Up-regulation of insulin-like growth factor 2 by ketamine requires glycogen synthase kinase-3 inhibition

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 72, Issue , 2017, Pages 49-54

  Grieco, Steven F ^a   Cheng, Yuyan ^a   Eldar Finkelman, Hagit ^b   Jope, Richard S ^a   Beurel, Eléonore ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Depression; Glycogen synthase kinase 3; Hippocampus; Insulin like growth factor 2; Ketamine; Learned helplessness

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; KETAMINE; L 803 MTS; MESSENGER RNA; SMALL INTERFERING RNA; SOMATOMEDIN B; UNCLASSIFIED DRUG; ANTIDEPRESSANT AGENT; N-MYRISTOYL-GLYCYL-LYSYL-GLUTAMYL-ALANYL-PROLYL-PROLYL-ALANYL-PROLYL-PROLYL-GLUTAMINYL-PHOSPHOSERYL-PROLINE; OLIGOPEPTIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOSE RESPONSE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LEARNED HELPLESSNESS; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE DISTRIBUTION; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; SEXUAL DEVELOPMENT;

ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HELPLESSNESS, LEARNED; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR II; KETAMINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGOPEPTIDES; RNA, MESSENGER; RNA, SMALL INTERFERING; SEX CHARACTERISTICS; UP-REGULATION;

EID: 84983801468     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2016.08.008     Document Type: Article

References (41)

