Login Register Cart 0
Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Evaluation of Insulin Resistance Induced Brain Tissue Dysfunction in Obese Dams and their Neonates: Role of Ipriflavone Amelioration

Author(s): Rania A. Gad, Eman S. Abdel-Reheim, Gaber M.G. Shehab, Hani S. Hafez* and Abdelaziz S.A. Abuelsaad*

Volume 24, Issue 6, 2021

Published on: 08 August, 2020

Page: [767 - 780] Pages: 14

DOI: 10.2174/1386207323666200808181148

Price: $65

Abstract

Background: Nonalcoholic steatohepatitis (NASH) is associated with activation of liver fibrogenesis and predisposes to cirrhosis and associated morbi-mortality. A high fat high cholesterol diet (HFD) was provided to female albino rats to establish a NASH model. It is well known that the offspring of obese mothers have an increased risk of obesity and diabetes. The present study aimed at evaluating the ameliorative effects of ipriflavone (IP) as a natural food supplement on lipid metabolism, improving insulin sensitivity, reducing oxidative stress and inflammation, modifying metabolic risk factors and/or reduce brain damage, in both neonates and their dams.

Materials and Methods: The present aim was achieved by evaluating the oxidative stress and antioxidant defense system biomarkers, as thiobarbituric acid reactive substances (TBARS) and reduced glutathione (GSH), catalase, and superoxide dismutase (SOD) activities. In addition, the neurotransmitter acetylcholine (Ach) and acetylcholine esterase (AchE) activities, as well as levels of the apolipoprotein E4 (APOE4); β-secretase, hyper phosphor-tau and β-amyloid 42; 3-hydroxy- 3-methyl glutaryl coenzyme A reductase (HMG CoA R)” and COX-II by immunoblotting assays in the brain tissue of neonates and their dams in all the studied groups.

Results: A very significant amelioration in acetylcholine and acetylcholine esterase neurotransmitters, Alzheimer’s makers (β-amyloid), antioxidants (reduced glutathione (GSH) contents, catalase (CAT) and superoxide dismutase (SOD); and inflammatory cytokines in NASH model is observed upon administrating ipriflavone (IP) as a natural food supplement. The multifunctional activities of ipriflavone as an antioxidant, anti-inflammatory and anti-insulin resistance drug were discussed and correlated with other investigations.

Conclusion: Regarding steatohepatitis, the present study confirmed the anti-inflammatory effects of the ipriflavone (IP). Therefore, future studies should focus on hepatic fatty acid uptake, hepatic lipogenesis, and fatty acid oxidation and the role of IP in regulating hepatic fat metabolism. In addition, natural products like IP could be combined with the highly used pharmaceutical drugs to reduce the side effects of nonalcoholic steatohepatitis, and minimize progression of dementia. Moreover, the present study supports further attempts to heal the neural dysfunction via antioxidant and anti-inflammatory cascade activities using ipriflavone (IP).

Keywords: Neonates obesity, insulin resistance, Nonalcoholic Fatty Liver Disease (NAFLD), Ipriflavone HMG CoA R, Acetylcholine esterase, oxidative stress.

« Previous Next »
[1]
Svegliati-Baroni, G.; Candelaresi, C.; Saccomanno, S.; Ferretti, G.; Bachetti, T.; Marzioni, M.; De Minicis, S.; Nobili, L.; Salzano, R.; Omenetti, A.; Pacetti, D.; Sigmund, S.; Benedetti, A.; Casini, A. A model of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptor-α and n-3 polyunsaturated fatty acid treatment on liver injury. Am. J. Pathol., 2006, 169(3), 846-860.
[http://dx.doi.org/10.2353/ajpath.2006.050953] [PMID: 16936261]
[2]
Bloomgarden, Z.T. Insulin resistance: current concepts. Clin. Ther., 1998, 20(2), 216-231.
