateen F, Idema S, de Witt Hamer PC, Navis AC, Leenders WPJ, Hoeben A, Moraal B, Noske DP, Vandertop WP, Nilsson RJA, Tannous BA, Wesseling P, Reijneveld JC, Best MG, Wurdinger T (2020) Tumor-educated platelet RNA for the detection and (pseudo)progression monitoring of glioblastoma. Cell Rep Med 1(7):100101. https://doi.org/10.1016/j.xcrm.2020.100101
doi: 10.1016/j.xcrm.2020.100101
pubmed: 33103128
pmcid: 7576690
Gachet C, Hechler B (2020) Platelet purinergic receptors in thrombosis and inflammation. Hamostaseologie. https://doi.org/10.1055/a-1113-0711
doi: 10.1055/a-1113-0711
pubmed: 32464678
Atkinson B, Dwyer K, Enjyoji K, Robson SC (2006) Ecto-nucleotidases of the CD39/NTPDase family modulate platelet activation and thrombus formation: potential as therapeutic targets. Blood Cells Mol Dis 36(2):217–222. https://doi.org/10.1016/j.bcmd.2005.12.025
doi: 10.1016/j.bcmd.2005.12.025
pubmed: 16476557
Marx S, Xiao Y, Baschin M, Splittstöhser M, Altmann R, Moritz E, Jedlitschky G, Bien-Möller S, Schroeder HWS, Rauch BH (2019) The role of platelets in cancer pathophysiology: focus on malignant glioma. Cancers (Basel) 11(4):569. https://doi.org/10.3390/cancers11040569
doi: 10.3390/cancers11040569
Campanella R, Guarnaccia L, Cordiglieri C, Trombetta E, Caroli M, Carrabba G, La Verde N, Rampini P, Gaudino C, Costa A, Luzzi S, Mantovani G, Locatelli M, Riboni L, Navone SE, Marfia G (2020) Tumor-educated platelets and angiogenesis in glioblastoma: another brick in the wall for novel prognostic and targetable biomarkers, changing the vision from a localized tumor to a systemic pathology. Cells 9(2):294. https://doi.org/10.3390/cells9020294
doi: 10.3390/cells9020294
pmcid: 7072723
Berghoff AS, Kiesel B, Widhalm G, Rajky O, Ricken G, Wöhrer A, Dieckmann K, Filipits M, Brandstetter A, Weller M, Kurscheid S, Hegi ME, Zielinski CC, Marosi C, Hainfellner JA, Preusser M, Wick W (2015) Programmed death ligand 1 expression and tumor-infiltrating lymphocytes in glioblastoma. Neuro Oncol 17(8):1064–1075. https://doi.org/10.1093/neuonc/nou307
doi: 10.1093/neuonc/nou307
pubmed: 25355681
Stagg J, Smyth MJ (2010) Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29(39):5346–5358. https://doi.org/10.1038/onc.2010.292onc2010292
doi: 10.1038/onc.2010.292onc2010292
pubmed: 20661219
Drill M, Powell KL, Kan LK, Jones NC, O’Brien TJ, Hamilton JA, Monif M (2020) Inhibition of purinergic P2X receptor 7 (P2X7R) decreases granulocyte-macrophage colony-stimulating factor (GM-CSF) expression in U251 glioblastoma cells. Sci Rep 10(1):14844. https://doi.org/10.1038/s41598-020-71887-x
doi: 10.1038/s41598-020-71887-x
pubmed: 32908225
pmcid: 7481200
Ledur PF, Villodre ES, Paulus R, Cruz LA, Flores DG, Lenz G (2012) Extracellular ATP reduces tumor sphere growth and cancer stem cell population in glioblastoma cells. Purinergic Signal 8(1):39–48. https://doi.org/10.1007/s11302-011-9252-9
doi: 10.1007/s11302-011-9252-9
pubmed: 21818572
Nie F, Liang Y, Jiang B, Li X, Xun H, He W, Lau HT, Ma X (2016) Apoptotic effect of tannic acid on fatty acid synthase over-expressed human breast cancer cells. Tumour Biol 37(2):2137–2143. https://doi.org/10.1007/s13277-015-4020-z
doi: 10.1007/s13277-015-4020-z
pubmed: 26349913
Nagesh PKB, Hatami E, Chowdhury P, Kashyap VK, Khan S, Hafeez BB, Chauhan SC, Jaggi M, Yallapu MM (2018) Tannic acid induces endoplasmic reticulum stress-mediated apoptosis in prostate cancer. Cancers (Basel) 10(3):68. https://doi.org/10.3390/cancers10030068
doi: 10.3390/cancers10030068
pmcid: 5876643
Mhlanga P, Perumal PO, Somboro AM, Amoako DG, Khumalo HM, Khan RB (2019) Mechanistic insights into oxidative stress and apoptosis mediated by tannic acid in human liver hepatocellular carcinoma cells. Int J Mol Sci 20(24):6145. https://doi.org/10.3390/ijms20246145
doi: 10.3390/ijms20246145
pmcid: 6940809
Sp N, Kang DY, Jo ES, Rugamba A, Kim WS, Park YM, Hwang DY, Yoo JS, Liu Q, Jang KJ, Yang YM (2020) Tannic acid promotes TRAIL-induced extrinsic apoptosis by regulating mitochondrial ROS in human embryonic carcinoma cells. Cells 9(2):282. https://doi.org/10.3390/cells9020282
doi: 10.3390/cells9020282
pmcid: 7072125
Vavaev AV, Buryachkovskaya LI, Uchitel IA, Tishchenko EG, Maksimenko AV (2012) Effect of hydrogen peroxide and catalase derivatives on functional activity of platelets. Bull Exp Biol Med 152:307–312. https://doi.org/10.1007/s10517-012-1515-0
doi: 10.1007/s10517-012-1515-0
pubmed: 22803073
Kim DA, Choi HS, Ryu ES, Ko J, Shin HS, Lee JM, Chung H, Jun E, Oh ES, Kang DH (2019) Tannic acid attenuates the formation of cancer stem cells by inhibiting NF-κB-mediated phenotype transition of breast cancer cells. Am J Cancer Res 9(8):1664–1681
pubmed: 31497349
pmcid: 6726983
Darvin P, Joung YH, Kang DY, Sp N, Byun HJ, Hwang TS, Sasidharakurup H, Lee CH, Cho KH, Park KD, Lee HK, Yang YM (2017) Tannic acid inhibits EGFR/STAT1/3 and enhances p38/STAT1 signalling axis in breast cancer cells. J Cell Mol Med 21(4):720–734. https://doi.org/10.1111/jcmm.13015
doi: 10.1111/jcmm.13015
pubmed: 27862996