Startseite Lebenswissenschaften Functions of adiponectin signaling in regulating neural plasticity and its application as the therapeutic target to neurological and psychiatric diseases
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Functions of adiponectin signaling in regulating neural plasticity and its application as the therapeutic target to neurological and psychiatric diseases

  • Li-na Sun und Xiao-li Liu EMAIL logo
Veröffentlicht/Copyright: 8. Januar 2019

Abstract

Convergent lines of evidence indicate the critical roles of adiponectin in regulating neural functions on different levels. Because of the importance in maintaining neural plasticity including adult neurogenesis and synaptic plasticity, adiponectin has the potential to serve as the treatment targets in therapies of neurological and psychiatric disorders. Hence, systematic review is needed to summarize how adiponectin works in the brain, and how the adiponectin pathway is employed as the treatment method needs to be determined. Moreover, the benefits of adiponectin as the regulator for neural plasticity such as synaptic plasticity and neurogenesis have been supported by many literatures. In the current article, we reviewed the functions of adiponectin in different types of neural plasticity. We also demonstrated the potential value of adiponectin as the treatment target for different types of neurodegenerative and psychiatric disorders. Taken together, this review offers a new insight about adiponectin as the ideal target to develop the new treatment methods against neurodegeneration or psychiatric diseases.

Award Identifier / Grant number: 31571221

Funding statement: This study was supported by National Natural Science Foundation of China (31571221), the China Postdoctoral Science Fund (2014M560198) and Fundamental Research Funds for the Central Universities (2018NTSS30).

  1. Conflict of interest statement: No conflict of interest exists among the authors regarding this article.

References

Aimone, J.B., Li, Y., Lee, S.W., Clemenson, G.D., Deng, W., and Gage, F.H. (2014). Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 94, 991–1026.10.1152/physrev.00004.2014Suche in Google Scholar PubMed

Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., and Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963–970.10.1038/nm747Suche in Google Scholar PubMed

Bauche, I.B., El Mkadem, S.A., Pottier, A.M., Senou, M., Many, M.C., Rezsohazy, R., Penicaud, L., Maeda, N., Funahashi, T., and Brichard, S.M. (2007). Overexpression of adiponectin targeted to adipose tissue in transgenic mice: impaired adipocyte differentiation. Endocrinology 148, 1539–1549.10.1210/en.2006-0838Suche in Google Scholar PubMed

Bayer, T.A., Wirths, O., Majtenyi, K., Hartmann, T., Multhaup, G., Beyreuther, K., and Czech, C. (2001). Key factors in Alzheimer’s disease: beta-amyloid precursor protein processing, metabolism and intraneuronal transport. Brain Pathol. 11, 1–11.10.1111/j.1750-3639.2001.tb00376.xSuche in Google Scholar PubMed

Berg, A.H., Combs, T.P., Du, X., Brownlee, M., and Scherer, P.E. (2001). The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 7, 947–953.10.1038/90992Suche in Google Scholar PubMed

Biessels, G.J., Kamal, A., Ramakers, G.M., Urban, I.J., Spruijt, B.M., Erkelens, D.W., and Gispen, W.H. (1996). Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45, 1259–1266.10.2337/diab.45.9.1259Suche in Google Scholar PubMed

Biessels, G.J., Kamal, A., Urban, I.J., Spruijt, B.M., Erkelens, D.W., and Gispen, W.H. (1998). Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res. 800, 125–135.10.1016/S0006-8993(98)00510-1Suche in Google Scholar PubMed

Brindley, D.N. and Rolland, Y. (1989). Possible connections between stress, diabetes, obesity, hypertension and altered lipoprotein metabolism that may result in atherosclerosis. Clin. Sci. (Lond). 77, 453–461.10.1042/cs0770453Suche in Google Scholar PubMed

Burke, S.N. and Barnes, C.A. (2006). Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 7, 30–40.10.1038/nrn1809Suche in Google Scholar PubMed

Canto, C., Gerhart-Hines, Z., Feige, J.N., Lagouge, M., Noriega, L., Milne, J.C., Elliott, P.J., Puigserver, P., and Auwerx, J. (2009). AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458, 1056–1060.10.1038/nature07813Suche in Google Scholar PubMed PubMed Central

Chan, K.H., Lam, K.S., Cheng, O.Y., Kwan, J.S., Ho, P.W., Cheng, K.K., Chung, S.K., Ho, J.W., Guo, V.Y., and Xu, A. (2012). Adiponectin is protective against oxidative stress induced cytotoxicity in amyloid-beta neurotoxicity. PLoS One 7, e52354.10.1371/journal.pone.0052354Suche in Google Scholar PubMed PubMed Central