[http://dx.doi.org/10.1016/S0149-2918(98)80086-6] [PMID: 9589814]
[3]
Boden, G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes, 1997, 46(1), 3-10.
[http://dx.doi.org/10.2337/diab.46.1.3] [PMID: 8971073]
[4]
Haffner, S.M.; Mykkänen, L.; Festa, A.; Burke, J.P.; Stern, M.P. Insulin-resistant prediabetic subjects have more atherogenic risk factors than insulin-sensitive prediabetic subjects: implications for preventing coronary heart disease during the prediabetic state. Circulation, 2000, 101(9), 975-980.
[http://dx.doi.org/10.1161/01.CIR.101.9.975] [PMID: 10704163]
[5]
González-Saldivar, G.; Rodríguez-Gutiérrez, R.; Ocampo-Candiani, J.; González-González, J.G.; Gómez-Flores, M. Skin manifestations of insulin resistance: from a biochemical stance to a clinical diagnosis and management. Dermatol. Ther. (Heidelb.), 2017, 7(1), 37-51.
[http://dx.doi.org/10.1007/s13555-016-0160-3] [PMID: 27921251]
[6]
Watson, G.S.; Craft, S. The role of insulin resistance in the pathogenesis of Alzheimer’s disease: implications for treatment. CNS Drugs, 2003, 17(1), 27-45.
[http://dx.doi.org/10.2165/00023210-200317010-00003] [PMID: 12467491]
[7]
Manolopoulos, K.N.; Klotz, L.O.; Korsten, P.; Bornstein, S.R.; Barthel, A. Linking Alzheimer’s disease to insulin resistance: the FoxO response to oxidative stress. Mol. Psychiatry, 2010, 15(11), 1046-1052.
[http://dx.doi.org/10.1038/mp.2010.17] [PMID: 20966918]
[8]
Wang, X.; Zhou, X.; Li, G.; Zhang, Y.; Wu, Y.; Song, W. Modifications and trafficking of APP in the pathogenesis of Alzheimer’s disease. Front. Mol. Neurosci., 2017, 10, 294.
[http://dx.doi.org/10.3389/fnmol.2017.00294] [PMID: 28966576]
[9]
Araki, W. Post-translational regulation of the β-secretase BACE1. Brain Res. Bull., 2016, 126(Pt 2), 170-177.
[http://dx.doi.org/10.1016/j.brainresbull.2016.04.009] [PMID: 27086128]
[10]
Ghosh, A.K.; Cárdenas, E.L.; Osswald, H.L. The design, development, and evaluation of BACE1 inhibitors for the treatment of Alzheimer’s disease. Alzheimer’s Disease II; Springer, 2016, pp. 27-85.
[http://dx.doi.org/10.1007/7355_2016_16]
[11]
Sabbah, D.A.; Zhong, H.A. Modeling the protonation states of β-secretase binding pocket by molecular dynamics simulations and docking studies. J. Mol. Graph. Model., 2016, 68, 206-215.
[http://dx.doi.org/10.1016/j.jmgm.2016.07.005] [PMID: 27474865]
[12]
Brambillaa, A.; Lonati, E.; Milani, C.; Rizzo, A.M.; Farina, F.; Botto, L.; Masserini, M.; Palestini, P.; Bulbarelli, A. Ischemic conditions and ß-secretase activation: The impact of membrane cholesterol enrichment as triggering factor in rat brain endothelial cells. Int. J. Biochem. Cell Biol., 2015, 69, 95-104.
[http://dx.doi.org/10.1016/j.biocel.2015.10.005] [PMID: 27022655]
[13]
Youn, K.; Lee, J.; Ho, C-T.; Jun, M. Discovery of polymethoxyflavones from black ginger (Kaempferia parviflora) as potential β-secretase (BACE1) inhibitors. J. Funct. Foods, 2016, 20, 567-574.