1. Åberg, D., Johansson, P., Isgaard, J., Wallin, A., Johansson, J.O., Andreasson, U., Blennow, K., Zetterberg, H., Åberg, N.D., Svensson, J., Increased cerebrospinal fluid level of insulin-like growth factor-II in male patients with Alzheimer's disease. J. Alzheimers Dis. 48 (2015), 637–646.
2. Andrus, B.M., Blizinsky, K., Vedell, P.T., Dennis, K., Shukla, P.K., Schaffer, D.J., Radulovic, J., Churchill, G.A., Redei, E.E., Gene expression patterns in the hippocampus and amygdala of endogenous depression and chronic stress models. Mol. Psychiatry 17 (2012), 49–61.
3. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., Kavalali, E.T., Monteggia, L.M., NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475 (2011), 91–95.
4. Beurel, E., Song, L., Jope, R.S., Inhibition of glycogen synthase kinase-3 is necessary for the rapid antidepressant effect of ketamine in mice. Mol. Psychiatry 16 (2011), 1068–1070.
5. Beurel, E., Kaidanovich-Beilin, O., Yeh, W.I., Song, L., Palomo, V., Michalek, S.M., Woodgett, J.R., Harrington, L.E., Eldar-Finkelman, H., Martinez, A., Jope, R.S., Regulation of Th1 cells and experimental autoimmune encephalomyelitis by glycogen synthase kinase-3. J. Immunol. 190 (2013), 5000–5011.
6. Beurel, E., Harrington, L.E., Jope, R.S., Inflammatory T helper 17 cells promote depression-like behavior in mice. Biol. Psychiatry 73 (2013), 622–630.
7. Beurel, E., Grieco, S.F., Jope, R.S., Glycogen synthase kinase-3 (GSK3): Regulation, actions, and diseases. Pharmacol. Ther. 148 (2015), 114–131.
8. Bracko, O., Singer, T., Aigner, S., Knobloch, M., Winner, B., Ray, J., Clemenson, G.D. Jr., Suh, H., Couillard-Despres, S., Aigner, L., Gage, F.H., Jessberger, S., Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J. Neurosci. 32 (2012), 3376–3387.
9. Caracausi, M., Rigon, V., Piovesan, A., Strippoli, P., Vitale, L., Pelleri, M.C., A quantitative transcriptome reference map of the normal human hippocampus. Hippocampus 26 (2016), 13–26.
10. Chen, H., Tung, Y.C., Li, B., Iqbal, K., Grundke-Iqbal, I., Trophic factors counteract elevated FGF-2-induced inhibition of adult neurogenesis. Neurobiol. Aging 28 (2007), 1148–1162.
11. Chiu C.T., Scheuing L., Liu G., Liao H.M., Linares G.R., Lin D., Chuang D.M., 2014. The mood stabilizer lithium potentiates the antidepressant-like effects and ameliorates oxidative stress induced by acute ketamine in a mouse model of stress. Int J Neuropsychopharmacol. 18 (6), pii: pyu102.
12. Cline, B.H., Steinbusch, H.W., Malin, D., Revishchin, A.V., Pavlova, G.V., Cespuglio, R., Strekalova, T., The neuronal insulin sensitizer dicholine succinate reduces stress-induced depressive traits and memory deficit: Possible role of insulin-like growth factor 2. BMC Neurosci., 13, 2012, 110.
13. Córdova-Palomera, A., Fatjó-Vilas, M., Gastó, C., Navarro, V., Krebs, M.O., Fañanás, L., Genome-wide methylation study on depression: Differential methylation and variable methylation in monozygotic twins. Transl. Psychiatry, 5, 2015, e557.
14. Eom, T.Y., Jope, R.S., Blocked inhibitory serine-phosphorylation of glycogen synthase kinase-3alpha/beta impairs in vivo neural precursor cell proliferation. Biol. Psychiatry 66 (2009), 494–502.
15. Ferrón, S.R., Radford, E.J., Domingo-Muelas, A., Kleine, I., Ramme, A., Gray, D., Sandovici, I., Constancia, M., Ward, A., Menheniott, T.R., Ferguson-Smith, A.C., Differential genomic imprinting regulates paracrine and autocrine roles of IGF2 in mouse adult neurogenesis. Nat. Commun., 6, 2015, 8265.
16. Ghasemi, M., Raza, M., Dehpour, A.R., NMDA receptor antagonists augment antidepressant-like effects of lithium in the mouse forced swimming test. J. Psychopharmacol. 24 (2010), 585–594.
17. Kaidanovich-Beilin, O., Milman, A., Weizman, A., Pick, C.G., Eldar-Finkelman, H., Rapid antidepressive-like activity of specific glycogen synthase kinase-3 inhibitor and its effect on beta-catenin in mouse hippocampus. Biol. Psychiatry 55 (2004), 781–784.
18. Kita, Y., Ago, Y., Higashino, K., Asada, K., Takano, E., Takuma, K., Matsuda, T., Galantamine promotes adult hippocampal neurogenesis via M₁ muscarinic and α7 nicotinic receptors in mice. Int. J. Neuropsychopharmacol. 17 (2014), 1957–1968.
19. Lauterio, T.J., Rieg, T.S., Ahmed, I., Aravich, P.F., Fluoxetine induced insulin-like growth factor II (IGF-II) changes in hypothalami of normal, exercised and food restricted rats. Regul. Pept. 48 (1993), 21–28.
20. Li, N., Lee, B., Liu, R.J., Banasr, M., Dwyer, J.M., Iwata, M., Li, X.Y., Aghajanian, G., Duman, R.S., mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329 (2010), 959–964.
21. Lisowski, P., Juszczak, G.R., Goscik, J., Stankiewicz, A.M., Wieczorek, M., Zwierzchowski, L., Swiergiel, A.H., Stress susceptibility-specific phenotype associated with different hippocampal transcriptomic responses to chronic tricyclic antidepressant treatment in mice. BMC Neurosci., 14, 2013, 144.
