Glucagon-Like Peptide-2 Receptor is Involved in Spatial Cognitive Dysfunction in Rats After Chronic Cerebral Hypoperfusion
Abstract
Chronic cerebral hypoperfusion (CCH) affects the aging population and especially patients with neurodegenerative diseases, such as Alzheimer's disease or Parkinson's disease. CCH is closely related to the cognitive dysfunction in these diseases. Glucagon-like peptide-2 receptor (GLP2R) mRNA and protein are highly expressed in the gut and in hippocampal neurons. This receptor is involved in the regulation of food intake and the control of energy balance and glucose homeostasis. The present study employed behavioral techniques, electrophysiology, western blotting, immunohistochemistry, quantitative real time polymerase chain reaction (qRT-PCR), and Golgi staining to investigate whether the expression of GLP2R changes after CCH and whether GLP2R is involved in cognitive impairment caused by CCH. Our findings show that CCH significantly decreased hippocampal GLP2R mRNA and protein levels. GLP2R upregulation could prevent CCH-induced cognitive impairment. It also improved the CCH-induced impairment of long-term potentiation and long-term depression. Additionally, GLP2R modulated after CCH the AKT-mTOR-p70S6K pathway in the hippocampus. Moreover, an upregulation of the GLP2R increased the neurogenesis in the dentate gyrus, neuronal activity, and density of dendritic spines and mushroom spines in hippocampal neurons. Our findings reveal the involvement of GLP2R via a modulation of the AKT-mTOR-p70S6K pathway in the mechanisms underlying CCH-induced impairments of spatial learning and memory. We suggest that the GLP2R and the AKT-mTOR-p70S6K pathway in the hippocampus are promising targets to treat cognition deficits in CCH.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
GLp2r is expressed in the brain and the gut and involved in spatial cognitive injury following chronic cerebral hypoperfusion.
“GLp2r is especially intriguing as it is expressed in the brain and the gut and involved in spatial cognitive injury following chronic cerebral hypoperfusion36.”
From Integrated analysis of behavioral, epigenetic, and gut microbiome analyses in AppNL-G-F, AppNL-F, and wild type mice (2021) · cites this paper as [36]
Cites
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Running enhances neurogenesis, learning, and long-term potentiation in mice
van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13427 · Cited by 2,904 · see citing works
mTOR-Dependent Synapse Formation Underlies the Rapid Antidepressant Effects of NMDA Antagonists
Li, N., Lee, B., Liu, R.-J., Banasr, M., Dwyer, J. M., Iwata, M., Li, X.-Y., Aghajanian, G., & Duman, R. S. (2010) · Science · doi:10.1126/science.1190287 · Cited by 2,881 · see citing works
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., et al. (2009) · Science · doi:10.1126/science.1173215 · Cited by 1,642 · see citing works
Dendritic spine pathology in neuropsychiatric disorders
Penzes, P., Cahill, M. E., Jones, K. A., VanLeeuwen, J.-E., & Woolfrey, K. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2741 · Cited by 1,523 · see citing works
mTOR signaling: At the crossroads of plasticity, memory and disease
Hoeffer, C. A., & Klann, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.003 · Cited by 1,128 · see citing works
Saxe, M. D., Battaglia, F., Wang, J.-W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., Santarelli, L., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607207103 · Cited by 1,020 · see citing works
Learning-Induced LTP in Neocortex
Rioult-Pedotti, M.-S., Friedman, D. J., & Donoghue, J. P. (2000) · Science · doi:10.1126/science.290.5491.533 · Cited by 1,014 · see citing works
Engineering a memory with LTD and LTP
Nabavi, S., Fox, R., Proulx, C. D., Lin, J. Y., Tsien, R. Y., & Malinow, R. (2014) · Nature · doi:10.1038/nature13294 · Cited by 980 · see citing works
Do thin spines learn to be mushroom spines that remember?
