Generic placeholder image

Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Research Article

Ethanolic Extract of Artemisia herba-alba Ameliorates Hyperinsulinemia and Hyperglycemia-Induced HepG2 Cells Through Cell Survival Promotion, Oxidative Stress Mitigation, and Insulin Signaling Restoration

Author(s): Yasmina Bourebaba*, Malwina Mularczyk, Katarzyna Kornicka-Garbowska, Krzysztof Marycz, Lynda Bourebaba and Anna Kowalczuk*

Volume 19, Issue 6, 2023

Published on: 02 March, 2023

Article ID: e200123212933 Pages: 17

DOI: 10.2174/1573407219666230120103107

Price: $65

Abstract

Background: In recent years, diabetes and its risk factors were linked to an augmented occurrence of cardiovascular diseases (CVD), which are considered major causes of morbidity and mortality in diabetes mellitus subjects. Hyperinsulinemia (HI) and hyperglycemia (HG) are recognized as insulin resistance-inducers, which can trigger several alterations in cellular biogenesis besides inflammatory signaling activation. As a folk medicine in many countries, Artemisia herbaalba has been preclinically studied for treatment of type 2 diabetes mellitus (T2DM) and showed beneficial effects on hyperglycemia.

Methods: In the current work, we explored the potential mechanisms underlying the antihyperglycemic behavior of the ethanolic extract of A. herba-alba and its bioactive compounds.

Results: Obtained data demonstrated that ethanolic extract of A. herba-alba enhances HepG2 viability and proliferation, decreases considerably the apoptosis, through the regulation of pro- and anti-apoptotic pathways implying p53, p21 and Bcl-2 genes expression and Pan caspases activation under IR concentration at the lowest concentrations. A. herba-alba extract treatment additionally exhibited a potential antioxidant effect, evidenced by the significant decrease in total intracellular reactive oxygen species (ROS) levels and the improved mitochondrial transmembrane potential in HG/HI-challenged HepG2 cells (p < 0.001). Furthermore, A. herba-alba positively upregulated Irs1 and Irs2 as well as Akt/Pi3K pathway compared to insulin-resistant untreated cells, and subsequently stimulated glucose uptake in response to insulin infusion, as a consequence of its signal transduction restoration.

Conclusion: Overall, the obtained data highlighted the beneficial effects of A. herba-alba ethanolic extract in ameliorating insulin signaling and liver cells metabolic balance, and shed the light for its use as a promising and safe therapeutic lead for the management of type 2 diabetes and underlying metabolic failures.

Keywords: Artemisia herba-alba, insulin resistance, hyperglycemia, hyperinsulinemia, glucose uptake, oxidative stress.

