Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article

Neuroprotective Substances: Are they Able to Protect the Pancreatic Beta- Cells Too?

Author(s): Rita U. Ostrovskaya and Sergei V. Ivanov*

Volume 22, Issue 8, 2022

Published on: 29 April, 2022

Page: [834 - 841] Pages: 8

DOI: 10.2174/1871530322666220303162844

Price: $65

Abstract

Background: Growing pieces of evidence demonstrate a close relationship between type 2 diabetes (T2D) and neurodegenerative disorders such as Alzheimer’s disease. The similarity of physiological and pathological processes occurring in pancreatic β-cells and neurons over the course of these pathologies allows raising the question of the practicability of studying neuroprotective substances for their potential antidiabetic activity.

Objective: This review analyzes studies of antidiabetic and cytoprotective action on pancreatic β- cells of the neuroprotective compounds that can attenuate the oxidative stress and enhance the expression of neurotrophins: low-molecular-weight NGF mimetic compound GK-2, selective anxiolytic afobazole, antidepressants lithium chloride, and lithium carbonate on the rat streptozotocin model of T2D.

Results: It was found that all the above-listed neuroprotective substances have a pronounced antidiabetic activity. The decrease in the β-cells number, the average area of the pancreatic islets, as well as the violation of their morphological structure caused by the streptozotocin was significantly weakened by the therapy with the investigated neuroprotective substances. The extent of these morphological changes clearly correlates with the antihyperglycemic effect of these compounds.

Conclusion: The presented data indicate that the neuroprotective substances attenuating the damaging effect of oxidative stress and neurotrophins deficit cannot only protect neurons but also exert their cytoprotective effect towards pancreatic β-cells. These data may provide a theoretical basis for the further study of neuroprotective drugs as potential therapeutic options for T2D prevention and treatment.

Keywords: Type 2 diabetes, cytoprotection, neuroprotection, β-cells, streptozotocin, neurotrophins.