Chen, J., Tan, B., Karteris, E., Zervou, S., Digby, J., Hillhouse, E.W., Vatish, M., and Randeva, H.S. (2006). Secretion of adiponectin by human placenta: differential modulation of adiponectin and its receptors by cytokines. Diabetologia 49, 1292–1302.10.1007/s00125-006-0194-7Suche in Google Scholar PubMed

Chung, M.M., Chen, Y.L., Pei, D., Cheng, Y.C., Sun, B., Nicol, C.J., Yen, C.H., Chen, H.M., Liang, Y.J., and Chiang, M.C. (2015). The neuroprotective role of metformin in advanced glycation end product treated human neural stem cells is AMPK-dependent. Biochim. Biophys. Acta 1852, 720–731.10.1016/j.bbadis.2015.01.006Suche in Google Scholar PubMed

Civitarese, A.E., Ukropcova, B., Carling, S., Hulver, M., DeFronzo, R.A., Mandarino, L., Ravussin, E., and Smith, S.R. (2006). Role of adiponectin in human skeletal muscle bioenergetics. Cell Metab 4, 75–87.10.1016/j.cmet.2006.05.002Suche in Google Scholar PubMed PubMed Central

Craggs, L. and Kalaria, R.N. (2011). Revisiting dietary antioxidants, neurodegeneration and dementia. Neuroreport 22, 1–3.10.1097/WNR.0b013e328342741cSuche in Google Scholar PubMed

De Roo, M., Klauser, P., Mendez, P., Poglia, L., and Muller, D. (2008). Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cerebral Cortex 18, 151–161.10.1093/cercor/bhm041Suche in Google Scholar PubMed

Detopoulou, P., Panagiotakos, D.B., Chrysohoou, C., Fragopoulou, E., Nomikos, T., Antonopoulou, S., Pitsavos, C., and Stefanadis, C. (2010). Dietary antioxidant capacity and concentration of adiponectin in apparently healthy adults: the ATTICA study. Eur. J. Clin. Nutr. 64, 161–168.10.1038/ejcn.2009.130Suche in Google Scholar PubMed

Deuschle, M. (2013). Effects of antidepressants on glucose metabolism and diabetes mellitus type 2 in adults. Curr. Opin. Psychiatry 26, 60–65.10.1097/YCO.0b013e32835a4206Suche in Google Scholar PubMed

Dhar, M., Zhu, M., Impey, S., Lambert, T.J., Bland, T., Karatsoreos, I.N., Nakazawa, T., Appleyard, S.M., and Wayman, G.A. (2014). Leptin induces hippocampal synaptogenesis via CREB-regulated microRNA-132 suppression of p250GAP. Mol. Endocrinol. 28, 1073–1087.10.1210/me.2013-1332Suche in Google Scholar PubMed PubMed Central

Diez, J.J. and Iglesias, P. (2003). The role of the novel adipocyte-derived hormone adiponectin in human disease. Eur. J. Endocrinol. 148, 293–300.10.1530/eje.0.1480293Suche in Google Scholar PubMed

Ding, Q., Vaynman, S., Souda, P., Whitelegge, J.P., and Gomez-Pinilla, F. (2006). Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur. J. Neurosci. 24, 1265–1276.10.1111/j.1460-9568.2006.05026.xSuche in Google Scholar PubMed

Duman, R.S., Nakagawa, S., and Malberg, J. (2001). Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 25, 836–844.10.1016/S0893-133X(01)00358-XSuche in Google Scholar PubMed

Duman, R.S., Aghajanian, G.K., Sanacora, G., and Krystal, J.H. (2016). Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat. Med. 22, 238–249.10.1038/nm.4050Suche in Google Scholar PubMed

Efstathiou, S.P., Tsioulos, D.I., Tsiakou, A.G., Gratsias, Y.E., Pefanis, A.V., and Mountokalakis, T.D. (2005). Plasma adiponectin levels and five-year survival after first-ever ischemic stroke. Stroke 36, 1915–1919.10.1161/01.STR.0000177874.29849.f0Suche in Google Scholar PubMed

Eisch, A.J. (2002). Adult neurogenesis: implications for psychiatry. Prog. Brain Res. 138, 315–342.10.1016/S0079-6123(02)38085-3Suche in Google Scholar PubMed

Erion, J.R., Wosiski-Kuhn, M., Dey, A., Hao, S., Davis, C.L., Pollock, N.K., and Stranahan, A.M. (2014). Obesity elicits interleukin 1-mediated deficits in hippocampal synaptic plasticity. J. Neurosci. 34, 2618–2631.10.1523/JNEUROSCI.4200-13.2014Suche in Google Scholar PubMed PubMed Central

Fasshauer, M., Paschke, R., and Stumvoll, M. (2004). Adiponectin, obesity, and cardiovascular disease. Biochimie 86, 779–784.10.1016/j.biochi.2004.09.016Suche in Google Scholar PubMed