Bourne, J., & Harris, K. M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.009 · Cited by 843 · see citing works
Arc/Arg3.1 Is Essential for the Consolidation of Synaptic Plasticity and Memories
Plath, N., Ohana, O., Dammermann, B., Errington, M. L., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.024 · Cited by 827 · see citing works
Structural dynamics of dendritic spines in memory and cognition
Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., & Noguchi, J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.001 · Cited by 804 · see citing works
Farkas, E., Luiten, P. G. M., & Bari, F. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.01.003 · Cited by 724 · see citing works
Lugert, S., Basak, O., Knuckles, P., Haussler, U., Fabel, K., Götz, M., Haas, C. A., Kempermann, G., Taylor, V., & Giachino, C. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.03.017 · Cited by 704 · see citing works
Hippocampal synaptic plasticity, spatial memory and anxiety
Bannerman, D. M., Sprengel, R., Sanderson, D. J., McHugh, S. B., Rawlins, J. N. P., Monyer, H., & Seeburg, P. H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3677 · Cited by 688 · see citing works
Potential role for adult neurogenesis in the encoding of time in new memories
Aimone, J. B., Wiles, J., & Gage, F. H. (2006) · Nature Neuroscience · doi:10.1038/nn1707 · Cited by 644 · see citing works
Pastuzyn, E. D., Day, C. E., Kearns, R. B., Kyrke‐Smith, M., Taibi, A. V., McCormick, J. F., Yoder, N., Belnap, D. M., Erlendsson, S., Morado, D. R., et al. (2018) · Cell · doi:10.1016/j.cell.2017.12.024 · Cited by 642 · see citing works
Ziemann, U., Ilic, T. V., Pauli, C., Meintzschel, F., & Ruge, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5016-03.2004 · Cited by 587 · see citing works
Park, S., Park, J. M., Kim, S., Kim, J.-A., Shepherd, J. D., Smith-Hicks, C. L., Chowdhury, S., Kaufmann, W., Kuhl, D., Ryazanov, A. G., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.023 · Cited by 516 · see citing works
Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning
Nakashiba, T., Young, J. Z., McHugh, T. J., Buhl, D. L., & Tonegawa, S. (2008) · Science · doi:10.1126/science.1151120 · Cited by 492 · see citing works
New views of Arc, a master regulator of synaptic plasticity
Shepherd, J. D., & Bear, M. F. (2011) · Nature Neuroscience · doi:10.1038/nn.2708 · Cited by 481 · see citing works
Dendritic structural plasticity and neuropsychiatric disease
Forrest, M. P., Parnell, E., & Penzes, P. (2018) · Nature Reviews Neuroscience · doi:10.1038/nrn.2018.16 · Cited by 464 · see citing works
Arc in synaptic plasticity: from gene to behavior
Korb, E., & Finkbeiner, S. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.007 · Cited by 388 · see citing works
Hippocampal long-term depression: master or minion in declarative memory processes?