Graphical Abstract
[1]
Glaser, B. Type 2 diabetes: hypoinsulinism, hyperinsulinism, or both? PLoS Med., 2007, 4(4)e148
[http://dx.doi.org/10.1371/journal.pmed.0040148] [PMID: 17407388]
[2]
Zimmet, P.; Alberti, K.G.M.M.; Shaw, J. Global and societal implications of the diabetes epidemic. Nature, 2001, 414(6865), 782-787.
[http://dx.doi.org/10.1038/414782a] [PMID: 11742409]
[3]
Ehrmann, B. J. Diabetes. A Comprehensive Guide to Geriatric Rehabilitation; Elsevier, 2014, pp. 329-336.
[http://dx.doi.org/10.1016/B978-0-7020-4588-2.00046-2]
[4]
Muoio, D.M.; Newgard, C.B. Molecular and metabolic mechanisms of insulin resistance and β-cell failure in type 2 diabetes. Nat. Rev. Mol. Cell Biol., 2008, 9(3), 193-205.
[http://dx.doi.org/10.1038/nrm2327] [PMID: 18200017]
[5]
Zheng, X.; Li, Y.; Zhang, L.; Feng, W.; Zhang, X. Antihyperglycemic activity of Selaginella tamariscina (Beauv.) Spring. J. Ethnopharmacol., 2011, 133(2), 531-537.
[http://dx.doi.org/10.1016/j.jep.2010.10.028] [PMID: 20969941]
[6]
Kawahito, S.; Kitahata, H.; Oshita, S. Problems associated with glucose toxicity: Role of hyperglycemia-induced oxidative stress. World J. Gastroenterol., 2009, 15(33), 4137-4142.
[http://dx.doi.org/10.3748/wjg.15.4137] [PMID: 19725147]
[7]
Ormazabal, V.; Nair, S.; Elfeky, O.; Aguayo, C.; Salomon, C.; Zuñiga, F.A. Association between insulin resistance and the development of cardiovascular disease. Cardiovasc. Diabetol., 2018, 17(1), 122.
[http://dx.doi.org/10.1186/s12933-018-0762-4] [PMID: 30170598]
[8]
Tomás, E.; Lin, Y.S.; Dagher, Z.; Saha, A.; Luo, Z.; Ido, Y.; Ruderman, N.B. Hyperglycemia and insulin resistance: possible mechanisms. Ann. N. Y. Acad. Sci., 2002, 967(1), 43-51.
[http://dx.doi.org/10.1111/j.1749-6632.2002.tb04262.x] [PMID: 12079834]
[9]
Maciejczyk, M.; Żebrowska, E.; Chabowski, A. Insulin resistance and oxidative stress in the brain: What’s new? Int. J. Mol. Sci., 2019, 20(4), 874.
[http://dx.doi.org/10.3390/ijms20040874] [PMID: 30781611]
[10]
Deshpande, M.C.; Venkateswarlu, V.; Babu, R.K.; Trivedi, R.K. Design and evaluation of oral bioadhesive controlled release formulations of miglitol, intended for prolonged inhibition of intestinal α-glucosidases and enhancement of plasma glucagon like peptide-1 levels. Int. J. Pharm., 2009, 380(1-2), 16-24.
[http://dx.doi.org/10.1016/j.ijpharm.2009.06.024] [PMID: 19563873]
[11]
Vaidyula, V.R.; Rao, A.K.; Mozzoli, M.; Homko, C.; Cheung, P.; Boden, G. Effects of hyperglycemia and hyperinsulinemia on circulating tissue factor procoagulant activity and platelet CD40 ligand. Diabetes, 2006, 55(1), 202-208.
[http://dx.doi.org/10.2337/diabetes.55.01.06.db05-1026] [PMID: 16380494]
[12]
Haller, H.; Drab, M.; Luft, F.C. The role of hyperglycemia and hyperinsulinemia in the pathogenesis of diabetic angiopathy. Clin. Nephrol., 1996, 46(4), 246-255.
[PMID: 8905209]
[13]
Ahmad, Z.A.; Abdul-hussian, B.A. Effect of Artemisia herb on induced hyperglycemia in wistar rats. QJVMS, 2016, 15, 7.
[14]
Lee, Y.; Fluckey, J.D.; Chakraborty, S.; Muthuchamy, M. Hyperglycemia‐ and hyperinsulinemia‐induced insulin resistance causes alterations in cellular bioenergetics and activation of inflammatory signaling in lymphatic muscle. FASEB J., 2017, 31(7), 2744-2759.