[http://dx.doi.org/10.1016/j.jff.2015.10.036]
[14]
Sun, J-H.; Yu, J-T.; Tan, L. The role of cholesterol metabolism in Alzheimer’s disease. Mol. Neurobiol., 2015, 51(3), 947-965.
[http://dx.doi.org/10.1007/s12035-014-8749-y] [PMID: 24838626]
[15]
Gardner, L.E.; White, J.D.; Eimerbrink, M.J.; Boehm, G.W.; Chumley, M.J. Imatinib methanesulfonate reduces hyperphosphorylation of tau following repeated peripheral exposure to lipopolysaccharide. Neuroscience, 2016, 331, 72-77.
[http://dx.doi.org/10.1016/j.neuroscience.2016.06.007] [PMID: 27320209]
[16]
Head, K. Ipriflavone: an important bone-building isoflavone. Altern. Med. Rev., 1999, 4(1), 10-22.
[17]
Lu, C.; Wang, Y.; Wang, D.; Zhang, L.; Lv, J.; Jiang, N.; Fan, B.; Liu, X.; Wang, F. Neuroprotective effects of soy isoflavones on scopolamine-induced amnesia in mice. Nutrients, 2018, 10(7), 853.
[http://dx.doi.org/10.3390/nu10070853] [PMID: 29966363]
[18]
Agnusdei, D.; Bufalino, L. Efficacy of ipriflavone in established osteoporosis and long-term safety. Calcif. Tissue Int., 1997, 61(1)(Suppl. 1), S23-S27.
[http://dx.doi.org/10.1007/s002239900381] [PMID: 9263613]
[19]
Pagano, L.; Teofili, L.; Mele, L.; Piantelli, M.; Ranelletti, F.O.; Equitani, F.; Larocca, L.M.; Leone, G. Oral ipriflavone (7-isopropoxy-isoflavone) treatment for elderly patients with resistant acute leukemias. Ann. Oncol., 1999, 10(1), 124-125.
[http://dx.doi.org/10.1023/A:1008364402623] [PMID: 10076734]
[20]
Larocca, L.M.; Teofili, L.; Leone, G.; Sica, S.; Pierelli, L.; Menichella, G.; Scambia, G.; Benedetti Panici, P.; Ricci, R.; Piantelli, M. Antiproliferative activity of quercetin on normal bone marrow and leukaemic progenitors. Br. J. Haematol., 1991, 79(4), 562-566.
[http://dx.doi.org/10.1111/j.1365-2141.1991.tb08082.x] [PMID: 1772777]
[21]
Padhi, E.M.; Hawke, A.; Liu, R.; Zhu, H.; Duncan, A.M.; Tsao, R. Tracking isoflavones in whole soy flour, soy muffins and the plasma of hypercholesterolaemic adults. J. Funct. Foods, 2016, 24, 420-428.
[http://dx.doi.org/10.1016/j.jff.2016.04.027]
[22]
Abdel-Latif, M.S.; Abady, M.M.; Saleh, S.R.; Abdel-Monaem, N.; Ghareeb, D.A. Effect of berberine and ipriflavone mixture against scopolamine-induced alzheimer-like disease. Int. J. Pharm., 2019, 9(3), 48-63.
[23]
Hafez, H.S.; Ghareeb, D.A.; Saleh, S.R.; Abady, M.M.; El Demellawy, M.A.; Hussien, H.; Abdel-Monem, N. Neuroprotective effect of ipriflavone against scopolamine-induced memory impairment in rats. Psychopharmacology (Berl.), 2017, 234(20), 3037-3053.
[http://dx.doi.org/10.1007/s00213-017-4690-x] [PMID: 28733814]
[24]
Abdel-Reheim, E.S.; Hosni, A.A. Ameliorative effects of cinnamaldehyde and ellagic acid on hematological alterations associated with pathophysiology of gestational diabetes mellitus in albino rats. Egypt. J. Zool. (Lond.), 2013, 60, 375-396.