Kemp, A., & Manahan-Vaughan, D. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.01.002 · Cited by 336 · see citing works
Prototypic G protein-coupled receptor for the intestinotrophic factor glucagon-like peptide 2
Munroe, D. G., Gupta, A., Kooshesh, F., Vyas, T., Rizkalla, G., Wang, H., Demchyshyn, L. L., Yang, Z., Kamboj, R. K., Chen, H., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1569 · Cited by 328 · see citing works
Rehman, S. U., Shah, S. A., Ali, T., Chung, J. I., & Kim, M. O. (2016) · Molecular Neurobiology · doi:10.1007/s12035-015-9604-5 · Cited by 285 · see citing works
Hippocampal neurogenesis: Learning to remember
Lazarov, O., & Hollands, C. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.006 · Cited by 281 · see citing works
Hippocampal long-term depression is required for the consolidation of spatial memory
Ge, Y., Dong, Z., Bagot, R. C., Howland, J. G., Phillips, A. G., Wong, T. P., & Wang, Y. T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008200107 · Cited by 280 · see citing works
Tang‐Christensen, M., Larsen, P. J., Thulesen, J., Rømer, J., & Vrang, N. (2000) · Nature Medicine · doi:10.1038/77535 · Cited by 269 · see citing works
Cognitive deficits in Tsc1+/−mice in the absence of cerebral lesions and seizures
Goorden, S. M. I., van Woerden, G. M., van der Weerd, L., Cheadle, J. P., & Elgersma, Y. (2007) · Annals of Neurology · doi:10.1002/ana.21317 · Cited by 247 · see citing works
Arc regulates spine morphology and maintains network stability in vivo
Peebles, C. L., Yoo, J., Thwin, M. T., Palop, J. J., Noebels, J. L., & Finkbeiner, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006546107 · Cited by 245 · see citing works
Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze
Dong, Z., Bai, Y., Wu, X., Li, H., Gong, B., Howland, J. G., Huang, Y., He, W., Li, T., & Wang, Y. T. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.027 · Cited by 219 · see citing works
Wang, X., Liu, D., Huang, H., Wang, Z., Hou, T., Yang, X., Pang, P., Wei, N., Zhou, Y., Dupras, M.-J., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.07.023 · Cited by 205 · see citing works
Alberi, L. A., Liu, S., Wang, Y. J., Badie, R., Smith‐Hicks, C. L., Wu, J., Pierfelice, T. J., Abazyan, B. N., Mattson, M. P., Kuhl, D., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.004 · Cited by 199 · see citing works
Hotspots of dendritic spine turnover facilitate clustered spine addition and learning and memory
Frank, A. C., Huang, S., Zhou, M., Gdalyahu, A., Kastellakis, G., Silva, T. K., Lu, E. D., Wen, X., Poirazi, P., Trachtenberg, J. T., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02751-2 · Cited by 178 · see citing works
Sarti, C., Pantoni, L., Bartolini, L., & Inzitari, D. (2002) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(02)00302-7 · Cited by 151 · see citing works
Estall, J. L., & Drucker, D. J. (2006) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.26.061505.111223 · Cited by 147 · see citing works
Hollands, C., Tobin, M. K., Hsu, M., Musaraca, K., Yu, T., Mishra, R., Kernie, S. G., & Lazarov, O. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0207-7 · Cited by 144 · see citing works
Plasticity of the Synaptic Modification Range
Rioult-Pedotti, M.-S., Donoghue, J. P., & Dunaevsky, A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00164.2007 · Cited by 137 · see citing works
Miyanohara, J., Kakae, M., Nagayasu, K., Nakagawa, T., Mori, Y., Arai, K., Shirakawa, H., & Kaneko, S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2451-17.2018 · Cited by 135 · see citing works
mTORC1 signalling and mRNA translation