Folmes, C.D., Dzeja, P.P., Nelson, T.J., and Terzic, A. (2012). Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11, 596–606.10.1016/j.stem.2012.10.002Suche in Google Scholar PubMed PubMed Central

Gage, F.H. (2002). Neurogenesis in the adult brain. J. Neurosci. 22, 612–613.10.1523/JNEUROSCI.22-03-00612.2002Suche in Google Scholar PubMed

Gao, C., Liu, Y., Jiang, Y., Ding, J., and Li, L. (2014). Geniposide ameliorates learning memory deficits, reduces tau phosphorylation and decreases apoptosis via GSK3beta pathway in streptozotocin-induced alzheimer rat model. Brain Pathol. 24, 261–269.10.1111/bpa.12116Suche in Google Scholar PubMed PubMed Central

Gao, C., Wang, Q., Chung, S.K., and Shen, J. (2017). Crosstalk of metabolic factors and neurogenic signaling in adult neurogenesis: implication of metabolic regulation for mental and neurological diseases. Neurochem. Int. 106, 24–36.10.1016/j.neuint.2017.02.001Suche in Google Scholar PubMed

Gao, C., Chen, X., Xu, A., Cheng, K., and Shen, J. (2018a). Adaptor protein APPL2 affects adult antidepressant behaviors and hippocampal neurogenesis via regulating the sensitivity of glucocorticoid receptor. Mol. Neurobiol. 55, 5537–5547.10.1007/s12035-017-0785-ySuche in Google Scholar

Gao, C., Du, Q., Li, W., Deng, R., Wang, Q., Xu, A., and Shen, J. (2018b). Baicalin Modulates APPL2/Glucocorticoid Receptor Signaling Cascade, Promotes Neurogenesis, and Attenuates Emotional and Olfactory Dysfunctions in Chronic Corticosterone-Induced Depression. Mol Neurobiol. 55, 9334–9348.10.1007/s12035-018-1042-8Suche in Google Scholar

Gault, V.A. and Holscher, C. (2018). GLP-1 receptor agonists show neuroprotective effects in animal models of diabetes. Peptides 100, 101–107.10.1016/j.peptides.2017.11.017Suche in Google Scholar PubMed

Hajszan, T., MacLusky, N.J., and Leranth, C. (2005). Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur. J. Neurosci. 21, 1299–1303.10.1111/j.1460-9568.2005.03968.xSuche in Google Scholar PubMed

Harvey, J. (2007). Leptin regulation of neuronal excitability and cognitive function. Curr. Opin. Pharmacol. 7, 643–647.10.1016/j.coph.2007.10.006Suche in Google Scholar PubMed

Huang, C.Y., Chang, A.C., Chen, H.T., Wang, S.W., Lo, Y.S., and Tang, C.H. (2016). Adiponectin promotes VEGF-C-dependent lymphangiogenesis by inhibiting miR-27b through a CaMKII/AMPK/p38 signaling pathway in human chondrosarcoma cells. Clin. Sci. (Lond). 130, 1523–1533.10.1042/CS20160117Suche in Google Scholar PubMed

Huot, R.L., Plotsky, P.M., Lenox, R.H., and McNamara, R.K. (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res. 950, 52–63.10.1016/S0006-8993(02)02985-2Suche in Google Scholar PubMed

Huttenlocher, P.R. and Dabholkar, A.S. (1997). Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387, 167–178.10.1002/(SICI)1096-9861(19971020)387:2<167::AID-CNE1>3.0.CO;2-ZSuche in Google Scholar PubMed

Hwang, L.L., Wang, C.H., Li, T.L., Chang, S.D., Lin, L.C., Chen, C.P., Chen, C.T., Liang, K.C., Ho, I.K., Yang, W.S., et al. (2010). Sex differences in high-fat diet-induced obesity, metabolic alterations and learning, and synaptic plasticity deficits in mice. Obesity (Silver Spring) 18, 463–469.10.1038/oby.2009.273Suche in Google Scholar PubMed

Ibi, D., Takuma, K., Koike, H., Mizoguchi, H., Tsuritani, K., Kuwahara, Y., Kamei, H., Nagai, T., Yoneda, Y., Nabeshima, T., et al. (2008). Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J. Neurochem. 105, 921–932.10.1111/j.1471-4159.2007.05207.xSuche in Google Scholar PubMed

Inoki, K., Ouyang, H., Zhu, T., Lindvall, C., Wang, Y., Zhang, X., Yang, Q., Bennett, C., Harada, Y., Stankunas, K., et al. (2006). TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126, 955–968.10.1016/j.cell.2006.06.055Suche in Google Scholar PubMed