Graphical Abstract
[1]
Zhang, Y.; Huang, N.Q.; Yan, F.; Jin, H.; Zhou, S.Y.; Shi, J.S.; Jin, F. Diabetes mellitus and Alzheimer’s disease: GSK-3β as a potential link. Behav. Brain Res., 2018, 339, 57-65.
[http://dx.doi.org/10.1016/j.bbr.2017.11.015] [PMID: 29158110]
[2]
Fiore, V.; De Rosa, A.; Falasca, P.; Marci, M.; Guastamacchia, E.; Licchelli, B.; Giagulli, V.A.; De Pergola, G.; Poggi, A.; Triggiani, V. Focus on the correlations between Alzheimer’s disease and type 2 diabetes. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(5), 571-579.
[http://dx.doi.org/10.2174/1871530319666190311141855] [PMID: 30854980]
[3]
Tumminia, A.; Vinciguerra, F.; Parisi, M.; Frittitta, L. Type 2 diabetes mellitus and Alzheimer’s disease: Role of insulin signalling and therapeutic implications. Int. J. Mol. Sci., 2018, 19(11), 3306.
[http://dx.doi.org/10.3390/ijms19113306] [PMID: 30355995]
[4]
Ahmad, W.; Ijaz, B.; Shabbiri, K.; Ahmed, F.; Rehman, S. Oxidative toxicity in diabetes and Alzheimer’s disease: Mechanisms behind ROS/RNS generation. J. Biomed. Sci., 2017, 24(1), 76.
[http://dx.doi.org/10.1186/s12929-017-0379-z] [PMID: 28927401]
[5]
de Matos, A.M.; de Macedo, M.P.; Rauter, A.P. Bridging type 2 diabetes and Alzheimer’s disease: Assembling the puzzle pieces in the quest for the molecules with therapeutic and preventive potential. Med. Res. Rev., 2018, 38(1), 261-324.
[http://dx.doi.org/10.1002/med.21440] [PMID: 28422298]
[6]
Movassat, J.; Delangre, E.; Liu, J.; Gu, Y.; Janel, N. Hypothesis and theory: Circulating Alzheimer’s-related biomarkers in type 2 diabetes. Insight from the Goto-Kakizaki rat. Front. Neurol., 2019, 10, 649.
[http://dx.doi.org/10.3389/fneur.2019.00649] [PMID: 31293498]
[7]
Rorbach-Dolata, A.; Piwowar, A. Neurometabolic evidence supporting the hypothesis of increased incidence of type 3 diabetes mellitus in the 21st century. BioMed Res. Int., 2019, 2019, 1435276.
[http://dx.doi.org/10.1155/2019/1435276] [PMID: 31428627]
[8]
Baekkeskov, S.; Aanstoot, H.J.; Christgau, S.; Reetz, A.; Solimena, M.; Cascalho, M.; Folli, F.; Richter-Olesen, H.; De Camilli, P. Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature, 1990, 347(6289), 151-156.
[http://dx.doi.org/10.1038/347151a0] [PMID: 1697648]
[9]
Noble, E.E.; Billington, C.J.; Kotz, C.M.; Wang, C. The lighter side of BDNF. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2011, 300(5), R1053-R1069.
[http://dx.doi.org/10.1152/ajpregu.00776.2010] [PMID: 21346243]
[10]
Otter, S.; Lammert, E. Exciting times for pancreatic islets: Glutamate signaling in endocrine cells. Trends Endocrinol. Metab., 2016, 27(3), 177-188.
[http://dx.doi.org/10.1016/j.tem.2015.12.004] [PMID: 26740469]
[11]
Heinis, M.; Simon, M.T.; Ilc, K.; Mazure, N.M.; Pouysségur, J.; Scharfmann, R.; Duvillié, B. Oxygen tension regulates pancreatic beta-cell differentiation through hypoxia-inducible factor 1alpha. Diabetes, 2010, 59(3), 662-669.
[http://dx.doi.org/10.2337/db09-0891] [PMID: 20009089]
[12]
Cheng, K.; Ho, K.; Stokes, R.; Scott, C.; Lau, S.M.; Hawthorne, W.J.; O’Connell, P.J.; Loudovaris, T.; Kay, T.W.; Kulkarni, R.N.; Okada, T.; Wang, X.L.; Yim, S.H.; Shah, Y.; Grey, S.T.; Biankin, A.V.; Kench, J.G.; Laybutt, D.R.; Gonzalez, F.J.; Kahn, C.R.; Gunton, J.E. Hypoxia-inducible factor-1alpha regulates beta cell function in mouse and human islets. J. Clin. Invest., 2010, 120(6), 2171-2183.