Proud, C. G. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370227 · Cited by 131 · see citing works
Liu, D., Tang, H., Li, X.-Y., Deng, M.-F., Wei, N., Wang, X., Zhou, Y.-F., Wang, D.-Q., Fu, P., Wang, J.-Z., et al. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.01.018 · Cited by 127 · see citing works
Qiu, L., Ng, G., Tan, E. K., Liao, P., Kandiah, N., & Zeng, L. (2016) · Scientific Reports · doi:10.1038/srep23964 · Cited by 115 · see citing works
Liu, Q., Radwanski, R. E., Babadjouni, R., Patel, A. B., Hodis, D. M., Baumbacher, P., Zhao, Z., Zloković, B. V., & Mack, W. J. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17743670 · Cited by 109 · see citing works
Central GLP-2 Enhances Hepatic Insulin Sensitivity via Activating PI3K Signaling in POMC Neurons
Shi, X., Zhou, F., Li, X., Chang, B. H.-J., Li, D., Wang, Y., Tong, Q., Xu, Y., Fukuda, M., Zhao, J. J., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.06.014 · Cited by 104 · see citing works
Chen, T., Wang, D., & Chen, S. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22057 · Cited by 98 · see citing works
The Temporal Dynamics of Arc Expression Regulate Cognitive Flexibility
Wall, M. J., Collins, D. R., Chéry, S. L., Allen, Z. D., Pastuzyn, E. D., George, A. J., Nikolova, V. D., Moy, S. S., Philpot, B. D., Shepherd, J. D., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.012 · Cited by 97 · see citing works
Zhiyou, C., Yong, Y., Shanquan, S., Jun, Z., Liangguo, H., Ling, Y., & Li, J. (2009) · Neurochemical Research · doi:10.1007/s11064-008-9899-y · Cited by 96 · see citing works
Farkas, E., Institóris, Á., Domoki, F., Mihály, A., Luiten, P. G. M., & Bari, F. (2004) · Brain Research · doi:10.1016/j.brainres.2004.02.037 · Cited by 90 · see citing works
Dong, Z., Gong, B., Li, H., Bai, Y., Wu, X., Huang, Y. Y., He, W., Li, T., & Wang, Y. T. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0984-12.2012 · Cited by 89 · see citing works
Khajevand-Khazaei, M.-R., Ziaee, P., Motevalizadeh, S.-A., Rohani, M., Afshin‐Majd, S., Baluchnejadmojarad, T., & Roghani, M. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.03.001 · Cited by 86 · see citing works
Lovshin, J. A., Huang, Q., Seaberg, R. M., Brubaker, P. L., & Drucker, D. J. (2004) · Endocrinology · doi:10.1210/en.2004-0100 · Cited by 84 · see citing works
Chronic cerebral hypoperfusion induces post-stroke dementia following acute ischemic stroke in rats
Back, D. B., Kwon, K. J., Choi, D.-H., Shin, C. Y., Lee, J., Han, S., & Kim, H. Y. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0992-5 · Cited by 78 · see citing works
Dendritic Spine Dynamics Regulate the Long-Term Stability of Synaptic Plasticity
O’Donnell, C., Nolan, M. F., & van Rossum, M. C. W. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2520-11.2011 · Cited by 76 · see citing works
The CNS glucagon-like peptide-2 receptor in the control of energy balance and glucose homeostasis
Guan, X. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00096.2014 · Cited by 68 · see citing works
Stagni, F., Giacomini, A., Guidi, S., Emili, M., Uguagliati, B., Salvalai, M. E., Bortolotto, V., Grilli, M., Rimondini, R., & Bartesaghi, R. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.08.018 · Cited by 63 · see citing works
Romine, J., Gao, X., Xu, X., So, K., & Chen, J. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.01.003 · Cited by 62 · see citing works
Zhang, H., Shang, Y., Xiao, X., Yu, M., & Zhang, T. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.09.001 · Cited by 61 · see citing works