Jenwitheesuk, A., Nopparat, C., Mukda, S., Wongchitrat, P., and Govitrapong, P. (2014). Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int. J. Mol. Sci. 15, 16848–16884.10.3390/ijms150916848Suche in Google Scholar PubMed PubMed Central

Jung, Y.S., Ha, S.K., Kim, S.D., Kim, S.H., Lim, D.J., and Choi, J.I. (2013). The role of adiponectin in secondary inflammatory reaction in cerebral ischemia. J. Cerebrovasc. Endovasc. Neurosurg. 15, 171–176.10.7461/jcen.2013.15.3.171Suche in Google Scholar PubMed PubMed Central

Kamal, A., Biessels, G.J., Duis, S.E., and Gispen, W.H. (2000). Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia 43, 500–506.10.1007/s001250051335Suche in Google Scholar PubMed

Kiebish, M.A., Young, D.M., Lehman, J.J., and Han, X. (2012). Chronic caloric restriction attenuates a loss of sulfatide content in PGC-1alpha-/- mouse cortex: a potential lipidomic role of PGC-1alpha in neurodegeneration. J. Lipid Res. 53, 273–281.10.1194/jlr.M020628Suche in Google Scholar PubMed PubMed Central

Kiefer, F., Jahn, H., Otte, C., Demiralay, C., Wolf, K., and Wiedemann, K. (2005). Increasing leptin precedes craving and relapse during pharmacological abstinence maintenance treatment of alcoholism. J. Psychiatr. Res. 39, 545–551.10.1016/j.jpsychires.2004.11.005Suche in Google Scholar PubMed

Kim, J.J. and Diamond, D.M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453–462.10.1038/nrn849Suche in Google Scholar PubMed

Kim, J., Kundu, M., Viollet, B., and Guan, K.L. (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132–141.10.1038/ncb2152Suche in Google Scholar PubMed PubMed Central

Klampfl, S. and Maass, W. (2013). Emergence of dynamic memory traces in cortical microcircuit models through STDP. J. Neurosci. 33, 11515–11529.10.1523/JNEUROSCI.5044-12.2013Suche in Google Scholar PubMed PubMed Central

Leo, R., Di Lorenzo, G., Tesauro, M., Cola, C., Fortuna, E., Zanasi, M., Troisi, A., Siracusano, A., Lauro, R., and Romeo, F. (2006). Decreased plasma adiponectin concentration in major depression. Neurosci. Lett. 407, 211–213.10.1016/j.neulet.2006.08.043Suche in Google Scholar PubMed

Li, D., Huang, Y., Cheng, B., Su, J., Zhou, W.X., and Zhang, Y.X. (2016). Streptozotocin induces mild cognitive impairment at appropriate doses in mice as determined by long-term potentiation and the Morris water maze. J. Alzheimer’s Dis. 54, 89–98.10.3233/JAD-150979Suche in Google Scholar PubMed

Liu, D., Diorio, J., Day, J.C., Francis, D.D., and Meaney, M.J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799–806.10.1038/77702Suche in Google Scholar PubMed

Liu, J., Guo, M., Zhang, D., Cheng, S.Y., Liu, M., Ding, J., Scherer, P.E., Liu, F., and Lu, X.Y. (2012). Adiponectin is critical in determining susceptibility to depressive behaviors and has antidepressant-like activity. Proc. Natl. Acad. Sci. USA 109, 12248–12253.10.1073/pnas.1202835109Suche in Google Scholar PubMed PubMed Central

Liu, L.H., Xie, J.Y., Guo, W.W., Wu, G.Y., Chen, Z.F., Yi, J.Y., Zhang, L., Zhang, Z.J., and Li, Z. (2014). Evodiamine activates AMPK and promotes adiponectin multimerization in 3T3-L1 adipocytes. J. Asian Nat. Prod. Res. 16, 1074–1083.10.1080/10286020.2014.939071Suche in Google Scholar PubMed

Lou, Y.B., Fan, F.X., Mu, Y.C., and Dong, X. (2018). The implication of diabetes metabolomics in the early diagnosis and pathogenesis of pancreatic cancer. J. Biol. Regul. Homeost. Agents 32, 75–82.Suche in Google Scholar PubMed

Lu, X.Y. (2007). The leptin hypothesis of depression: a potential link between mood disorders and obesity? Curr. Opin. Pharmacol. 7, 648–652.10.1016/j.coph.2007.10.010Suche in Google Scholar PubMed PubMed Central

Luo, X.H., Guo, L.J., Yuan, L.Q., Xie, H., Zhou, H.D., Wu, X.P., and Liao, E.Y. (2005). Adiponectin stimulates human osteoblasts proliferation and differentiation via the MAPK signaling pathway. Exp. Cell Res. 309, 99–109.10.1016/j.yexcr.2005.05.021Suche in Google Scholar PubMed