[http://dx.doi.org/10.1172/JCI35846] [PMID: 20440072]
[13]
Atouf, F.; Czernichow, P.; Scharfmann, R. Expression of neuronal traits in pancreatic beta cells. Implication of neuron-restrictive silencing factor/repressor element silencing transcription factor, a neuron-restrictive silencer. J. Biol. Chem., 1997, 272(3), 1929-1934.
[http://dx.doi.org/10.1074/jbc.272.3.1929] [PMID: 8999882]
[14]
Polak, M.; Scharfmann, R.; Seilheimer, B.; Eisenbarth, G.; Dressler, D.; Verma, I.M.; Potter, H. Nerve growth factor induces neuron-like differentiation of an insulin-secreting pancreatic beta cell line. Proc. Natl. Acad. Sci. USA, 1993, 90(12), 5781-5785.
[http://dx.doi.org/10.1073/pnas.90.12.5781] [PMID: 8516328]
[15]
Bathina, S.; Das, U.N. Brain-derived neurotrophic factor and its clinical implications. Arch. Med. Sci., 2015, 11(6), 1164-1178.
[http://dx.doi.org/10.5114/aoms.2015.56342] [PMID: 26788077]
[16]
Cruz, S.A.; Tseng, Y.C.; Kaiya, H.; Hwang, P.P. Ghrelin affects carbohydrate-glycogen metabolism via insulin inhibition and glucagon stimulation in the zebrafish (DANIO RERIO) brain. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2010, 156(2), 190-200.
[http://dx.doi.org/10.1016/j.cbpa.2010.01.019] [PMID: 20138234]
[17]
Fontaine, J.; Le Lièvre, C.; Le Douarin, N.M. What is the developmental fate of the neural crest cells which migrate into the pancreas in the avian embryo? Gen. Comp. Endocrinol., 1977, 33(3), 394-404.
[http://dx.doi.org/10.1016/0016-6480(77)90055-7] [PMID: 924129]
[18]
Jensen, J. Gene regulatory factors in pancreatic development. Dev. Dyn., 2004, 229(1), 176-200.
[http://dx.doi.org/10.1002/dvdy.10460] [PMID: 14699589]
[19]
Arntfield, M.E.; van der Kooy, D. β-Cell evolution: How the pancreas borrowed from the brain: The shared toolbox of genes expressed by neural and pancreatic endocrine cells may reflect their evolutionary relationship. BioEssays, 2011, 33(8), 582-587.
[http://dx.doi.org/10.1002/bies.201100015] [PMID: 21681773]
[20]
Han, Y.F.; Holscher, C.; Wang, Z.J.; Zhang, J.; Yuan, L.; Tong, J.Q.; Wang, D.D.; Wu, M.N.; Qi, J.S. Neuroprotective effects of a novel antidiabetic drug (D-Ser2)Oxm on amyloid β protein-induced cytotoxicity. Sheng Li Xue Bao, 2016, 68(3), 265-275.
[PMID: 27350199]
[21]
Femminella, G.D.; Frangou, E.; Love, S.B.; Busza, G.; Holmes, C.; Ritchie, C.; Lawrence, R.; McFarlane, B.; Tadros, G.; Ridha, B.H.; Bannister, C.; Walker, Z.; Archer, H.; Coulthard, E.; Underwood, B.R.; Prasanna, A.; Koranteng, P.; Karim, S.; Junaid, K.; McGuinness, B.; Nilforooshan, R.; Macharouthu, A.; Donaldson, A.; Thacker, S.; Russell, G.; Malik, N.; Mate, V.; Knight, L.; Kshemendran, S.; Harrison, J.; Hölscher, C.; Brooks, D.J.; Passmore, A.P.; Ballard, C.; Edison, P. Evaluating the effects of the novel GLP-1 analogue liraglutide in Alzheimer’s disease: Study protocol for a randomised controlled trial (ELAD study). Trials, 2019, 20(1), 191.
[http://dx.doi.org/10.1186/s13063-019-3259-x] [PMID: 30944040]
[22]
Isik, A.T.; Soysal, P.; Yay, A.; Usarel, C. The effects of sitagliptin, a DPP-4 inhibitor, on cognitive functions in elderly diabetic patients with or without Alzheimer’s disease. Diabetes Res. Clin. Pract., 2017, 123, 192-198.
[http://dx.doi.org/10.1016/j.diabres.2016.12.010] [PMID: 28056430]
[23]
Kornelius, E.; Lin, C.L.; Chang, H.H.; Li, H.H.; Huang, W.N.; Yang, Y.S.; Lu, Y.L.; Peng, C.H.; Huang, C.N. DPP-4 inhibitor linagliptin attenuates abeta-induced cytotoxicity through activation of AMPK in neuronal cells. CNS Neurosci. Ther., 2015, 21(7), 549-557.