Xiong, Y., Liu, F., Liu, D., Huang, H., Wei, N., Tan, L., Chen, J., Man, H., Gong, C., Lu, Y., et al. (2015) · Aging Cell · doi:10.1111/acel.12366 · Cited by 56 · see citing works
Zhai, Y., Yamashita, T., Nakano, Y., Sun, Z., Shang, J., Feng, T., Morihara, R., Fukui, Y., Ohta, Y., Hishikawa, N., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160345 · Cited by 54 · see citing works
Henry, F. E., Hockeimer, W., Chen, A., Mysore, S. P., & Sutton, M. A. (2017) · Molecular Brain · doi:10.1186/s13041-017-0330-y · Cited by 54 · see citing works
Chen, Y., Tian, H., Yao, E., Tian, Y., Zhang, H., Xu, L., Yu, Z., Fang, Y., Wang, W., Du, P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-08227-z · Cited by 51 · see citing works
Hagena, H., & Manahan‐Vaughan, D. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00023 · Cited by 47 · see citing works
Glucagon‐like peptide‐2 stimulates the proliferation of cultured rat astrocytes
Velázquez, E., Ruiz‐Albusac, J. M., & Blázquez, E. (2003) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03677.x · Cited by 45 · see citing works
Micheau, J., Vimeney, A., Normand, E., Mulle, C., & Riedel, G. (2014) · Hippocampus · doi:10.1002/hipo.22290 · Cited by 43 · see citing works
Wang, D., Lin, Q. D., Su, S., Liu, K., Wu, Y., & Hai, J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.12.034 · Cited by 41 · see citing works
Wan, L., Liu, H., Jiang, H., Wang, C., Guo, Y., Sun, Y. X., Zhao, X. S., Xiong, X., Zhang, X., Zhang, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-10283-4 · Cited by 41 · see citing works
Antidepressant-like effects of glucagon-like peptide-2 in mice occur via monoamine pathways
Iwai, T., Hayashi, Y., Narita, S., Kasuya, Y., Jin, K., Tsugane, M., & Oka, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.020 · Cited by 39 · see citing works
Lee, K., Kobayashi, Y., Seo, H., Kwak, J., Masuda, A., Lim, C., Lee, H., Kang, S. J., Park, P., Sim, S.-E., et al. (2015) · Molecular Brain · doi:10.1186/s13041-015-0130-1 · Cited by 39 · see citing works
Radiation-induced overexpression of transthyretin inhibits retinol-mediated hippocampal neurogenesis
Kang, J., Kim, W., Seo, H., Kim, E., Son, B., Lee, S., Park, G., Jo, S., Moon, C., Youn, H., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-26762-1 · Cited by 39 · see citing works
Chronic Cerebral Hypoperfusion Induced Synaptic Proteome Changes in the rat Cerebral Cortex
Völgyi, K., Gulyássy, P., Todorov, M. I., Puska, G., Badics, K., Hlatky, D., Kékesi, K. A., Nyitrai, G., Czurkó, A., Drahos, L., et al. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0641-0 · Cited by 35 · see citing works
Glucagon-like peptide-2 but not imipramine exhibits antidepressant-like effects in ACTH-treated mice
Iwai, T., Ohnuki, T., Sasaki‐Hamada, S., Saitoh, A., Sugiyama, A., & Oka, J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.010 · Cited by 34 · see citing works
Yang, C., Zhang, X., Gao, J., Wang, M., & Yang, Z. R. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.121 · Cited by 33 · see citing works
Yao, Z., Zhang, J., & Xie, X. (2012) · Current Neurovascular Research · doi:10.2174/156720212801618974 · Cited by 32 · see citing works
Self-citationShi, X., Li, X., Wang, Y., Zhang, K., Zhou, F., Chan, L., Li, D., & Guan, X. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00620.2010 · Cited by 27 · see citing works
Glucagon-like peptide-2-induced memory improvement and anxiolytic effects in mice
Iwai, T., Jin, K., Ohnuki, T., Sasaki‐Hamada, S., Nakamura, M., Saitoh, A., Sugiyama, A., Ikeda, M., Tanabe, M., & Oka, J. (2014) · Neuropeptides · doi:10.1016/j.npep.2014.11.001 · Cited by 25 · see citing works