[25]
Zhurnal, K-F. Chemical. Pharm. J., 1990, 24(9), 38.
[26]
Siest, G.; Henny, J.; Schiele, F. Interprétation des examens de laboratoire: valeurs de référence et variations biologiques; S. Karger AG: Switzerland, 1981.
[27]
Olsson, R.; Carlsson, P-O. Better vascular engraftment and function in pancreatic islets transplanted without prior culture. Diabetologia, 2005, 48(3), 469-476.
[http://dx.doi.org/10.1007/s00125-004-1650-x] [PMID: 15696296]
[28]
Friedewald, W.T.; Levy, R.I.; Fredrickson, D.S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem., 1972, 18(6), 499-502.
[http://dx.doi.org/10.1093/clinchem/18.6.499] [PMID: 4337382]
[29]
Mihara, M.; Uchiyama, M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem., 1978, 86(1), 271-278.
[http://dx.doi.org/10.1016/0003-2697(78)90342-1] [PMID: 655387]
[30]
Sinha, A.K. Colorimetric assay of catalase. Anal. Biochem., 1972, 47(2), 389-394.
[http://dx.doi.org/10.1016/0003-2697(72)90132-7] [PMID: 4556490]
[31]
Sedlak, J.; Lindsay, R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem., 1968, 25(1), 192-205.
[http://dx.doi.org/10.1016/0003-2697(68)90092-4] [PMID: 4973948]
[32]
Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 1974, 47(3), 469-474.
[http://dx.doi.org/10.1111/j.1432-1033.1974.tb03714.x] [PMID: 4215654]
[33]
Ghareeb, D.A.; Hafez, H.S.; Hussien, H.M.; Kabapy, N.F. Non-alcoholic fatty liver induces insulin resistance and metabolic disorders with development of brain damage and dysfunction. Metab. Brain Dis., 2011, 26(4), 253-267.
[http://dx.doi.org/10.1007/s11011-011-9261-y] [PMID: 21881966]
[34]
Gilberstadt, M.L.; Russell, J.A. Determination of picomole quantities of acetylcholine and choline in physiologic salt solutions. Anal. Biochem., 1984, 138(1), 78-85.
[http://dx.doi.org/10.1016/0003-2697(84)90772-3] [PMID: 6731854]
[35]
Kovarik, Z.; Radić, Z.; Berman, H.A.; Simeon-Rudolf, V.; Reiner, E.; Taylor, P. Acetylcholinesterase active centre and gorge conformations analysed by combinatorial mutations and enantiomeric phosphonates. Biochem. J., 2003, 373(Pt 1), 33-40.
[http://dx.doi.org/10.1042/bj20021862] [PMID: 12665427]
[36]
Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 2001, 29(9), e45-e45.
[http://dx.doi.org/10.1093/nar/29.9.e45] [PMID: 11328886]
[37]
Bradford, M.M. 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.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[38]
Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 nature, 1970, 227(5229), 680.
[39]
Chen, L.; Deng, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J.; Li, Y.; Wang, X.; Zhao, L. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget, 2017, 9(6), 7204-7218.
[http://dx.doi.org/10.18632/oncotarget.23208] [PMID: 29467962]
[40]
Lu, M-P.; Wang, R.; Song, X.; Chibbar, R.; Wang, X.; Wu, L.; Meng, Q.H. Dietary soy isoflavones increase insulin secretion and prevent the development of diabetic cataracts in streptozotocin-induced diabetic rats. Nutr. Res., 2008, 28(7), 464-471.
[http://dx.doi.org/10.1016/j.nutres.2008.03.009] [PMID: 19083447]
[41]
Stintzing, F.C.; Hoffmann, M.; Carle, R. Thermal degradation kinetics of isoflavone aglycones from soy and red clover. Mol. Nutr. Food Res., 2006, 50(4-5), 373-377.