[http://dx.doi.org/10.1111/cns.12404] [PMID: 26010513]
[24]
Lu, J.; Xu, Z. Efficacy of intranasal insulin in improving cognition in mild cognitive impairment and Alzheimer disease: A systematic review and meta-analysis. Am. J. Ther., 2019, 26(6), e756-e762.
[http://dx.doi.org/10.1097/MJT.0000000000000926] [PMID: 30648990]
[25]
Imai, R.; Misaka, S.; Horita, S.; Yokota, S.; O’hashi, R.; Maejima, Y.; Shimomura, K. Memantine has no effect on KATP channels in pancreatic β cells. BMC Res. Notes, 2018, 11(1), 614.
[http://dx.doi.org/10.1186/s13104-018-3715-9] [PMID: 30144824]
[26]
Ebrahimpour, S.; Zakeri, M.; Esmaeili, A. Crosstalk between obesity, diabetes, and alzheimer’s disease: Introducing quercetin as an effective triple herbal medicine. Ageing Res. Rev., 2020, 62, 101095.
[http://dx.doi.org/10.1016/j.arr.2020.101095] [PMID: 32535272]
[27]
Ostrovskaya, R.U.; Vakhitova, Y.V.; Kuzmina, U.Sh.; Salimgareeva, M.Kh.; Zainullina, L.F.; Gudasheva, T.A.; Vakhitov, V.A.; Seredenin, S.B. Neuroprotective effect of novel cognitive enhancer noopept on AD-related cellular model involves the attenuation of apoptosis and tau hyperphosphorylation. J. Biomed. Sci., 2014, 21(1), 74.
[http://dx.doi.org/10.1186/s12929-014-0074-2] [PMID: 25096780]
[28]
Ostrovskaya, R.U.; Zolotov, N.N.; Ozerova, I.V.; Ivanova, E.A.; Kapitsa, I.G.; Taraban, K.V.; Michunskaya, A.M.; Voronina, T.A.; Gudasheva, T.A.; Seredenin, S.B. Noopept normalizes parameters of the incretin system in rats with experimental diabetes. Bull. Exp. Biol. Med., 2014, 157(3), 344-349.
[http://dx.doi.org/10.1007/s10517-014-2562-5] [PMID: 25065315]
[29]
Lysenko, A.V.; Uskova, N.I.; Ostrovskaia, R.U.; Gudasheva, T.A.; Voronina, T.A. Dipeptide nootropic agent GVS-111 prevents accumulation of the lipid peroxidation products during immobilization. Eksp. Klin. Farmakol., 1997, 60(5), 15-18.
[PMID: 9483398]
[30]
Andreeva, N.A.; Stel’mashuk, E.V.; Isaev, N.K.; Ostrovskaya, R.U.; Gudasheva, T.A.; Viktorov, I.V. Neuroprotective properties of nootropic dipeptide GVS-111 in in vitro oxygen-glucose deprivation, glutamate toxicity and oxidative stress. Bull. Exp. Biol. Med., 2000, 130(10), 969-972.
[http://dx.doi.org/10.1023/A:1002828707337] [PMID: 11177296]
[31]
Ostrovskaya, R.U.; Gudasheva, T.A.; Zaplina, A.P.; Vahitova, J.V.; Salimgareeva, M.H.; Jamidanov, R.S.; Seredenin, S.B. Noopept stimulates the expression of NGF and BDNF in rat hippocampus. Bull. Exp. Biol. Med., 2008, 146(3), 334-337.
[http://dx.doi.org/10.1007/s10517-008-0297-x] [PMID: 19240853]
[32]
Ostrovskaya, R.U.; Antipova, T.A.; Nikolaev, S.V.; Kruglov, S.V.; Ozerova, I.V.; Gudasheva, T.A.; Seredenin, S.B. Deficit of neurotrophins in experimental diabetes – correction with a proline-containing dipeptide. Neurosci. Behav. Physiol., 2019, 49(7), 809-815.
[http://dx.doi.org/10.1007/s11055-019-00806-z]
[33]
Gudasheva, T.A.; Povarnina, P.Y.; Tarasiuk, A.V.; Seredenin, S.B. Low-molecular mimetics of nerve growth factor and brain-derived neurotrophic factor: Design and pharmacological properties. Med. Res. Rev., 2020.
[http://dx.doi.org/10.1002/med.21721] [PMID: 32808322]
[34]
Behensky, A.A.; Katnik, C.; Yin, H.; Cuevas, J. Activation of sigma receptors with Afobazole modulates microglial, but not neuronal, apoptotic gene expression in response to long-term ischemia exposure. Front. Neurosci., 2019, 13, 414.