Tang, H., Gao, Y., Zhang, Q., Nie, K., Zhu, R., Gao, L., Feng, S., Wang, L., Zhao, J., Huang, Z., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.061 · Cited by 25 · see citing works
Self-citationO’Riordan, K. J., Hu, N., & Rowan, M. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-22768-x · Cited by 25 · see citing works
Park, J., & Lee, C. H. (2017) · Journal of Veterinary Science · doi:10.4142/jvs.2017.18.1.11 · Cited by 24 · see citing works
Wang, Y., & Guan, X. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00585.2009 · Cited by 22 · see citing works
Oxiracetam can improve cognitive impairment after chronic cerebral hypoperfusion in rats
Yao, X.-L., Yao, Z., Li, L., Nie, L., & Zhang, S.-F. (2016) · Psychiatry Research · doi:10.1016/j.psychres.2016.10.006 · Cited by 21 · see citing works
Self-citationGlucagon-like peptide-2 exhibits protective effect on hepatic ischemia-reperfusion injury in rats
Topaloğlu, N., Küçük, A., Yıldırım, Ş., Tekin, M., Erdem, H., & Deniz, M. (2015) · Frontiers of Medicine · doi:10.1007/s11684-015-0403-1 · Cited by 6 · see citing works
Nilsson (1999) · doi:10.1002/(sici)1097-4695(19990615)39:4
Flagged first, then by citations
Cited by
Sorted by citations
Kundu, P., Torres, E. R. S., Stagaman, K., Kasschau, K., Okhovat, M., Holden, S., Ward, S., Nevonen, K. A., Davis, B. A., Saito, T., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-83851-4 · Cited by 75 · see citing works
Wang, D., Yin, H., Lin, Q. D., Fang, S.-P., Shen, J.-H., Wu, Y., Su, S.-H., & Hai, J. (2019) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-019-01672-9 · Cited by 57 · see citing works
Yao, Z., Wang, J., Yuan, J., Xiao, K., Zhang, S., Xie, Y., & Mei, J. (2021) · Aging · doi:10.18632/aging.202555 · Cited by 34 · see citing works
Self-citationCao, W., Lin, J., Xiang, W., Liu, J., Wang, B., Liao, W., & Jiang, T. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.866336 · Cited by 29 · see citing works
Su, Y., Zhang, Z., Li, H., Ma, J., Sun, L., Shao, S., Zhang, Z., & Hölscher, C. (2020) · Drug Research · doi:10.1055/a-1266-3263 · Cited by 27 · see citing works
Gao, J., Yao, M., Chang, D., & Liu, J. (2022) · Stroke · doi:10.1161/strokeaha.122.040376 · Cited by 26 · see citing works
Wang, N., Ma, J., Liu, J., Wang, J., Liu, C., Wang, H., Liu, Y. U., Yan, H., & Jiang, S. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01583 · Cited by 23 · see citing works
Gao, J., Liu, J., Yao, M., Zhang, W., Yang, B., & Wang, G. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.889404 · Cited by 20 · see citing works
Systemic Inflammation Causes Microglial Dysfunction With a Vascular AD phenotype
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fischer, A., Ballabani, E., Doucey, M., & Alberi, L. A. (2022) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2022.100568 · Cited by 20 · see citing works
Neuroprotective Effects of a GLP-2 Analogue in the MPTP Parkinson’s Disease Mouse Model
Zhang, Z., Li, H., Shi, M., Yu, Z., Shao, S., Yuan, Y., Zhang, Z., & Hölscher, C. (2021) · Journal of Parkinson s Disease · doi:10.3233/jpd-202318 · Cited by 19 · see citing works
Protective potential of glucagon like peptide 2 (GLP-2) against the neurodegeneration
Mulè, F., & Amato, A. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.259612 · Cited by 17 · see citing works
Wang, D., Lv, Q., Lin, Q. D., Kang, K., Jin, K.-Y., & Hai, J. (2019) · Neurotoxicity Research · doi:10.1007/s12640-019-00141-8 · Cited by 15 · see citing works
Ang, M. J., Kim, J., Lee, S., Kim, S., Kim, J.-C., Jeon, T., Im, S., & Moon, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114131 · Cited by 13 · see citing works