Luo, X.H., Guo, L.J., Xie, H., Yuan, L.Q., Wu, X.P., Zhou, H.D., and Liao, E.Y. (2006). Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J. Bone Miner. Res. 21, 1648–1656.10.1359/jbmr.060707Suche in Google Scholar PubMed

Maeda, N., Takahashi, M., Funahashi, T., Kihara, S., Nishizawa, H., Kishida, K., Nagaretani, H., Matsuda, M., Komuro, R., Ouchi, N., et al. (2001). PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 50, 2094–2099.10.2337/diabetes.50.9.2094Suche in Google Scholar PubMed

Majumdar, D., Nebhan, C.A., Hu, L., Anderson, B., and Webb, D.J. (2011). An APPL1/Akt signaling complex regulates dendritic spine and synapse formation in hippocampal neurons. Mol. Cell. Neurosci. 46, 633–644.10.1016/j.mcn.2011.01.003Suche in Google Scholar PubMed PubMed Central

Martinez-Tellez, R., Gomez-Villalobos Mde, J., and Flores, G. (2005). Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin. Brain Res. 1048, 108–115.10.1016/j.brainres.2005.04.048Suche in Google Scholar PubMed

Mazer, C., Muneyyirci, J., Taheny, K., Raio, N., Borella, A., and Whitaker-Azmitia, P. (1997). Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat: a possible model of neurodevelopmental disorders with cognitive deficits. Brain Res. 760, 68–73.10.1016/S0006-8993(97)00297-7Suche in Google Scholar

Moon, H.S., Dincer, F., and Mantzoros, C.S. (2013). Amylin-induced downregulation of hippocampal neurogenesis is attenuated by leptin in a STAT3/AMPK/ERK-dependent manner in mice. Diabetologia 56, 627–634.10.1007/s00125-012-2799-3Suche in Google Scholar PubMed

Nabavi, S., Fox, R., Proulx, C.D., Lin, J.Y., Tsien, R.Y., and Malinow, R. (2014). Engineering a memory with LTD and LTP. Nature 511, 348–352.10.1038/nature13294Suche in Google Scholar PubMed PubMed Central

Narita, K., Murata, T., Takahashi, T., Kosaka, H., Omata, N., and Wada, Y. (2006). Plasma levels of adiponectin and tumor necrosis factor-alpha in patients with remitted major depression receiving long-term maintenance antidepressant therapy. Prog. Neuropsychopharmacol. Biol. Psychiatry 30, 1159–1162.10.1016/j.pnpbp.2006.03.030Suche in Google Scholar PubMed

Ng, R.C., Cheng, O.Y., Jian, M., Kwan, J.S., Ho, P.W., Cheng, K.K., Yeung, P.K., Zhou, L.L., Hoo, R.L., Chung, S.K., et al. (2016). Chronic adiponectin deficiency leads to Alzheimer’s disease-like cognitive impairments and pathologies through AMPK inactivation and cerebral insulin resistance in aged mice. Mol. Neurodegener. 11, 71.10.1186/s13024-016-0136-xSuche in Google Scholar PubMed PubMed Central

Nicolas, S., Veyssiere, J., Gandin, C., Zsurger, N., Pietri, M., Heurteaux, C., Glaichenhaus, N., Petit-Paitel, A., and Chabry, J. (2015). Neurogenesis-independent antidepressant-like effects of enriched environment is dependent on adiponectin. Psychoneuroendocrinology 57, 72–83.10.1016/j.psyneuen.2015.03.017Suche in Google Scholar PubMed

Nicolas, S., Debayle, D., Bechade, C., Maroteaux, L., Gay, A.S., Bayer, P., Heurteaux, C., Guyon, A., and Chabry, J. (2018). Adiporon, an adiponectin receptor agonist acts as an antidepressant and metabolic regulator in a mouse model of depression. Transl. Psychiatry. 8, 159.10.1038/s41398-018-0210-ySuche in Google Scholar PubMed PubMed Central

O’Kusky, J.R., Ye, P., and D’Ercole, A.J. (2000). Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J. Neurosci. 20, 8435–8442.10.1523/JNEUROSCI.20-22-08435.2000Suche in Google Scholar PubMed

Okuyama, S., Shinoka, W., Nakamura, K., Kotani, M., Sawamoto, A., Sugawara, K., Sudo, M., Nakajima, M., and Furukawa, Y. (2018). Suppressive effects of the peel of Citrus kawachiensis (Kawachi Bankan) on astroglial activation, tau phosphorylation, and inhibition of neurogenesis in the hippocampus of type 2 diabetic db/db mice. Biosci. Biotechnol. Biochem. 82, 1384–1395.10.1080/09168451.2018.1469396Suche in Google Scholar PubMed