22. Liu, R.J., Fuchikami, M., Dwyer, J.M., Lepack, A.E., Duman, R.S., Aghajanian, G.K., GSK-3 inhibition potentiates the synaptogenic and antidepressant-like effects of subthreshold doses of ketamine. Neuropsychopharmacology 38 (2013), 2268–2277.
23. Luo, Y.W., Xu, Y., Cao, W.Y., Zhong, X.L., Duan, J., Wang, X.Q., Hu, Z.L., Li, F., Zhang, J.Y., Zhou, M., Dai, R.P., Li, C.Q., Insulin-like growth factor 2 mitigates depressive behavior in a rat model of chronic stress. Neuropharmacology 89 (2015), 318–324.
24. Maeng, S., Zarate, C.A. Jr., Du, J., Schloesser, R.J., McCammon, J., Chen, G., Manji, H.K., Cellular mechanisms underlying the antidepressant effects of ketamine: Role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol. Psychiatry 63 (2008), 349–352.
25. McEwen, B.S., Gray, J., Nasca, C., Recognizing resilience: Learning from the effects of stress on the brain. Neurobiol Stress. 1 (2015), 1–11.
26. McManus, E.J., Sakamoto, K., Armit, L.J., Ronaldson, L., Shpiro, N., Marquez, R., Alessi, D.R., Role that phosphorylation of GSK3 plays in insulin and Wnt signaling defined by knockin analysis. EMBO J. 24 (2005), 1571–1583.
27. Mellott, T.J., Pender, S.M., Burke, R.M., Langley, E.A., Blusztajn, J.K., IGF2 ameliorates amyloidosis, increases cholinergic marker expression and raises BMP9 and neurotrophin levels in the hippocampus of the APPswePS1dE9 Alzheimer's disease model mice. PLoS One, 9, 2014, e94287.
28. Newport D.J., Carpenter L.L., McDonald W.M., Potash J.B., Tohen M., Nemeroff C.B.; APA Council of Research Task Force on Novel Biomarkers and Treatments. 2015. Ketamine and other NMDA antagonists: Early clinical trials and possible mechanisms in depression. Am. J. Psychiatry 172, 950–966.
29. Niciu, M.J., Henter, I.D., Luckenbaugh, D.A., Zarate, C.A. Jr., Charney, D.S., Glutamate receptor antagonists as fast-acting therapeutic alternatives for the treatment of depression: Ketamine and other compounds. Annu. Rev. Pharmacol. Toxicol. 54 (2014), 119–139.
30. Plotkin, B., Kaidanovich, O., Talior, I., Eldar-Finkelman, H., Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 305 (2003), 974–980.
31. Polter, A., Beurel, E., Yang, S., Garner, R., Song, L., Miller, C.A., Sweatt, J.D., McMahon, L., Bartolucci, A.A., Li, X., Jope, R.S., Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 35 (2010), 1761–1774.
32. Sárvári, M., Kalló, I., Hrabovszky, E., Solymosi, N., Rodolosse, A., Vastagh, C., Auer, H., Liposits, Z., Hippocampal Gene expression is highly responsive to estradiol replacement in middle-aged female rats. Endocrinology 156 (2015), 2632–2645.
33. Sárvári, M., Kalló, I., Hrabovszky, E., Solymosi, N., Rodolosse, A., Liposits, Z., Long-term estrogen receptor Beta agonist treatment modifies the hippocampal transcriptome in middle-aged Ovariectomized rats. Front. Cell. Neurosci., 10, 2016, 149.
34. Takeo, C., Ikeda, K., Horie-Inoue, K., Inoue, S., Identification of Igf2, Igfbp2 and Enpp2 as estrogen-responsive genes in rat hippocampus. Endocr J. 56 (2009), 113–120.
35. Scheuing, L., Chiu, C.T., Liao, H.M., Chuang, D.M., Antidepressant mechanism of ketamine: Perspective from preclinical studies. Front. Neurosci., 9, 2015, 249.
36. Tham, A., Nordberg, A., Grissom, F.E., Carlsson-Skwirut, C., Viitanen, M., Sara, V.R., Insulin-like growth factors and insulin-like growth factor binding proteins in cerebrospinal fluid and serum of patients with dementia of the Alzheimer type. J. Neural Transm. Park. Dis. Dement. Sect. 5 (1993), 165–176.
37. Wilczak, N., De Bleser, P., Luiten, P., Geerts, A., Teelken, A., De Keyser, J., Insulin-like growth factor II receptors in human brain and their absence in astrogliotic plaques in multiple sclerosis. Brain Res. 863 (2000), 282–288.
38. Yang, C., Zhou, Z.Q., Gao, Z.Q., Shi, J.Y., Yang, J.J., Acute increases in plasma mammalian target of rapamycin, glycogen synthase kinase-3β, and eukaryotic elongation factor 2 phosphorylation after ketamine treatment in three depressed patients. Biol. Psychiatry 73 (2013), e35–e36.
39. Zanos, P., Moaddel, R., Morris, P.J., Georgiou, P., Fischell, J., Elmer, G.I., Alkondon, M., Yuan, P., Pribut, H.J., Singh, N.S., Dossou, K.S., Fang, Y., Huang, X.P., Mayo, C.L., Wainer, I.W., Albuquerque, E.X., Thompson, S.M., Thomas, C.J., Zarate, C.A. Jr., Gould, T.D., NMDAR inhibition-independent antidepressant actions of ketamine metabolites. Nature 533 (2016), 481–486.
40. Zhou, W., Dong, L., Wang, N., Shi, J.Y., Yang, J.J., Zuo, Z.Y., Zhou, Z.Q., Akt mediates GSK-3β phosphorylation in the rat prefrontal cortex during the process of ketamine exerting rapid antidepressant actions. Neuroimmunomodulation, 21(183), 2014, 188.
41. Zunszain, P.A., Horowitz, M.A., Cattaneo, A., Lupi, M.M., Pariante, C.M., Ketamine: Synaptogenesis, immunomodulation and glycogen synthase kinase-3 as underlying mechanisms of its antidepressant properties. Mol. Psychiatry 8 (2013), 1236–1241.