[http://dx.doi.org/10.1096/fj.201600887R] [PMID: 28298335]
[15]
Valenzuela, R.; Videla, L.A. Crosstalk mechanisms in hepatoprotection: Thyroid hormone-docosahexaenoic acid (DHA) and DHA-extra virgin olive oil combined protocols. Pharmacol. Res., 2018, 132, 168-175.
[http://dx.doi.org/10.1016/j.phrs.2017.12.013] [PMID: 29253525]
[16]
Valenzuela, R.; Videla, L.A. Impact of the co-administration of N-3 fatty acids and olive oil components in preclinical nonalcoholic fatty liver disease models: A mechanistic view. Nutrients, 2020, 12(2), 499.
[http://dx.doi.org/10.3390/nu12020499] [PMID: 32075238]
[17]
Pari, L.; Umamaheswari, J. Antihyperglycaemic activity of Musa sapientum flowers: effect on lipid peroxidation in alloxan diabetic rats. Phytother. Res., 2000, 14(2), 136-138.
[http://dx.doi.org/10.1002/(SICI)1099-1573(200003)14:2<136:AID-PTR607>3.0.CO;2-K] [PMID: 10685115]
[18]
Venkatesh, S.; Reddy, G.D.; Reddy, B.M.; Ramesh, M.; Rao, A.V.N.A. Antihyperglycemic activity of Caralluma attenuata. Fitoterapia, 2003, 74(3), 274-279.
[http://dx.doi.org/10.1016/S0367-326X(03)00021-2] [PMID: 12727493]
[19]
Al-Khazraji, S.M.; Al-Shamaony, L.A.; Twaij, H.A.A. Hypoglycaemic effect of Artemisia herba-alba. I. Effect of different parts and influence of the solvent on hypoglycaemic activity. J. Ethnopharmacol., 1993, 40(3), 163-166.
[http://dx.doi.org/10.1016/0378-8741(93)90064-C] [PMID: 8145571]
[20]
Réggami, Y.; Benkhaled, A.; Boudjelal, A.; Berredjem, H.; Amamra, A.; Benyettou, H.; Larabi, N.; Senator, A.; Siracusa, L.; Ruberto, G. Artemisia herba-alba aqueous extract improves insulin sensitivity and hepatic steatosis in rodent model of fructose-induced metabolic syndrome. Arch. Physiol. Biochem., 2021, 127(6), 541-550.
[21]
Harlev, E.; Nevo, E.; Mirsky, N.; Ofir, R. Antidiabetic attributes of desert and steppic plants: A review. Planta Med., 2013, 79(6), 425-436.
[http://dx.doi.org/10.1055/s-0032-1328331] [PMID: 23539351]
[22]
Feuerstein, I.; Müller, D.; Hubert, K.; Danin, A.; Segal, R. The constitution of essential oils from Artemisia herba-alba populations of Israel and Sinai. Phytochemistry, 1986, 25(10), 2343-2347.
[http://dx.doi.org/10.1016/S0031-9422(00)81692-1]
[23]
Khafagy, S.; Gharbo, S.; Sarg, T. Phytochemical investigation of Artemisia herba-alba. Planta Med., 1971, 20(3), 90-96.
[http://dx.doi.org/10.1055/s-0028-1099670] [PMID: 5154610]
[24]
Marrif, H.I.; Ali, B.H.; Hassan, K.M. Some pharmacological studies on Artemisia herba-alba (Asso.) in rabbits and mice. J. Ethnopharmacol., 1995, 49(1), 51-55.
[http://dx.doi.org/10.1016/0378-8741(95)01302-4] [PMID: 8786657]
[25]
Salah, S.M.; Jäger, A.K. Screening of traditionally used Lebanese herbs for neurological activities. J. Ethnopharmacol., 2005, 97(1), 145-149.
[http://dx.doi.org/10.1016/j.jep.2004.10.023] [PMID: 15652288]
[26]
Salido, S.; Valenzuela, L.R.; Altarejos, J.; Nogueras, M.; Sánchez, A.; Cano, E. Composition and infraspecific variability of Artemisia herba-alba from southern Spain. Biochem. Syst. Ecol., 2004, 32(3), 265-277.
[http://dx.doi.org/10.1016/j.bse.2003.09.002]