Ormerod, B.K., Hanft, S.J., Asokan, A., Haditsch, U., Lee, S.W., and Palmer, T.D. (2013). PPARgamma activation prevents impairments in spatial memory and neurogenesis following transient illness. Brain Behav. Immun. 29, 28–38.10.1016/j.bbi.2012.10.017Suche in Google Scholar PubMed

Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T., Funahashi, T., and Walsh, K. (2004). Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J. Biol. Chem. 279, 1304–1309.10.1074/jbc.M310389200Suche in Google Scholar PubMed

Pendlebury, S.T. and Rothwell, P.M. (2009). Prevalence, incidence, and factors associated with pre-stroke and post-stroke dementia: a systematic review and meta-analysis. Lancet Neurol. 8, 1006–1018.10.1016/S1474-4422(09)70236-4Suche in Google Scholar PubMed

Pousti, F., Ahmadi, R., Mirahmadi, F., Hosseinmardi, N., and Rohampour, K. (2018). Adiponectin modulates synaptic plasticity in hippocampal dentate gyrus. Neurosci. Lett. 662, 227–232.10.1016/j.neulet.2017.10.042Suche in Google Scholar PubMed

Qiu, G., Wan, R., Hu, J., Mattson, M.P., Spangler, E., Liu, S., Yau, S.Y., Lee, T.M., Gleichmann, M., Ingram, D.K., So, K.F., and Zou, S. (2011). Adiponectin protects rat hippocampal neurons against excitotoxicity. Age (Dordr). 33, 155–165.10.1007/s11357-010-9173-5Suche in Google Scholar PubMed PubMed Central

Ruan, H. and Dong, L.Q. (2016). Adiponectin signaling and function in insulin target tissues. J. Mol. Cell Biol. 8, 101–109.10.1093/jmcb/mjw014Suche in Google Scholar PubMed PubMed Central

Saeedi Saravi, S.S., Saeedi Saravi, S.S., Khoshbin, K., and Dehpour, A.R. (2017). Current insights into pathogenesis of Parkinson;s disease: Approach to mevalonate pathway and protective role of statins. Biomed. Pharmacother. 90, 724–730.10.1016/j.biopha.2017.04.038Suche in Google Scholar PubMed

Sarlak, G., Jenwitheesuk, A., Chetsawang, B., and Govitrapong, P. (2013). Effects of melatonin on nervous system aging: neurogenesis and neurodegeneration. J. Pharmacol. Sci. 123, 9–24.10.1254/jphs.13R01SRSuche in Google Scholar PubMed

Scheff, S. (2003). Reactive synaptogenesis in aging and Alzheimer’s disease: lessons learned in the Cotman laboratory. Neurochem. Res. 28, 1625–1630.10.1023/A:1026048619220Suche in Google Scholar PubMed

Schulz, P.E., Cook, E.P., and Johnston, D. (1994). Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J. Neurosci. 14, 5325–5337.10.1523/JNEUROSCI.14-09-05325.1994Suche in Google Scholar PubMed

Shankar, G.M., Li, S., Mehta, T.H., Garcia-Munoz, A., Shepardson, N.E., Smith, I., Brett, F.M., Farrell, M.A., Rowan, M.J., Lemere, C.A., et al. (2008). Amyloid-beta protein dimers isolated directly from Alzheimer’s brains impair synaptic plasticity and memory. Nat. Med. 14, 837–842.10.1038/nm1782Suche in Google Scholar PubMed

Shapiro, L. and Scherer, P.E. (1998). The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr. Biol. 8, 335–338.10.1016/S0960-9822(98)70133-2Suche in Google Scholar PubMed

Shi, L., Zhang, Z., Li, L., and Holscher, C. (2017). A novel dual GLP-1/GIP receptor agonist alleviates cognitive decline by re-sensitizing insulin signaling in the Alzheimer icv. STZ rat model. Behav. Brain Res. 327, 65–74.10.1016/j.bbr.2017.03.032Suche in Google Scholar PubMed

Snyder, J.S., Soumier, A., Brewer, M., Pickel, J., and Cameron, H.A. (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476, 458–461.10.1038/nature10287Suche in Google Scholar PubMed PubMed Central

Song, J., Lee, W.T., Park, K.A., and Lee, J.E. (2014). Association between risk factors for vascular dementia and adiponectin. Biomed. Res. Int. 2014, 261672.10.1155/2014/261672Suche in Google Scholar PubMed PubMed Central

Spielman, L.J., Little, J.P., and Klegeris, A. (2014). Inflammation and insulin/IGF-1 resistance as the possible link between obesity and neurodegeneration. J. Neuroimmunol. 273, 8–21.10.1016/j.jneuroim.2014.06.004Suche in Google Scholar PubMed