[http://dx.doi.org/10.1002/mnfr.200500187] [PMID: 16598813]
[42]
Hamad, E.M.; Taha, S.H.; Abou Dawood, A.G.; Sitohy, M.Z.; Abdel-Hamid, M. Protective effect of whey proteins against nonalcoholic fatty liver in rats. Lipids Health Dis., 2011, 10(1), 57.
[http://dx.doi.org/10.1186/1476-511X-10-57] [PMID: 21489294]
[43]
Sundaresan, S.; Vijayagopal, P.; Mills, N.; Imrhan, V.; Prasad, C. A mouse model for nonalcoholic steatohepatitis. J. Nutr. Biochem., 2011, 22(10), 979-984.
[http://dx.doi.org/10.1016/j.jnutbio.2010.08.011] [PMID: 21190824]
[44]
Andersen, C.; Schjoldager, J.G.; Tortzen, C.G.; Vegge, A.; Hufeldt, M.R.; Skaanild, M.T. 2-heptyl-formononetin increases cholesterol and induces hepatic steatosis in mice. BioMed research international, 2013.
[45]
El-Sayed, M.M.; Ghareeb, D.A.; Talat, H.A.; Sarhan, E.M. High fat diet induced insulin resistance and elevated retinol binding protein 4 in female rats; treatment and protection with Berberis vulgaris extract and vitamin A Pak J Pharm Sc, 2013, 26(6)
[46]
García-Monzón, C.; Lo Iacono, O.; Mayoral, R.; González-Rodríguez, A.; Miquilena-Colina, M.E.; Lozano-Rodríguez, T.; García-Pozo, L.; Vargas-Castrillón, J.; Casado, M.; Boscá, L.; Valverde, A.M.; Martín-Sanz, P. Hepatic insulin resistance is associated with increased apoptosis and fibrogenesis in nonalcoholic steatohepatitis and chronic hepatitis C. J. Hepatol., 2011, 54(1), 142-152.
[http://dx.doi.org/10.1016/j.jhep.2010.06.021] [PMID: 20888662]
[47]
Sertoglu, E.; Ercin, C.N.; Celebi, G.; Gurel, H.; Kayadibi, H.; Genc, H.; Kara, M.; Dogru, T. The relationship of serum uric acid with non-alcoholic fatty liver disease. Clin. Biochem., 2014, 47(6), 383-388.
[http://dx.doi.org/10.1016/j.clinbiochem.2014.01.029] [PMID: 24525254]
[48]
Da Silva, H.E.; Arendt, B.M.; Noureldin, S.A.; Therapondos, G.; Guindi, M.; Allard, J.P. A cross-sectional study assessing dietary intake and physical activity in Canadian patients with nonalcoholic fatty liver disease vs healthy controls. J. Acad. Nutr. Diet., 2014, 114(8), 1181-1194.
[http://dx.doi.org/10.1016/j.jand.2014.01.009] [PMID: 24631112]
[49]
Hyogo, H.; Yamagishi, S.; Maeda, S.; Kimura, Y.; Ishitobi, T.; Chayama, K. Atorvastatin improves disease activity of nonalcoholic steatohepatitis partly through its tumour necrosis factor-α-lowering property. Dig. Liver Dis., 2012, 44(6), 492-496.
[http://dx.doi.org/10.1016/j.dld.2011.12.013] [PMID: 22265683]
[50]
Jungbauer, A.; Medjakovic, S. Phytoestrogens and the metabolic syndrome. J. Steroid Biochem. Mol. Biol., 2014, 139, 277-289.
[http://dx.doi.org/10.1016/j.jsbmb.2012.12.009] [PMID: 23318879]
[51]
Ying, H-Z.; Liu, Y-H.; Yu, B.; Wang, Z-Y.; Zang, J-N.; Yu, C-H. Dietary quercetin ameliorates nonalcoholic steatohepatitis induced by a high-fat diet in gerbils. Food Chem. Toxicol., 2013, 52, 53-60.