Głombik, K., Detka, J., Kukla‐Bartoszek, M., Maciejska, A., & Budziszewska, B. (2022) · Pharmacological Reports · doi:10.1007/s43440-022-00395-8 · Cited by 11 · see citing works
Ang, M. J., Lee, S., Wada, M., Weerasinghe-Mudiyanselage, P. D. E., Kim, S., Shin, T., Jeon, T., Im, S., & Moon, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116103 · Cited by 10 · see citing works
Liu, J., Zhang, Z.-Q., Zhu, Z., Li, K., Xu, Q., Zhang, J., Cheng, X., Li, H., Sun, Y., Wang, J., et al. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01302-2 · Cited by 8 · see citing works
Yang, L., Wu, W., Jiang, W., Zhu, C., & Yao, Z. (2023) · Aging · doi:10.18632/aging.204654 · Cited by 4 · see citing works
Self-citationPareek, T., Vergis, J. M., Zhang, X., Platt, D. M., Grant, K. A., McCullumsmith, R., Gisabella, B., O'Donovan, S. M., & Pantazopoulos, H. (2026) · Scientific Reports · doi:10.1038/s41598-026-51816-0 · Cited by 1 · see citing works
Czarnecki, M., Baranowska-Bik, A., Litwiniuk, A., Kalisz, M., Domańska, A., Kurdyła, A., & Bik, W. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27031609 · Cited by 1 · see citing works
Systemic inflammation causes microglial dysfunction with a mixed AD-like pathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fischer, A., Ballabani, E., Doucey, M., & Alberi, L. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.27.223198 · Cited by 1 · see citing works
Systemic Inflammation Causes Microglial Dysfunction with a Mixed AD-Like Pathology.Preprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fisher, A., Babaliani, E., Doucey, M., & Alberi, L. A. (2020) · Research Square · doi:10.21203/rs.3.rs-48807/v1
Systemic inflammation causes microglial dysfunction with a mixed AD-like pathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fischer, A., Ballabani, E., Doucey, M., & Alberi, L. A. (2021) · Research Square · doi:10.21203/rs.3.rs-145868/v1
Systemic Inflammation Causes Microglial Dysfunction With a Mixed Ad-like PathologyPreprint
Bathini, P., Dupanloup, I., Zenaro, E., Terrabuio, E., Fisher, A., Babaliani, E., Doucey, M., & Alberi, L. A. (2020) · Research Square · doi:10.21203/rs.3.rs-80087/v1
Jiang, Y., Han, G., Zhang, Z., Hu, S., & Mu, M. (2026) · Comprehensive physiology · doi:10.1002/cph4.70144
- Authors
- Xie, Y.-C., Yao, Z.-H., Yao, X.-L., Pan, J.-Z., Zhang, S.-F., Zhang, Y., & Hu, J.-C.
- Affiliations
- Department of Neurology, Renmin Hospital of Wuhan University, Wuhan, China
- Department of Geriatrics, Renmin Hospital of Wuhan University, Wuhan, China
- Zhengzhou Central Hospital (CN)
- Renmin Hospital of Wuhan University (CN)
- Department of Pathology, Renmin Hospital of Wuhan University, Wuhan, China
- ORCID
- Zhang, Yong
- Venue
- Journal of Alzheimer's Disease
- Publisher
- SAGE Publications
- Published
- 2018-12-12
- Volume
- 66
- Issue
- 4
- Pages
- 1559-1576
- ISSN
- 1387-2877 (ISSN-L)
- 1875-8908
- OpenAlex
- W2901051078
- Cited by
- 24
- References
- 85
- Citations by year
- 2026: 3 · 2024: 1 · 2023: 1 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 3
- FWCI
- 1.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Alzheimer s Disease (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- chronic cerebral hypoperfusion
- MeSH terms
- Glucagon-Like Peptide-2 Receptor, Animals, Brain Ischemia, Disease Models, Animal, Hippocampus, Male, Neuronal Plasticity, Neurons, Phosphorylation, Signal Transduction, Up-Regulation, Rats, Sprague-Dawley, Dendritic Spines, Proto-Oncogene Proteins c-akt, Rats, TOR Serine-Threonine Kinases, Spatial Memory, Spatial Learning
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review