Stranahan, A.M., Norman, E.D., Lee, K., Cutler, R.G., Telljohann, R.S., Egan, J.M., and Mattson, M.P. (2008). Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18, 1085–1088.10.1002/hipo.20470Suche in Google Scholar PubMed PubMed Central

Sugiyama, M., Takahashi, H., Hosono, K., Endo, H., Kato, S., Yoneda, K., Nozaki, Y., Fujita, K., Yoneda, M., Wada, K., et al. (2009). Adiponectin inhibits colorectal cancer cell growth through the AMPK/mTOR pathway. Int. J. Oncol. 34, 339–344.Suche in Google Scholar PubMed

Takeuchi, S., Wada, K., Nawashiro, H., Uozumi, Y., Otani, N., Osada, H., Nagatani, K., Kobayashi, H., Suzuki, T., and Shima, K. (2013). Adiponectin and traumatic brain injury. Acta Neurochir. Suppl. 118, 111–114.10.1007/978-3-7091-1434-6_19Suche in Google Scholar PubMed

Tanaka, K., Wilson, R.M., Essick, E.E., Duffen, J.L., Scherer, P.E., Ouchi, N., and Sam, F. (2014). Effects of adiponectin on calcium-handling proteins in heart failure with preserved ejection fraction. Circ. Heart Fail. 7, 976–985.10.1161/CIRCHEARTFAILURE.114.001279Suche in Google Scholar PubMed PubMed Central

Teixeira, A.L., Diniz, B.S., Campos, A.C., Miranda, A.S., Rocha, N.P., Talib, L.L., Gattaz, W.F., and Forlenza, O.V. (2013). Decreased levels of circulating adiponectin in mild cognitive impairment and Alzheimer’s disease. Neuromolecular Med. 15, 115–121.10.1007/s12017-012-8201-2Suche in Google Scholar PubMed

Une, K., Takei, Y.A., Tomita, N., Asamura, T., Ohrui, T., Furukawa, K., and Arai, H. (2011). Adiponectin in plasma and cerebrospinal fluid in MCI and Alzheimer’s disease. Eur J Neurol. 18, 1006–1009.10.1111/j.1468-1331.2010.03194.xSuche in Google Scholar PubMed

Vafaei-Nezhad, S., Hami, J., Sadeghi, A., Ghaemi, K., Hosseini, M., Abedini, M.R., and Haghir, H. (2016). The impacts of diabetes in pregnancy on hippocampal synaptogenesis in rat neonates. Neurosci. 318, 122–133.10.1016/j.neuroscience.2016.01.025Suche in Google Scholar PubMed

Villeda, S.A., Luo, J., Mosher, K.I., Zou, B., Britschgi, M., Bieri, G., Stan, T.M., Fainberg, N., Ding, Z., Eggel, A., et al. (2011). The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477, 90–94.10.1038/nature10357Suche in Google Scholar PubMed PubMed Central

Wang, Y., Lam, K.S., Xu, J.Y., Lu, G., Xu, L.Y., Cooper, G.J., and Xu, A. (2005). Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J. Biol. Chem. 280, 18341–18347.10.1074/jbc.M501149200Suche in Google Scholar PubMed

Wang, C., Mao, X., Wang, L., Liu, M., Wetzel, M.D., Guan, K.L., Dong, L.Q., and Liu, F. (2007). Adiponectin sensitizes insulin signaling by reducing p70 S6 kinase-mediated serine phosphorylation of IRS-1. J. Biol. Chem. 282, 7991–7996.10.1074/jbc.M700098200Suche in Google Scholar PubMed

Wang, C., Xin, X., Xiang, R., Ramos, F.J., Liu, M., Lee, H.J., Chen, H., Mao, X., Kikani, C.K., Liu, F., et al. (2009a). Yin-Yang regulation of adiponectin signaling by APPL isoforms in muscle cells. J. Biol. Chem. 284, 31608–31615.10.1074/jbc.M109.010355Suche in Google Scholar PubMed PubMed Central

Wang, S.H., Sun, Z.L., Guo, Y.J., Yuan, Y., and Li, L. (2009b). PPARgamma-mediated advanced glycation end products regulation of neural stem cells. Mol. Cell. Endocrinol. 307, 176–184.10.1016/j.mce.2009.02.012Suche in Google Scholar PubMed

Weisz, F., Piccinin, S., Mango, D., Ngomba, R.T., Mercuri, N.B., Nicoletti, F., and Nistico, R. (2017). The role of adiponectin receptors in the regulation of synaptic transmission in the hippocampus. Synapse 71.10.1002/syn.21964Suche in Google Scholar PubMed