[27]
Twaij, H.A.A.; Al-Badr, A.A. Hypoglycemic activity of Artemisia herba-alba. J. Ethnopharmacol., 1988, 24(2-3), 123-126.
[http://dx.doi.org/10.1016/0378-8741(88)90143-2] [PMID: 3253482]
[28]
Yashphe, J.; Segal, R.; Breuer, A.; Erdreich-Naftali, G. Antibacterial activity of Artemisia herba-alba. J. Pharm. Sci., 1979, 68(7), 924-925.
[http://dx.doi.org/10.1002/jps.2600680742] [PMID: 458619]
[29]
Al-Shamaony, L.; Al-Khazraji, S.M.; Twaij, H.A.A. Hypoglycaemic effect of Artemisia herba-alba. II. Effect of a valuable extract on some blood parameters in diabetic animals. J. Ethnopharmacol., 1994, 43(3), 167-171.
[http://dx.doi.org/10.1016/0378-8741(94)90038-8] [PMID: 7990489]
[30]
Iriadam, M.; Musa, D.; Gümüflhan, H.; Baba, F. Effects of two turkish medicinal plants Artemisia herba-alba and Teucrium polium on blood glucose levels and other biochemical parameters in rabbits. J. Mol. Cell Biol., 2006, 5, 19-24.
[31]
Bennani-Kabchi, N.; Cherrah, Y.; Fdhil, H.; Marque, G. Therapeutic effect of Artemisia herba-alba on lipidic and carbohydrate metabolism in diabetic sand rat (Psammomys obesus). Pharmacol. Res., 1995, 31, 381.
[http://dx.doi.org/10.1016/1043-6618(95)87782-7]
[32]
He, L.; Wu, Y.; Lin, L.; Wang, J.; Wu, Y.; Chen, Y.; Yi, Z.; Liu, M.; Pang, X. Hispidulin, a small flavonoid molecule, suppresses the angiogenesis and growth of human pancreatic cancer by targeting vascular endothelial growth factor receptor 2-mediated PI3K/Akt/mTOR signaling pathway. Cancer Sci., 2011, 102(1), 219-225.
[http://dx.doi.org/10.1111/j.1349-7006.2010.01778.x] [PMID: 21087351]
[33]
Ji, H.F.; Li, X.J.; Zhang, H.Y. Natural products and drug discovery. EMBO Rep., 2009, 10(3), 194-200.
[http://dx.doi.org/10.1038/embor.2009.12] [PMID: 19229284]
[34]
Jung, M.; Park, M.; Lee, H.; Kang, Y.H.; Kang, E.; Kim, S. Antidiabetic agents from medicinal plants. Curr. Med. Chem., 2006, 13(10), 1203-1218.
[http://dx.doi.org/10.2174/092986706776360860] [PMID: 16719780]
[35]
Sekiou, O.; Boumendjel, M.; Taibi, F.; Boumendjel, A.; Messarah, M. Mitigating effects of antioxidant properties of Artemisia herba-alba aqueous extract on hyperlipidemia and oxidative damage in alloxan-induced diabetic rats. Arch. Physiol. Biochem., 2019, 125(2), 163-173.
[http://dx.doi.org/10.1080/13813455.2018.1443470] [PMID: 29482369]
[36]
Nakajima, K.; Yamauchi, K.; Shigematsu, S.; Ikeo, S.; Komatsu, M.; Aizawa, T.; Hashizume, K. Selective attenuation of metabolic branch of insulin receptor down-signaling by high glucose in a hepatoma cell line, HepG2 cells. J. Biol. Chem., 2000, 275(27), 20880-20886.
[http://dx.doi.org/10.1074/jbc.M905410199] [PMID: 10764799]
[37]
Belhattab, R.; Amor, L.; Barroso, J.G.; Pedro, L.G.; Cristina Figueiredo, A. Essential oil from Artemisia herba-alba Asso grown wild in Algeria: Variability assessment and comparison with an updated literature survey. Arab. J. Chem., 2014, 7(2), 243-251.
[http://dx.doi.org/10.1016/j.arabjc.2012.04.042]
[38]
Cirak, C.; Radusiene, J.; Ivanauskas, L.; Jakstas, V.; Çamaş, N. Changes in the content of bioactive substances among Hypericum montbretii populations from Turkey. Rev. Bras. Farmacogn., 2014, 24(1), 20-24.