[http://dx.doi.org/10.3389/fnins.2019.00414] [PMID: 31156357]
[35]
Khairova, R.; Pawar, R.; Salvadore, G.; Juruena, M.F.; de Sousa, R.T.; Soeiro-de-Souza, M.G.; Salvador, M.; Zarate, C.A.; Gattaz, W.F.; Machado-Vieira, R. Effects of lithium on oxidative stress parameters in healthy subjects. Mol. Med. Rep., 2012, 5(3), 680-682.
[PMID: 22200861]
[36]
Dwivedi, T.; Zhang, H. Lithium-induced neuroprotection is associated with epigenetic modification of specific BDNF gene promoter and altered expression of apoptotic-regulatory proteins. Front. Neurosci., 2015, 8(157), 457.
[http://dx.doi.org/10.3389/fnins.2014.00457] [PMID: 25642163]
[37]
Ma, J.; Liu, J.; Yu, H.; Chen, Y.; Wang, Q.; Xiang, L. Effect of metformin on Schwann cells under hypoxia condition. Int. J. Clin. Exp. Pathol., 2015, 8(6), 6748-6755.
[PMID: 26261558]
[38]
Moon, J.S.; Karunakaran, U.; Elumalai, S.; Lee, I.K.; Lee, H.W.; Kim, Y.W.; Won, K.C. Metformin prevents glucotoxicity by alleviating oxidative and ER stress-induced CD36 expression in pancreatic beta cells. J. Diab. Compl., 2017, 31(1), 21-30.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.09.001] [PMID: 27662780]
[39]
Bonner-Weir, S. beta-cell turnover: Its assessment and implications. Diabetes, 2001, 50(1)(Suppl. 1), S20-S24.
[http://dx.doi.org/10.2337/diabetes.50.2007.S20] [PMID: 11272192]
[40]
Gezginci-Oktayoglu, S.; Bolkent, S. Ras signaling in NGF reduction and TNF-α-related pancreatic β cell apoptosis in hyperglycemic rats. Apoptosis, 2012, 17(1), 14-24.
[http://dx.doi.org/10.1007/s10495-011-0657-2] [PMID: 21938476]
[41]
Vidaltamayo, R.; Mery, C.M.; Angeles-Angeles, A.; Robles-Díaz, G.; Hiriart, M. Expression of nerve growth factor in human pancreatic beta cells. Growth Factors, 2003, 21(3-4), 103-107.
[http://dx.doi.org/10.1080/08977190310001629566] [PMID: 14708938]
[42]
Seredenin, S.B.; Gudasheva, T.A. Dipeptide mimetics of NGF and BDNF neurotrophins. US Patent 9683014 B2, 2017.
[43]
Gudasheva, T.A.; Povarnina, P.Y.; Antipova, T.A.; Firsova, Y.N.; Konstantinopolsky, M.A.; Seredenin, S.B. Dimeric dipeptide mimetics of the nerve growth factor Loop 4 and Loop 1 activate TRKA with different patterns of intracellular signal transduction. J. Biomed. Sci., 2015, 22(1), 106.
[http://dx.doi.org/10.1186/s12929-015-0198-z] [PMID: 26642930]
[44]
Ozerova, I.V.; Povarnina, P.Iu.; Ostrovskaia, R.U.; Gudasheva, T.A.; Voronina, T.A.; Seredin, S.B. The efficacy of human NGF dipeptide mimetic on the streptozotocin-induced model of diabetes in rats. Eksp. Klin. Farmakol., 2013, 76(5), 10-13.
[PMID: 23901462]
[45]
Povarnina, P.Y.; Ozerova, I.V.; Ostrovskaya, R.U.; Gudasheva, T.A.; Seredenin, S.B. Antidiabetic activity of a novel dipeptide mimetic of nerve growth factor. Dokl. Biol. Sci., 2013, 449(1), 76-78.
[http://dx.doi.org/10.1134/S001249661302004X] [PMID: 23652431]
[46]
Cho, J.H.; Kim, J.W.; Shin, J.A.; Shin, J.; Yoon, K.H. β-cell mass in people with type 2 diabetes. J. Diabetes Investig., 2011, 2(1), 6-17.
[http://dx.doi.org/10.1111/j.2040-1124.2010.00072.x] [PMID: 24843456]
[47]
Ostrovskaya, R.U.; Ivanov, S.V.; Gudasheva, T.A.; Seredenin, S.B. A novel dipeptide NGF mimetic GK-2 selectively activating the PI3K/AKT signaling pathway promotes the survival of pancreatic β-cells in a rat model of diabetes. Acta Nat. (Engl. Ed.), 2019, 11(1), 48-57.