Whitehead, J.P., Richards, A.A., Hickman, I.J., Macdonald, G.A., and Prins, J.B. (2006). Adiponectin – a key adipokine in the metabolic syndrome. Diabetes Obes. Metab. 8, 264–280.10.1111/j.1463-1326.2005.00510.xSuche in Google Scholar PubMed

Wosiski-Kuhn, M., Erion, J.R., Gomez-Sanchez, E.P., Gomez-Sanchez, C.E., and Stranahan, A.M. (2014). Glucocorticoid receptor activation impairs hippocampal plasticity by suppressing BDNF expression in obese mice. Psychoneuroendocrinology 42, 165–177.10.1016/j.psyneuen.2014.01.020Suche in Google Scholar PubMed PubMed Central

Xie, L., Feng, X., Shi, Y., He, M., Wang, P., Wang, X., Mi, Z., Liu, Q., and Zhang, K. (2018). Blocking the glycolytic pathway sensitizes breast cancer to sonodynamic therapy. Ultrasound Med. Biol. 44, 1233–1243.10.1016/j.ultrasmedbio.2018.01.020Suche in Google Scholar PubMed

Xu, N., Zhang, Y., Doycheva, D.M., Ding, Y., Zhang, Y., Tang, J., Guo, H., and Zhang, J.H. (2018). Adiponectin attenuates neuronal apoptosis induced by hypoxia-ischemia via the activation of AdipoR1/APPL1/LKB1/AMPK pathway in neonatal rats. Neuropharmacology 133, 415–428.10.1016/j.neuropharm.2018.02.024Suche in Google Scholar PubMed

Yamada, K.A. (1998). Modulating excitatory synaptic neurotransmission: potential treatment for neurological disease? Neurobiol. Dis. 5, 67–80.10.1006/nbdi.1998.0190Suche in Google Scholar PubMed

Yau, S.Y., Li, A., Hoo, R.L., Ching, Y.P., Christie, B.R., Lee, T.M., Xu, A., and So, K.F. (2014). Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc. Natl. Acad. Sci. U S A 111, 15810–15815.10.1073/pnas.1415219111Suche in Google Scholar PubMed PubMed Central

Ye, J., Gao, Z., Yin, J., and He, Q. (2007). Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 293, E1118–E1128.10.1152/ajpendo.00435.2007Suche in Google Scholar PubMed

Yoon, G., Shah, S.A., Ali, T., and Kim, M.O. (2018). The adiponectin homolog osmotin enhances neurite outgrowth and synaptic complexity via AdipoR1/NgR1 signaling in Alzheimer’s disease. Mol. Neurobiol. 55, 6673–6686.10.1007/s12035-017-0847-1Suche in Google Scholar PubMed

Yuan, T.F. and Slotnick, B.M. (2014). Roles of olfactory system dysfunction in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 54, 26–30.10.1016/j.pnpbp.2014.05.013Suche in Google Scholar PubMed

Zhang, D., Guo, M., Zhang, W., and Lu, X.Y. (2011). Adiponectin stimulates proliferation of adult hippocampal neural stem/progenitor cells through activation of p38 mitogen-activated protein kinase (p38MAPK)/glycogen synthase kinase 3beta (GSK-3beta)/beta-catenin signaling cascade. J. Biol. Chem. 286, 44913–44920.10.1074/jbc.M111.310052Suche in Google Scholar PubMed PubMed Central

Zhang, D., Wang, X., and Lu, X.Y. (2016). Adiponectin exerts neurotrophic effects on dendritic arborization, spinogenesis, and neurogenesis of the dentate gyrus of male mice. Endocrinology 157, 2853–2869.10.1210/en.2015-2078Suche in Google Scholar PubMed PubMed Central

Zhao, C., Deng, W., and Gage, F.H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645–660.10.1016/j.cell.2008.01.033Suche in Google Scholar PubMed

Zubenko, G.S. and Moossy, J. (1988). Major depression in primary dementia. Clinical and neuropathologic correlates. Arch. Neurol. 45, 1182–1186.10.1001/archneur.1988.00520350020008Suche in Google Scholar PubMed

Zunszain, P.A., Horowitz, M.A., Cattaneo, A., Lupi, M.M., and Pariante, C.M. (2013). Ketamine: synaptogenesis, immunomodulation and glycogen synthase kinase-3 as underlying mechanisms of its antidepressant properties. Mol. Psychiatry 18, 1236–1241.10.1038/mp.2013.87Suche in Google Scholar PubMed PubMed Central

Received: 2018-06-20
Accepted: 2018-10-06
Published Online: 2019-01-08
Published in Print: 2019-07-26

©2019 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 22.12.2025 von https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2018-0062/html?lang=de
Button zum nach oben scrollen