[http://dx.doi.org/10.1590/0102-695X20142413352]
[39]
Khlifi, D.; Sghaier, R.M.; Amouri, S.; Laouini, D.; Hamdi, M.; Bouajila, J. Composition and anti-oxidant, anti-cancer and anti-inflammatory activities of Artemisia herba-alba, Ruta chalpensis L. and Peganum harmala L. Food Chem. Toxicol., 2013, 55, 202-208.
[http://dx.doi.org/10.1016/j.fct.2013.01.004] [PMID: 23333573]
[40]
Lupidi, G.; Bramucci, M.; Quassinti, L.; Fornari, E.; Avenali, L.; Khalife, H.; Gali-Muhtasib, H.U. Antiproliferative activities of Artemisia herba-alba ethanolic extract in human colon cancer cell line (HCT116). Alternative Medicine Studies, 2011, 1(1), 14.
[http://dx.doi.org/10.4081/ams.2011.e14]
[41]
Tilaoui, M.; Ait Mouse, H.; Jaafari, A.; Zyad, A. Comparative phytochemical analysis of essential oils from different biological parts of Artemisia herba-alba and their cytotoxic effect on cancer cells. PLoS One, 2015, 10(7)e0131799
[http://dx.doi.org/10.1371/journal.pone.0131799] [PMID: 26196123]
[42]
Abderrahman, S.M.; Jamal Shbailat, S. Genotoxic and cytotoxic effects of Artemisia herba-alba on mammalian cells. Caryologia, 2014, 67(4), 265-272.
[http://dx.doi.org/10.1080/0144235X.2014.974355]
[43]
Gacem, M.A.; Ould El Hadj-Khelil, A.; Boudjemaa, B.; Gacem, H. Phytochemistry, Toxicity and Pharmacology of Pistacia Lentiscus, Artemisia herba-alba and Citrullus Colocynthis. In: Sustain Agric Rev 39; Springer International Publishing: Cham , 2020; 39, pp. 57-93.
[44]
Hamza, N.; Berke, B.; Cheze, C.; Marais, S.; Lorrain, S.; Abdouelfath, A.; Lassalle, R.; Carles, D.; Gin, H.; Moore, N. Effect of Centaurium erythraea Rafn, Artemisia herba-alba Asso and Trigonella foenum-graecum L. on liver fat accumulation in C57BL/6J mice with high-fat diet-induced type 2 diabetes. J. Ethnopharmacol., 2015, 171, 4-11.
[http://dx.doi.org/10.1016/j.jep.2015.05.027] [PMID: 26023031]
[45]
Mansi, K.; Abu-Albasal, M.; Aburjia, T. Hepatoprotective activity of methanol extracts from Artemisia Sieberi Besser (A. herba-alba) against ethanol induced hepatic damage rats. Res. J. Med. Sci., 2019, 13(5), 102-108.
[http://dx.doi.org/10.36478/rjmsci.2019.102.108]
[46]
Rezaei, A. ShekarForoush, S.; Changizi Ashtiyani, S.; Aqababa, H.; Zarei, A.; Azizi, M.; Yarmahmodi, H. The effects of Artemisia aucheri extract on hepatotoxicity induced by thioacetamide in male rats. Avicenna J. Phytomed., 2013, 3(4), 293-301.
[PMID: 25050286]
[47]
Abushwereb, H.; Tolba, M. Gastroprotective activity of Artemisia herba-alba aqueous extract on aspirin-induced gastric lesions in albino rats. J. Pharm. Appl. Chem., 2016, 2(3), 141-145.
[http://dx.doi.org/10.18576/jpac/020303]
[48]
King, G.L.; Loeken, M.R. Hyperglycemia-induced oxidative stress in diabetic complications. Histochem. Cell Biol., 2004, 122(4), 333-338.
[http://dx.doi.org/10.1007/s00418-004-0678-9] [PMID: 15257460]
[49]
Bourebaba, L.; Bedjou, F.; Röcken, M.; Marycz, K. Nortropane alkaloids as pharmacological chaperones in the rescue of equine adipose-derived mesenchymal stromal stem cells affected by metabolic syndrome through mitochondrial potentiation, endoplasmic reticulum stress mitigation and insulin resistance alleviation. Stem Cell Res. Ther., 2019, 10(1), 178.