[http://dx.doi.org/10.32607/20758251-2019-11-1-48-57] [PMID: 31024748]
[48]
Ostrovskaya, R.U.; Ivanov, S.V.; Gudasheva, T.A.; Seredenin, S.B. A low molecular weight nerve growth factor (NGF) mimetic given per os increases the survival of pancreatic b-cells in a streptozotocin model of diabetes. Pharm. Chem. J., 2019, 53(7), 589-592.
[http://dx.doi.org/10.1007/s11094-019-02043-7]
[49]
Seredenin, S.B.; Ostrovskaya, R.U.; Voronina, T.A.; Zolotov, N.N.; Yarkova, M.A.; Durnev, A.D. Medicines for the prevention and treatment of diabetes. RU Patent 2597848, 2016.
[50]
Zabrodina, V.V.; Shreder, E.D.; Shreder, O.V.; Durnev, A.D.; Seredenin, S.B. Impaired prenatal development and glycemic status in the offspring of rats with experimental streptozotocin-induced diabetes and their correction with afobazole. Bull. Exp. Biol. Med., 2014, 158(1), 16-20.
[http://dx.doi.org/10.1007/s10517-014-2681-z] [PMID: 25403388]
[51]
Ostrovskaya, R.U.; Ivanov, S.V.; Voronin, M.V.; Ozerova, I.V.; Zolotov, N.N.; Seredenin, S.B. Antidiabetic activity of afobazole in Wistar rats. Bull. Exp. Biol. Med., 2018, 165(5), 649-652.
[http://dx.doi.org/10.1007/s10517-018-4233-4] [PMID: 30225697]
[52]
Ivanov, S.V.; Ostrovskaya, R.U.; Sorokina, A.V.; Seredenin, S.B. Analysis of cytoprotective properties of afobazole in streptozotocin model of diabetes. Bull. Exp. Biol. Med., 2020, 169(6), 783-786.
[http://dx.doi.org/10.1007/s10517-020-04978-4] [PMID: 33098515]
[53]
Woodgett, J.R. Physiological roles of glycogen synthase kinase-3: Potential as a therapeutic target for diabetes and other disorders. Curr. Drug Targets Immune Endocr. Metabol. Disord., 2003, 3(4), 281-290.
[http://dx.doi.org/10.2174/1568008033340153] [PMID: 14683459]
[54]
Ostrovskaya, R.U.; Ivanov, S.V.; Durnev, A.D. Neuroprotective lithium salts protect pancreatic β-cells from damage. Bull. Exp. Biol. Med., 2018, 165(6), 758-762.
[http://dx.doi.org/10.1007/s10517-018-4259-7] [PMID: 30353339]
[55]
Piro, S.; Rabuazzo, A.M.; Renis, M.; Purrello, F. Effects of metformin on oxidative stress, adenine nucleotides balance, and glucose-induced insulin release impaired by chronic free fatty acids exposure in rat pancreatic islets. J. Endocrinol. Invest., 2012, 35(5), 504-510.
[PMID: 21750398]
[56]
Lamontagne, J.; Al-Mass, A.; Nolan, C.J.; Corkey, B.E.; Madiraju, S.R.M.; Joly, E.; Prentki, M. Identification of the signals for glucose-induced insulin secretion in INS1 (832/13) β-cells using metformin-induced metabolic deceleration as a model. J. Biol. Chem., 2017, 292(47), 19458-19468.
[http://dx.doi.org/10.1074/jbc.M117.808105] [PMID: 28972173]
[57]
Huang, H.; Lorenz, B.R.; Zelmanovitz, P.H.; Chan, C.B. Metformin preserves β-cell compensation in insulin secretion and mass expansion in prediabetic nile rats. Int. J. Mol. Sci., 2021, 22(1), 421.
[http://dx.doi.org/10.3390/ijms22010421] [PMID: 33401592]
[58]
Tajima, K.; Shirakawa, J.; Okuyama, T.; Kyohara, M.; Yamazaki, S.; Togashi, Y.; Terauchi, Y. Effects of metformin on compensatory pancreatic β-cell hyperplasia in mice fed a high-fat diet. Am. J. Physiol. Endocrinol. Metab., 2017, 313(3), E367-E380.
[http://dx.doi.org/10.1152/ajpendo.00447.2016] [PMID: 28512156]
[59]
Rolo, A.P.; Palmeira, C.M. Diabetes and mitochondrial function: Role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol., 2006, 212(2), 167-178.
[http://dx.doi.org/10.1016/j.taap.2006.01.003] [PMID: 16490224]