[http://dx.doi.org/10.1016/j.fct.2012.10.030] [PMID: 23123425]
[52]
Zhou, C.; Lin, H.; Huang, Z.; Wang, J.; Wang, Y.; Yu, W. Effects of dietary soybean isoflavones on non-specific immune responses and hepatic antioxidant abilities and mRNA expression of two heat shock proteins (HSPs) in juvenile golden pompano Trachinotus ovatus under pH stress. Fish Shellfish Immunol., 2015, 47(2), 1043-1053.
[http://dx.doi.org/10.1016/j.fsi.2015.10.036] [PMID: 26518502]
[53]
Appel, B.; Fried, S.K. Effects of insulin and dexamethasone on lipoprotein lipase in human adipose tissue. Am. J. Physiol., 1992, 262(5 Pt 1), E695-E699.
[PMID: 1590379]
[54]
Oliveira, L.P.; de Jesús, R.P.; Freire, T.O.; Oliveira, C.P.; Castro Lyra, A.; Lyra, L.G. Possible molecular mechanisms soy-mediated in preventing and treating nonalcoholic fatty liver disease. Nutr. Hosp., 2012, 27(4), 991-998.
[PMID: 23165534]
[55]
Zhou, L.; Xiao, X.; Zhang, Q.; Zheng, J.; Deng, M. Maternal genistein intake mitigates the deleterious effects of high-fat diet on glucose and lipid metabolism and modulates gut microbiota in adult life of male mice. Front. Physiol., 2019, 10, 985.
[http://dx.doi.org/10.3389/fphys.2019.00985] [PMID: 31417434]
[56]
Huang, Y-H.; Ye, T-T.; Liu, C-X.; Wang, L.; Chen, Y-W.; Dong, Y. Maternal high-fat diet impairs glucose metabolism, β-cell function and proliferation in the second generation of offspring rats. Nutr. Metab. (Lond.), 2017, 14(1), 67.
[http://dx.doi.org/10.1186/s12986-017-0222-2] [PMID: 29118817]
[57]
Thompson, M.D.; Derse, A.; Ferey, J.; Reid, M.; Xie, Y.; Christ, M.; Chatterjee, D.; Nguyen, C.; Harasymowicz, N.; Guilak, F.; Moley, K.H.; Davidson, N.O. Transgenerational impact of maternal obesogenic diet on offspring bile acid homeostasis and nonalcoholic fatty liver disease. Am. J. Physiol. Endocrinol. Metab., 2019, 316(4), E674-E686.
[http://dx.doi.org/10.1152/ajpendo.00474.2018] [PMID: 30860882]
[58]
Kaur, N.; Sarkar, B.; Mittal, S.; Dhiman, M.; Taglialatela, G.; Perez-Polo, R.J. Oxidative stress events and neuronal dysfunction in Alzheimer’s disease: focus on APE1/Ref-1-mediated survival strategies.Free Radicals in Human Health and Disease; Springer, 2015, pp. 175-207.
[http://dx.doi.org/10.1007/978-81-322-2035-0_13]
[59]
Hopps, E.; Noto, D.; Caimi, G.; Averna, M.R. A novel component of the metabolic syndrome: the oxidative stress. Nutr. Metab. Cardiovasc. Dis., 2010, 20(1), 72-77.
[http://dx.doi.org/10.1016/j.numecd.2009.06.002] [PMID: 19747805]
[60]
Demircan, N.; Gurel, A.; Armutcu, F.; Unalacak, M.; Aktunc, E.; Atmaca, H. The evaluation of serum cystatin C, malondialdehyde, and total antioxidant status in patients with metabolic syndrome. Med. Sci. Monit., 2008, 14(2), CR97-CR101.
[PMID: 18227768]
[61]
Marseglia, L.; Manti, S.; D’Angelo, G.; Nicotera, A.; Parisi, E.; Di Rosa, G.; Gitto, E.; Arrigo, T. Oxidative stress in obesity: a critical component in human diseases. Int. J. Mol. Sci., 2014, 16(1), 378-400.