[http://dx.doi.org/10.1186/s13287-019-1292-z] [PMID: 31215461]
[50]
Kowaltowski, A.J.; de Souza-Pinto, N.C.; Castilho, R.F.; Vercesi, A.E. Mitochondria and reactive oxygen species. Free Radic. Biol. Med., 2009, 47(4), 333-343.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.05.004] [PMID: 19427899]
[51]
Mighri, H.; Hajlaoui, H.; Akrout, A.; Najjaa, H.; Neffati, M. Antimicrobial and antioxidant activities of Artemisia herba-alba essential oil cultivated in Tunisian arid zone. C. R. Chim., 2010, 13(3), 380-386.
[http://dx.doi.org/10.1016/j.crci.2009.09.008]
[52]
Mohamed, A.E-H.H.; El-Sayed, M.A.; Hegazy, M.E.; Helaly, S.E.; Esmail, A.M.; Mohamed, N.S. Chemical constituents and biological activities of Artemisia herba-alba. Rec. Nat. Prod., 2010, 4, 1-25.
[53]
Rafiq, R.; Hayek, S.; Anyanwu, U.; Hardy, B.; Giddings, V.; Ibrahim, S.; Tahergorabi, R.; Kang, H. Antibacterial and antioxidant activities of essential oils from Artemisia herba-alba Asso., Pelargonium capitatum × radens and Laurus nobilis L. Foods, 2016, 5(4), 28.
[http://dx.doi.org/10.3390/foods5020028] [PMID: 28231123]
[54]
Aouadi, D.; Luciano, G.; Vasta, V.; Nasri, S.; Brogna, D.M.R.; Abidi, S.; Priolo, A.; Salem, H.B. The antioxidant status and oxidative stability of muscle from lambs receiving oral administration of Artemisia herba-alba and Rosmarinus officinalis essential oils. Meat Sci., 2014, 97(2), 237-243.
[http://dx.doi.org/10.1016/j.meatsci.2014.02.005] [PMID: 24583334]
[55]
Sekiou, O.; Boumendjel, M.; Taibi, F.; Tichati, L.; Boumendjel, A.; Messarah, M. Nephroprotective effect of Artemisia herba-alba aqueous extract in alloxan-induced diabetic rats. J. Tradit. Complement. Med., 2021, 11(1), 53-61.
[http://dx.doi.org/10.1016/j.jtcme.2020.01.001] [PMID: 33511062]
[56]
Green, K.; Brand, M.D.; Murphy, M.P. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes, 2004, 53(Suppl. 1), S110-S118.
[http://dx.doi.org/10.2337/diabetes.53.2007.S110] [PMID: 14749275]
[57]
Sivitz, W.I.; Yorek, M.A. Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid. Redox Signal., 2010, 12(4), 537-577.
[http://dx.doi.org/10.1089/ars.2009.2531] [PMID: 19650713]
[58]
Rovira-Llopis, S.; Bañuls, C.; Diaz-Morales, N.; Hernandez-Mijares, A.; Rocha, M.; Victor, V.M. Mitochondrial dynamics in type 2 diabetes: Pathophysiological implications. Redox Biol., 2017, 11, 637-645.
[http://dx.doi.org/10.1016/j.redox.2017.01.013] [PMID: 28131082]
[59]
Saben, J.L.; Boudoures, A.L.; Asghar, Z.; Thompson, A.; Drury, A.; Zhang, W.; Chi, M.; Cusumano, A.; Scheaffer, S.; Moley, K.H. Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations. Cell Rep., 2016, 16(1), 1-8.
[http://dx.doi.org/10.1016/j.celrep.2016.05.065] [PMID: 27320925]
[60]
Echeverría, F.; Valenzuela, R.; Bustamante, A.; Álvarez, D.; Ortiz, M.; Espinosa, A.; Illesca, P.; Gonzalez-Mañan, D.; Videla, L.A. High-fat diet induces mouse liver steatosis with a concomitant decline in energy metabolism: attenuation by eicosapentaenoic acid (EPA) or hydroxytyrosol (HT) supplementation and the additive effects upon EPA and HT co-administration. Food Funct., 2019, 10(9), 6170-6183.