[60]
Ighodaro, O.M. Molecular pathways associated with oxidative stress in diabetes mellitus. Biomed. Pharmacother., 2018, 108, 656-662.
[http://dx.doi.org/10.1016/j.biopha.2018.09.058] [PMID: 30245465]
[61]
Al-Gayyar, M.M.; Mysona, B.A.; Matragoon, S.; Abdelsaid, M.A.; El-Azab, M.F.; Shanab, A.Y.; Ha, Y.; Smith, S.B.; Bollinger, K.E.; El-Remessy, A.B. Diabetes and overexpression of proNGF cause retinal neurodegeneration via activation of RhoA pathway. PLoS One, 2013, 8(1), e54692.
[http://dx.doi.org/10.1371/journal.pone.0054692] [PMID: 23365678]
[62]
Garofalo, R.S.; Orena, S.J.; Rafidi, K.; Torchia, A.J.; Stock, J.L.; Hildebrandt, A.L.; Coskran, T.; Black, S.C.; Brees, D.J.; Wicks, J.R.; McNeish, J.D.; Coleman, K.G. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J. Clin. Invest., 2003, 112(2), 197-208.
[http://dx.doi.org/10.1172/JCI16885] [PMID: 12843127]
[63]
Lenart, L.; Hodrea, J.; Hosszu, A.; Koszegi, S.; Zelena, D.; Balogh, D.; Szkibinszkij, E.; Veres-Szekely, A.; Wagner, L.; Vannay, A.; Szabo, A.J.; Fekete, A. The role of sigma-1 receptor and brain-derived neurotrophic factor in the development of diabetes and comorbid depression in streptozotocin-induced diabetic rats. Psychopharmacology (Berl.), 2016, 233(7), 1269-1278.
[http://dx.doi.org/10.1007/s00213-016-4209-x] [PMID: 26809458]
[64]
Colabufo, N.A.; Berardi, F.; Abate, C.; Contino, M.; Niso, M.; Perrone, R. Is the sigma2 receptor a histone binding protein? J. Med. Chem., 2006, 49(14), 4153-4158.
[http://dx.doi.org/10.1021/jm0600592] [PMID: 16821775]
[65]
Hayashi, T.; Su, T.P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell, 2007, 131(3), 596-610.
[http://dx.doi.org/10.1016/j.cell.2007.08.036] [PMID: 17981125]
[66]
Naganawa, M.; Lin, S.F.; Lim, K.; Labaree, D.; Ropchan, J.; Harris, P.; Huang, Y.; Ichise, M.; Carson, R.E.; Cline, G.W. Evaluation of pancreatic VMAT2 binding with active and inactive enantiomers of 18F-FP-DTBZ in baboons. Nucl. Med. Biol., 2016, 43(12), 743-751.
[http://dx.doi.org/10.1016/j.nucmedbio.2016.08.018] [PMID: 27673755]
[67]
Tsao, H.H.; Skovronsky, D.M.; Lin, K.J.; Yen, T.C.; Wey, S.P.; Kung, M.P. Sigma receptor binding of tetrabenazine series tracers targeting VMAT2 in rat pancreas. Nucl. Med. Biol., 2011, 38(7), 1029-1034.
[http://dx.doi.org/10.1016/j.nucmedbio.2011.03.006] [PMID: 21982574]
[68]
Jope, R.S.; Johnson, G.V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci., 2004, 29(2), 95-102.
[http://dx.doi.org/10.1016/j.tibs.2003.12.004] [PMID: 15102436]
[69]
Feng, Z.C.; Donnelly, L.; Li, J.; Krishnamurthy, M.; Riopel, M.; Wang, R. Inhibition of Gsk3β activity improves β-cell function in c-KitWv/+ male mice. Lab. Invest., 2012, 92(4), 543-555.
[http://dx.doi.org/10.1038/labinvest.2011.200] [PMID: 22249311]
[70]
Liu, Z.; Tanabe, K.; Bernal-Mizrachi, E.; Permutt, M.A. Mice with beta cell overexpression of glycogen synthase kinase-3beta have reduced beta cell mass and proliferation. Diabetologia, 2008, 51(4), 623-631.
[http://dx.doi.org/10.1007/s00125-007-0914-7] [PMID: 18219478]
[71]
Szkudelski, T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol. Res., 2001, 50(6), 537-546.
[PMID: 11829314]
[72]
Ring, D.B.; Johnson, K.W.; Henriksen, E.J.; Nuss, J.M.; Goff, D.; Kinnick, T.R.; Ma, S.T.; Reeder, J.W.; Samuels, I.; Slabiak, T.; Wagman, A.S.; Hammond, M.E.; Harrison, S.D. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes, 2003, 52(3), 588-595.