[http://dx.doi.org/10.3390/ijms16010378] [PMID: 25548896]
[62]
Kobayashi, H.; Matsuda, M.; Fukuhara, A.; Komuro, R.; Shimomura, I. Dysregulated glutathione metabolism links to impaired insulin action in adipocytes. Am. J. Physiol. Endocrinol. Metab., 2009, 296(6), E1326-E1334.
[http://dx.doi.org/10.1152/ajpendo.90921.2008] [PMID: 19366877]
[63]
Tsuda, M.; Kitazaki, T.; Ito, T.; Fujita, T. The effect of ipriflavone (TC-80) on bone resorption in tissue culture. J. Bone Miner. Res., 1986, 1(2), 207-211.
[http://dx.doi.org/10.1002/jbmr.5650010207] [PMID: 3503539]
[64]
Moscarini, M.; Patacchiola, F.; Spacca, G.; Palermo, P.; Caserta, D.; Valenti, M. New perspectives in the treatment of postmenopausal osteoporosis: ipriflavone. Gynecol. Endocrinol., 1994, 8(3), 203-207.
[http://dx.doi.org/10.3109/09513599409072456] [PMID: 7847106]
[65]
Mushtaq, G.; Greig, H Status of acetylcholinesterase and butyrylcholinesterase in Alzheimer's disease and type 2 diabetes mellitus CNS Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS Neurological Disorders), 2014, 13(8), 1432-1439.
[66]
Zhang, F.; Jiang, L. Neuroinflammation in Alzheimer’s disease. Neuropsychiatr. Dis. Treat., 2015, 11, 243-256.
[http://dx.doi.org/10.2147/NDT.S75546] [PMID: 25673992]
[67]
Das, A.; Kapoor, K.; Sayeepriyadarshini, A.T.; Dikshit, M.; Palit, G.; Nath, C. Immobilization stress-induced changes in brain acetylcholinesterase activity and cognitive function in mice. Pharmacol. Res., 2000, 42(3), 213-217.
[http://dx.doi.org/10.1006/phrs.2000.0678] [PMID: 10945925]
[68]
Emad, S.; Qadeer, S.; Sadaf, S.; Batool, Z.; Haider, S.; Perveen, T. Attenuation of stress induced memory deficits by nonsteroidal anti-inflammatory drugs (NSAIDs) in rats: Role of antioxidant enzymes. Pharmacol. Rep., 2017, 69(2), 300-305.
[http://dx.doi.org/10.1016/j.pharep.2016.11.009] [PMID: 28178591]
[69]
Thomareis, O.; Parlapani, A.; Kovatsi, L.; Giala, M. Effect of succinylcholine on the neuromuscular junction of hypoglycemic rats. Methods Find. Exp. Clin. Pharmacol., 2000, 22(3), 155-158.
[PMID: 10893697]
[70]
Antony, S.; Peeyush Kumar, T.; Mathew, J.; Anju, T.R.; Paulose, C.S. Hypoglycemia induced changes in cholinergic receptor expression in the cerebellum of diabetic rats. J. Biomed. Sci., 2010, 17(1), 7.
[http://dx.doi.org/10.1186/1423-0127-17-7] [PMID: 20137086]
[71]
Mattsson, J.L.; Maurissen, J.P.; Nolan, R.J.; Brzak, K.A. Lack of differential sensitivity to cholinesterase inhibition in fetuses and neonates compared to dams treated perinatally with chlorpyrifos. Toxicol. Sci., 2000, 53(2), 438-446.
[http://dx.doi.org/10.1093/toxsci/53.2.438] [PMID: 10696792]
[72]
Pope, C.N.; Chakraborti, T.K.; Chapman, M.L.; Farrar, J.D.; Arthun, D. Comparison of in vivo cholinesterase inhibition in neonatal and adult rats by three organophosphorothioate insecticides. Toxicology, 1991, 68(1), 51-61.