[http://dx.doi.org/10.1039/C9FO01373C] [PMID: 31501836]
[61]
Ortiz, M.; Soto-Alarcón, S.A.; Orellana, P.; Espinosa, A.; Campos, C.; López-Arana, S.; Rincón, M.A.; Illesca, P.; Valenzuela, R.; Videla, L.A. Suppression of high-fat diet-induced obesity-associated liver mitochondrial dysfunction by docosahexaenoic acid and hydroxytyrosol co-administration. Dig. Liver Dis., 2020, 52(8), 895-904.
[http://dx.doi.org/10.1016/j.dld.2020.04.019] [PMID: 32620521]
[62]
Bakkali, F.; Averbeck, S.; Averbeck, D.; Zhiri, A.; Idaomar, M. Cytotoxicity and gene induction by some essential oils in the yeast Saccharomyces cerevisiae. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2005, 585(1-2), 1-13.
[http://dx.doi.org/10.1016/j.mrgentox.2005.03.013] [PMID: 15975845]
[63]
Hamza, N.; Berke, B.; Cheze, C.; Le Garrec, R.; Lassalle, R.; Agli, A.N.; Robinson, P.; Gin, H.; Moore, N. Treatment of high fat diet induced type 2 diabetes in C57BL/6J mice by two medicinal plants used in traditional treatment of diabetes in the east of Algeria. J. Ethnopharmacol., 2011, 133(2), 931-933.
[http://dx.doi.org/10.1016/j.jep.2010.11.019] [PMID: 21094236]
[64]
Chakraborty, C. Biochemical and molecular basis of insulin resistance. Curr. Protein Pept. Sci., 2006, 7(2), 113-121.
[http://dx.doi.org/10.2174/138920306776359759] [PMID: 16611137]
[65]
Turban, S.; Hajduch, E. Protein kinase C isoforms: Mediators of reactive lipid metabolites in the development of insulin resistance. FEBS Lett., 2011, 585(2), 269-274.
[http://dx.doi.org/10.1016/j.febslet.2010.12.022] [PMID: 21176778]
[66]
Hamza, N.; Berke, B.; Cheze, C.; Agli, A.N.; Robinson, P.; Gin, H.; Moore, N. Prevention of type 2 diabetes induced by high fat diet in the C57BL/6J mouse by two medicinal plants used in traditional treatment of diabetes in the east of Algeria. J. Ethnopharmacol., 2010, 128(2), 513-518.
[http://dx.doi.org/10.1016/j.jep.2010.01.004] [PMID: 20064599]
[67]
Bourebaba, L.; Łyczko, J.; Alicka, M.; Bourebaba, N.; Szumny, A.; Fal, A.; Marycz, K. Inhibition of protein-Tyrosine phosphatase PTP1B and LMPTP promotes Palmitate/Oleate-challenged HepG2 cell survival by reducing lipoapoptosis, improving mitochondrial dynamics and mitigating oxidative and endoplasmic reticulum stress. J. Clin. Med., 2020, 9(5), 1294.
[http://dx.doi.org/10.3390/jcm9051294] [PMID: 32369900]
[68]
Bourebaba, L.; Marycz, K. Pathophysiological implication of fetuin-a glycoprotein in the development of metabolic disorders: A concise review. J. Clin. Med., 2019, 8(12), 2033.
[http://dx.doi.org/10.3390/jcm8122033] [PMID: 31766373]
[69]
Petra, P.H. The plasma sex steroid binding protein (SBP or SHBG). A critical review of recent developments on the structure, molecular biology and function. J. Steroid Biochem. Mol. Biol., 1991, 40(4-6), 735-753.
[http://dx.doi.org/10.1016/0960-0760(91)90299-K] [PMID: 1958572]
[70]
Le, T.N.; Nestler, J.E.; Strauss, J.F., III; Wickham, E.P., III Sex hormone-binding globulin and type 2 diabetes mellitus. Trends Endocrinol. Metab., 2012, 23(1), 32-40.
[http://dx.doi.org/10.1016/j.tem.2011.09.005] [PMID: 22047952]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy