Impaired Hippocampal Synaptic Plasticity and Enhanced Excitatory Transmission in a Novel Animal Model of Autism Spectrum Disorders with Telomerase Reverse Transcriptase Overexpression |
Rhee, Jeehae
(Department of Biological Sciences, College of Bioscience and Biotechnology, School of Medicine, Konkuk University)
Park, Kwanghoon (Department of Biological Sciences, College of Bioscience and Biotechnology, School of Medicine, Konkuk University) Kim, Ki Chan (Department of Neuroscience and Department of Advanced Translational Medicine, School of Medicine, Konkuk University) Shin, Chan Young (Department of Neuroscience and Department of Advanced Translational Medicine, School of Medicine, Konkuk University) Chung, ChiHye (Department of Biological Sciences, College of Bioscience and Biotechnology, School of Medicine, Konkuk University) |
1 | Prior, M., and Hoffmann, W. (1990). Brief report: neuropsychological testing of autistic children through an exploration with frontal lobe tests. J. Autism. Dev. Disord. 20, 581-590. DOI |
2 | Puscian, A., Leski, S., Gorkiewicz, T., Meyza, K., Lipp, H.P., and Knapska, E. (2014). A novel automated behavioral test battery assessing cognitive rigidity in two genetic mouse models of autism. Front Behav. Neurosci. 8, 140. |
3 | Qiao, F., Gao, X.P., Yuan, L., Cai, H.Y., and Qi, J.S. (2014). Apolipoprotein E4 impairs in vivo hippocampal long-term synaptic plasticity by reducing the phosphorylation of CaMKIIalpha and CREB. J. Alzheimers Dis. 41, 1165-1176. DOI |
4 | Rendall, A.R., Truong, D.T., and Fitch, R.H. (2016). Learning delays in a mouse model of Autism Spectrum Disorder. Behav. Brain Res. 303, 201-207. DOI |
5 | Riazi, K., Galic, M.A., Kentner, A.C., Reid, A.Y., Sharkey, K.A., and Pittman, Q.J. (2015). Microglia-dependent alteration of glutamatergic synaptic transmission and plasticity in the hippocampus during peripheral inflammation. J. Neurosci. 35, 4942-4952. DOI |
6 | Rubenstein, J.L., and Merzenich, M.M. (2003). Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255-267. DOI |
7 | Stein, V., House, D.R., Bredt, D.S., and Nicoll, R.A. (2003). Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci.23, 5503-5506. DOI |
8 | Sudhof, T.C. (2008). Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911. DOI |
9 | Sweatt, J.D. (1999). Toward a molecular explanation for long-term potentiation. Learn Mem. 6, 399-416. DOI |
10 | Villers, A., Giese, K.P., and Ris, L. (2014). Long-term potentiation can be induced in the CA1 region of hippocampus in the absence of alphaCaMKII T286-autophosphorylation. Learn Mem. 21, 616-626. DOI |
11 | Voikar, V., Koks, S., Vasar, E., and Rauvala, H. (2001). Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol. Behav. 72, 271-281. DOI |
12 | Wang, H., Feng, R., Phillip Wang, L., Li, F., Cao, X., and Tsien, J.Z. (2008). CaMKII activation state underlies synaptic labile phase of LTP and short-term memory formation. Curr. Biol. 18, 1546-1554. DOI |
13 | Won, H., Lee, H.R., Gee, H.Y., Mah, W., Kim, J.I., Lee, J., Ha, S., Chung, C., Jung, E.S., Cho, Y.S., et al. (2012). Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 486, 261-265. DOI |
14 | Yu, X., and Ren, T. (2013). Disruption of calmodulin-dependent protein kinase II alpha/brain-derived neurotrophic factor (alpha-CaMKII/BDNF) signalling is associated with zinc deficiency-induced impairments in cognitive and synaptic plasticity. Br. J. Nutr. 110, 2194-2200. DOI |
15 | Zhang, M.M., Yu, K., Xiao, C., and Ruan, D.Y. (2003). The influence of developmental periods of sodium valproate exposure on synaptic plasticity in the CA1 region of rat hippocampus. Neurosci. Lett. 351, 165-168. DOI |
16 | Zhao, X., Malhotra, G.K., Lele, S.M., Lele, M.S., West, W.W., Eudy, J.D., Band, H., and Band, V. (2010). Telomerase-immortalized human mammary stem/progenitor cells with ability to self-renew and differentiate. Proc. Natl. Acad. Sci. USA 107, 14146-14151. DOI |
17 | Park, J.I., Venteicher, A.S., Hong, J.Y., Choi, J., Jun, S., Shkreli, M., Chang, W., Meng, Z., Cheung, P., Ji, H., et al. (2009). Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 460, 66-72. DOI |
18 | Matsumoto, S., Banine, F., Struve, J., Xing, R., Adams, C., Liu, Y., Metzger, D., Chambon, P., Rao, M.S., and Sherman, L.S. (2006). Brg1 is required for murine neural stem cell maintenance and gliogenesis. Dev. Biol. 289, 372-383. DOI |
19 | Moyzis, R.K., Buckingham, J.M., Cram, L.S., Dani, M., Deaven, L.L., Jones, M.D., Meyne, J., Ratliff, R.L., and Wu, J.R. (1988). A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl. Acad. Sci. USA 85, 6622-6626. DOI |
20 | Owen, E.H., Logue, S.F., Rasmussen, D.L., and Wehner, J.M. (1997). Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80, 1087-1099. DOI |
21 | Peca, J., Feliciano, C., Ting, J.T., Wang, W., Wells, M.F., Venkatraman, T.N., Lascola, C.D., Fu, Z., and Feng, G. (2011). Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472, 437-442. DOI |
22 | Penagarikano, O., Abrahams, B.S., Herman, E.I., Winden, K.D., Gdalyahu, A., Dong, H., Sonnenblick, L.I., Gruver, R., Almajano, J., Bragin, A., et al. (2011). Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 147, 235-246. DOI |
23 | Pollak, D.D., Herkner, K., Hoeger, H., and Lubec, G. (2005). Behavioral testing upregulates pCaMKII, BDNF, PSD-95 and egr-1 in hippocampus of FVB/N mice. Behav. Brain Res. 163, 128-135. DOI |
24 | Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., and Silva, A.J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68. DOI |
25 | Appleby, V.J., Correa, S.A., Duckworth, J.K., Nash, J.E., Noel, J., Fitzjohn, S.M., Collingridge, G.L., and Molnar, E. (2011). LTP in hippocampal neurons is associated with a CaMKII-mediated increase in GluA1 surface expression. J. Neurochem. 116, 530-543. DOI |
26 | Autexier, C., and Lue, N.F. (2006). The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75, 493-517. DOI |
27 | Beeri, R., Le Novere, N., Mervis, R., Huberman, T., Grauer, E., Changeux, J.P., and Soreq, H. (1997). Enhanced hemicholinium binding and attenuated dendrite branching in cognitively impaired acetylcholinesterase-transgenic mice. J. Neurochem. 69, 2441-2451. |
28 | Brielmaier, J., Matteson, P.G., Silverman, J.L., Senerth, J.M., Kelly, S., Genestine, M., Millonig, J.H., DiCicco-Bloom, E., and Crawley, J.N. (2012). Autism-relevant social abnormalities and cognitive deficits in engrailed-2 knockout mice. PloS One 7, e40914. DOI |
29 | Brown, R.E., and Wong, A.A. (2007). The influence of visual ability on learning and memory performance in 13 strains of mice. Learn. Mem. 14, 134-144. DOI |
30 | Caron, M.J., Mottron, L., Rainville, C., and Chouinard, S. (2004). Do high functioning persons with autism present superior spatial abilities? Neuropsychologia 42, 467-481. DOI |
31 | Duffney, L.J., Zhong, P., Wei, J., Matas, E., Cheng, J., Qin, L., Ma, K., Dietz, D.M., Kajiwara, Y., Buxbaum, J.D., et al. (2015). Autism-like deficits in Shank3-deficient mice are rescued by targeting actin regulators. Cell Rep. 11, 1400-1413. DOI |
32 | Cheng, A., Shin-ya, K., Wan, R., Tang, S.C., Miura, T., Tang, H., Khatri, R., Gleichman, M., Ouyang, X., Liu, D., et al. (2007). Telomere protection mechanisms change during neurogenesis and neuronal maturation: newly generated neurons are hypersensitive to telomere and DNA damage. J. Neurosci. 27, 3722-3733. DOI |
33 | Choi, J., Southworth, L.K., Sarin, K.Y., Venteicher, A.S., Ma, W., Chang, W., Cheung, P., Jun, S., Artandi, M.K., Shah, N., et al. (2008). TERT promotes epithelial proliferation through transcriptional control of a Myc- and Wnt-related developmental program. PLoS Genet. 4, e10. DOI |
34 | Codagnone, M.G., Podesta, M.F., Uccelli, N.A., and Reines, A. (2015). Differential local connectivity and neuroinflammation profiles in the medial prefrontal cortex and hippocampus in the valproic acid rat model of autism. Dev. Neurosci. 37, 215-231. DOI |
35 | Eberhardt, M., Salmon, P., von Mach, M.A., Hengstler, J.G., Brulport, M., Linscheid, P., Seboek, D., Oberholzer, J., Barbero, A., Martin, I., et al. (2006). Multipotential nestin and Isl-1 positive mesenchymal stem cells isolated from human pancreatic islets. Biochem. Biophys. Res. Commun. 345, 1167-1176. DOI |
36 | Farley, S.J., McKay, B.M., Disterhoft, J.F., and Weiss, C. (2011). Reevaluating hippocampus-dependent learning in FVB/N mice. Behav. Neurosci. 125, 871-878. DOI |
37 | Edgin, J.O., and Pennington, B.F. (2005). Spatial cognition in autism spectrum disorders: Superior, impaired, or just intact? J. Autism Dev. Disord. 35, 729-745. DOI |
38 | Errijgers, V., Van Dam, D., Gantois, I., Van Ginneken, C.J., Grossman, A.W., D'Hooge, R., De Deyn, P.P., and Kooy, R.F. (2007). FVB.129P2-Pde6b(+) Tyr(c-ch)/Ant, a sighted variant of the FVB/N mouse strain suitable for behavioral analysis. Genes Brain Behav. 6, 552-557. DOI |
39 | Etherton, M., Foldy, C., Sharma, M., Tabuchi, K., Liu, X., Shamloo, M., Malenka, R.C., and Sudhof, T.C. (2011). Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proc. Natl. Acad. Sci. USA 108, 13764-13769. DOI |
40 | Etherton, M.R., Blaiss, C.A., Powell, C.M., and Sudhof, T.C. (2009). Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. USA 106, 17998-18003. DOI |
41 | Frankiewicz, T., and Parsons, C.G. (1999). Memantine restores long term potentiation impaired by tonic N-methyl-D-aspartate (NMDA) receptor activation following reduction of in hippocampal slices. Neuropharmacology 38, 1253-1259. DOI |
42 | Gao, J., Wang, X., Sun, H., Cao, Y., Liang, S., Wang, H., Wang, Y., Yang, F., Zhang, F., and Wu, L. (2016). Neuroprotective effects of docosahexaenoic acid on hippocampal cell death and learning and memory impairments in a valproic acid-induced rat autism model. Int. J. Dev. Neurosci. 49, 67-78. DOI |
43 | Kim, K.C., Rhee, J., Park, J.E., Lee, D.K., Choi, C.S., Kim, J.W., Lee, H.W., Song, M.R., Yoo, H.J., Chung, C., et al. (2015). Overexpression of telomerase reverse transcriptase induces autism-like excitatory phenotypes in mice. Mol. Neurobiol. 53, 7312-7328. |
44 | Gogolla, N., Leblanc, J.J., Quast, K.B., Sudhof, T.C., Fagiolini, M., and Hensch, T.K. (2009). Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J. Neurodev. Disord. 1, 172-181. DOI |
45 | Harley, C.B., Futcher, A.B., and Greider, C.W. (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460. DOI |
46 | Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., and Cole, G. (1996). Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102. DOI |
47 | Kang, H.J., Choi, Y.S., Hong, S.B., Kim, K.W., Woo, R.S., Won, S.J., Kim, E.J., Jeon, H.K., Jo, S.Y., Kim, T.K., et al. (2004). Ectopic expression of the catalytic subunit of telomerase protects against brain injury resulting from ischemia and NMDA-induced neurotoxicity. J. Neurosci. 24, 1280-1287. DOI |
48 | Kempermann, G., and Gage, F.H. (2002). Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur. J. Neurosci. 16, 129-136. DOI |
49 | Kim, S., Kim, M.S., Park, K., Kim, H.J., Jung, S.W., Nah, S.Y., Han, J.S., and Chung, C. (2016). Hippocampus-dependent cognitive enhancement induced by systemic gintonin administration. J. Ginseng Res. 40, 55-61. DOI |
50 | Kouser, M., Speed, H.E., Dewey, C.M., Reimers, J.M., Widman, A.J., Gupta, N., Liu, S., Jaramillo, T.C., Bangash, M., Xiao, B., et al. (2013). Loss of predominant Shank3 isoforms results in hippocampusdependent impairments in behavior and synaptic transmission. J. Neurosci. 33, 18448-18468. DOI |
51 | Lee, J., Chung, C., Ha, S., Lee, D., Kim, D.Y., Kim, H., and Kim, E. (2015). Shank3-mutant mice lacking exon 9 show altered excitation/inhibition balance, enhanced rearing, and spatial memory deficit. Front Cell Neurosci. 9, 94. |
52 | Lind, S.E., Williams, D.M., Raber, J., Peel, A., and Bowler, D.M. (2013). Spatial navigation impairments among intellectually highfunctioning adults with autism spectrum disorder: exploring relations with theory of mind, episodic memory, and episodic future thinking. J. Abnorm Psychol. 122, 1189-1199. DOI |