[http://dx.doi.org/10.1016/0300-483X(91)90061-5] [PMID: 1714639]
[73]
Liu, J.; Olivier, K.; Pope, C.N. Comparative neurochemical effects of repeated methyl parathion or chlorpyrifos exposures in neonatal and adult rats. Toxicol. Appl. Pharmacol., 1999, 158(2), 186-196.
[http://dx.doi.org/10.1006/taap.1999.8693] [PMID: 10406933]
[74]
Song, X.; Seidler, F.J.; Saleh, J.L.; Zhang, J.; Padilla, S.; Slotkin, T.A. Cellular mechanisms for developmental toxicity of chlorpyrifos: targeting the adenylyl cyclase signaling cascade. Toxicol. Appl. Pharmacol., 1997, 145(1), 158-174.
[http://dx.doi.org/10.1006/taap.1997.8171] [PMID: 9221834]
[75]
Ayaz, M.; Sadiq, A.; Junaid, M.; Ullah, F.; Ovais, M.; Ullah, I.; Ahmed, J.; Shahid, M. Flavonoids as prospective neuroprotectants and their therapeutic propensity in aging associated neurological disorders. Front. Aging Neurosci., 2019, 11, 155.
[http://dx.doi.org/10.3389/fnagi.2019.00155] [PMID: 31293414]
[76]
Rezai-Zadeh, K.; Douglas Shytle, R.; Bai, Y.; Tian, J.; Hou, H.; Mori, T.; Zeng, J.; Obregon, D.; Town, T.; Tan, J. Flavonoid-mediated presenilin-1 phosphorylation reduces Alzheimer’s disease β-amyloid production. J. Cell. Mol. Med., 2009, 13(3), 574-588.
[http://dx.doi.org/10.1111/j.1582-4934.2008.00344.x] [PMID: 18410522]
[77]
Vepsäläinen, S.; Koivisto, H.; Pekkarinen, E.; Mäkinen, P.; Dobson, G.; McDougall, G.J.; Stewart, D.; Haapasalo, A.; Karjalainen, R.O.; Tanila, H.; Hiltunen, M. Anthocyanin-enriched bilberry and blackcurrant extracts modulate amyloid precursor protein processing and alleviate behavioral abnormalities in the APP/PS1 mouse model of Alzheimer’s disease. J. Nutr. Biochem., 2013, 24(1), 360-370.
[http://dx.doi.org/10.1016/j.jnutbio.2012.07.006] [PMID: 22995388]
[78]
Durazzo, T.C.; Mattsson, N.; Weiner, M.W. Alzheimer’s Disease Neuroimaging Initiative. Smoking and increased Alzheimer’s disease risk: a review of potential mechanisms. Alzheimers Dement., 2014, 10(3)(Suppl.), S122-S145.
[http://dx.doi.org/10.1016/j.jalz.2014.04.009] [PMID: 24924665]
[79]
Safieh, M.; Korczyn, A.D.; Michaelson, D.M. ApoE4: an emerging therapeutic target for Alzheimer’s disease. BMC Med., 2019, 17(1), 64.
[http://dx.doi.org/10.1186/s12916-019-1299-4] [PMID: 30890171]
[80]
Li, Z. New APOE-related therapeutic options for Alzheimer’s disease; AIP Conference ProceedingsAIP Publishing, 2019.
[81]
Jayaraman, A.; Pike, C.J. Alzheimer’s disease and type 2 diabetes: multiple mechanisms contribute to interactions. Curr. Diab. Rep., 2014, 14(4), 476.
[http://dx.doi.org/10.1007/s11892-014-0476-2] [PMID: 24526623]

Rights & Permissions Print Cite
Article Metrics
16
1
© 2024 Bentham Science Publishers | Privacy Policy