[http://dx.doi.org/10.2337/diabetes.52.3.588] [PMID: 12606497]
[73]
Povarnina, P.Y.; Vorontsova, O.N.; Gudasheva, T.A.; Ostrovskaya, R.U.; Seredenin, S.B. Original nerve growth factor mimetic dipeptide GK-2 restores impaired cognitive functions in rat models of Alzheimer’s disease. Acta Nat. (Engl. Ed.), 2013, 5(3), 84-91.
[http://dx.doi.org/10.32607/20758251-2013-5-3-84-91] [PMID: 24303204]
[74]
Rosenbaum, T.; Vidaltamayo, R.; Sánchez-Soto, M.C.; Zentella, A.; Hiriart, M. Pancreatic beta cells synthesize and secrete nerve growth factor. Proc. Natl. Acad. Sci. USA, 1998, 95(13), 7784-7788.
[http://dx.doi.org/10.1073/pnas.95.13.7784] [PMID: 9636228]
[75]
Seredenin, S.B.; Antipova, T.A.; Voronin, M.V.; Kurchashova, S.Y.; Kuimov, A.N. Interaction of afobazole with sigma1-receptors. Bull. Exp. Biol. Med., 2009, 148(1), 42-44.
[http://dx.doi.org/10.1007/s10517-009-0624-x] [PMID: 19902093]
[76]
Nguyen, L.; Lucke-Wold, B.P.; Mookerjee, S.; Kaushal, N.; Matsumoto, R.R. Sigma-1 receptors and neurodegenerative diseases: Towards a hypothesis of sigma-1 receptors as amplifiers of neurodegeneration and neuroprotection. Adv. Exp. Med. Biol., 2017, 964, 133-152.
[http://dx.doi.org/10.1007/978-3-319-50174-1_10] [PMID: 28315269]
[77]
Voronin, M.V.; Kadnikov, I.A.; Voronkov, D.N.; Seredenin, S.B. Chaperone sigma1R mediates the neuroprotective action of afobazole in the 6-OHDA model of Parkinson’s disease. Sci. Rep., 2019, 9(1), 17020.
[http://dx.doi.org/10.1038/s41598-019-53413-w] [PMID: 31745133]
[78]
Antipova, T.A.; Sapozhnikova, D.S.; Bakhtina, L.Iu.; Seredenin, S.B. Selective anxiolytic afobazole increases the content of BDNF and NGF in cultured hippocampal HT-22 line neurons. Eksp. Klin. Farmakol., 2009, 72(1), 12-14.
[PMID: 19334503]
[79]
Katnik, C.; Garcia, A.; Behensky, A.A.; Yasny, I.E.; Shuster, A.M.; Seredenin, S.B.; Petrov, A.V.; Cuevas, J. Activation of σ1 and σ2 receptors by afobazole increases glial cell survival and prevents glial cell activation and nitrosative stress after ischemic stroke. J. Neurochem., 2016, 139(3), 497-509.
[http://dx.doi.org/10.1111/jnc.13756] [PMID: 27488244]
[80]
Nadeem, R.I.; Ahmed, H.I.; El-Denshary, E.E. Effect of imipramine, paroxetine, and lithium carbonate on neurobehavioral changes of streptozotocin in rats: Impact on glycogen synthase kinase-3 and blood glucose level. Neurochem. Res., 2015, 40(9), 1810-1818.
[http://dx.doi.org/10.1007/s11064-015-1670-6] [PMID: 26216050]
[81]
De-Paula, V.J.; Gattaz, W.F.; Forlenza, O.V. Long-term lithium treatment increases intracellular and extracellular brain-derived neurotrophic factor (BDNF) in cortical and hippocampal neurons at subtherapeutic concentrations. Bipolar Disord., 2016, 18(8), 692-695.
[http://dx.doi.org/10.1111/bdi.12449] [PMID: 27882645]
[82]
Li, W.A.; Moore-Langston, S.; Chakraborty, T.; Rafols, J.A.; Conti, A.C.; Ding, Y. Hyperglycemia in stroke and possible treatments. Neurol. Res., 2013, 35(5), 479-491.
[http://dx.doi.org/10.1179/1743132813Y.0000000209] [PMID: 23622737]
[83]
Kahn, L.S.; McIntyre, R.S.; Rafalson, L.; Berdine, D.E.; Fox, C.H. Fasting blood glucose and depressive mood among patients with mental illness in a medicaid managed care program. Depress. Res. Treat., 2011, 2011, 862708.
[http://dx.doi.org/10.1155/2011/862708] [PMID: 21738870]

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