Regulation of hippocampus-dependent memory by the zinc finger protein Zbtb20 in mature CA1 neurons

Journal of Physiology

Volumn 590, Issue 19, 2012, Pages 4917-4932

  Ren, Anjing ^a   Zhang, Huan ^a,b   Xie, Zhifang ^a   Ma, Xianhua ^a   Ji, Wenli ^a   He, David Z Z ^c   Yuan, Wenjun ^b   Ding, Yu Qiang ^d   Zhang, Xiao Hui ^e   Zhang, Weiping J ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b NINGXIA MEDICAL UNIVERSITY   (China)

^c CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^e Chinese Academy of Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; ZBTB20 PROTEIN; ZINC FINGER PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; LEARNING; LONG TERM POTENTIATION; MAZE TEST; MEMORY; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; SURVIVAL; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; WESTERN BLOTTING;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; LONG-TERM POTENTIATION; MEMORY; MICE; MICE, KNOCKOUT; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE; TRANSCRIPTION FACTORS;

EID: 84866875460     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.234187     Document Type: Article

References (50)

1. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM & Sweatt JD (1998). The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1, 602-609.
2. Benito E & Barco A (2010). CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33, 230-240.
3. Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S, Seabold GK, Mathur P, Davis MI, Bock R, Gustin RM, Colbran RJ, Alvarez VA, Nakazawa K, Delpire E, Lovinger DM & Holmes A (2010). Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci 30, 4590-4600.
4. Chan CS, Levenson JM, Mukhopadhyay PS, Zong L, Bradley A, Sweatt JD & Davis RL (2007). α3-Integrins are required for hippocampal long-term potentiation and working memory. Learn Mem 14, 606-615.
5. Cull-Candy SG & Leszkiewicz DN (2004). Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004, re16.
6. Dai JX, Han HL, Tian M, Cao J, Xiu JB, Song NN, Huang Y, Xu TL, Ding YQ & Xu L (2008). Enhanced contextual fear memory in central serotonin-deficient mice. Proc Natl Acad Sci U S A 105, 11981-11986.
7. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
8. English JD & Sweatt JD (1997). A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272, 19 103-19 106.
9. Fourgeaud L, Davenport CM, Tyler CM, Cheng TT, Spencer MB & Boulanger LM (2010). MHC class I modulates NMDA receptor function and AMPA receptor trafficking. Proc Natl Acad Sci U S A 107, 22278-22283.
10. Fukaya M, Kato A, Lovett C, Tonegawa S & Watanabe M (2003). Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc Natl Acad Sci U S A 100, 4855-4860.
11. 2+/calmodulin-dependent protein kinase II. J Biol Chem 268, 7863-7867.
12. Gould TD, O'Donnell KC, Picchini AM, Dow ER, Chen G & Manji HK (2008). Generation and behavioral characterization of β-catenin forebrain-specific conditional knock-out mice. Behav Brain Res 189, 117-125.
13. Gresack JE, Schafe GE, Orr PT & Frick KM (2009). Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation. Neuroscience 159, 451-467.
14. Gustafsson B, Wigstrom H, Abraham WC & Huang YY (1987). Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci 7, 774-780.
15. 2+ exchanger 2. Neuron 38, 965-976.
16. Kolb B, Buhrmann K, McDonald R & Sutherland RJ (1994). Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 4, 664-680.
17. Lau CG & Zukin RS (2007). NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8, 413-426.
18. Lein ES, Callaway EM, Albright TD & Gage FH (2005). Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. J Comp Neurol 485, 1-10.
19. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP & Wang YT (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024.
20. Lynch MA (2004). Long-term potentiation and memory. Physiol Rev 84, 87-136.
21. Malenka RC & Nicoll RA (1999). Long-term potentiation - a decade of progress? Science 285, 1870-1874.
22. 2+-dependent protein kinases with subsequent presynaptic enhancement. Prog Brain Res 89, 271-289.
23. Martin SJ, Grimwood PD & Morris RG (2000). Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23, 649-711.
24. Mitchelmore C, Kjaerulff KM, Pedersen HC, Nielsen JV, Rasmussen TE, Fisker MF, Finsen B, Pedersen KM & Jensen NA (2002). Characterization of two novel nuclear BTB/POZ domain zinc finger isoforms. Association with differentiation of hippocampal neurons, cerebellar granule cells, and macroglia. J Biol Chem 277, 7598-7609.
25. Mizuno K & Giese KP (2010). Towards a molecular understanding of sex differences in memory formation. Trends Neurosci 33, 285-291.
26. Nguyen PV & Kandel ER (1997). Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4, 230-243.
27. Nielsen JV, Blom JB, Noraberg J & Jensen NA (2010). Zbtb20-induced CA1 pyramidal neuron development and area enlargement in the cerebral midline cortex of mice. Cereb Cortex 20, 1904-1914.
28. Nielsen JV, Nielsen FH, Ismail R, Noraberg J & Jensen NA (2007). Hippocampus-like corticoneurogenesis induced by two isoforms of the BTB-zinc finger gene Zbtb20 in mice. Development 134, 1133-1140.
29. Phillips RG & LeDoux JE (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106, 274-285.
30. Pokorny J & Yamamoto T (1981a). Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborisation in pyramidal neurons. Brain Res Bull 7, 113-120.
31. Pokorny J & Yamamoto T (1981b). Postnatal ontogenesis of hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 7, 121-130.
32. Regehr WG, Delaney KR & Tank DW (1994). The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14, 523-537.
33. Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C & Sweatt JD (1999). The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19, 4337-4348.
34. Roberson ED & Sweatt JD (1996). Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271, 30436-30441.
35. Sakimura K, Kutsuwada T, Ito I, Manabe T, Takayama C, Kushiya E, Yagi T, Aizawa S, Inoue Y, Sugiyama H et al. (1995). Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature 373, 151-155.
36. Stanciu M, Radulovic J & Spiess J (2001). Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to Fos production. Brain Res Mol Brain Res 94, 15-24.
37. Stanfield BB & Cowan WM (1979). The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185, 423-459.
38. Sutherland AP, Zhang H, Zhang Y, Michaud M, Xie Z, Patti ME, Grusby MJ & Zhang WJ (2009). Zinc finger protein Zbtb20 is essential for postnatal survival and glucose homeostasis. Mol Cell Biol 29, 2804-2815.
39. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G & Tsien JZ (1999). Genetic enhancement of learning and memory in mice. Nature 401, 63-69.
40. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, Mayford M, Kandel ER & Tonegawa S (1996a). Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87, 1317-1326.
41. Tsien JZ, Huerta PT & Tonegawa S (1996b). The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87, 1327-1338.
42. Vaccarino F, Guidotti A & Costa E (1987). Ganglioside inhibition of glutamate-mediated protein kinase C translocation in primary cultures of cerebellar neurons. Proc Natl Acad Sci U S A 84, 8707-8711.
43. Waltereit R & Weller M (2003). Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27, 99-106.
44. Winder DG & Schramm NL (2001). Plasticity and behavior: new genetic techniques to address multiple forms and functions. Physiol Behav 73, 763-780.
45. Xie Z, Ma X, Ji W, Zhou G, Lu Y, Xiang Z, Wang YX, Zhang L, Hu Y, Ding YQ & Zhang WJ (2010). Zbtb20 is essential for the specification of CA1 field identity in the developing hippocampus. Proc Natl Acad Sci U S A 107, 6510-6515.
46. Xie Z, Zhang H, Tsai W, Zhang Y, Du Y, Zhong J, Szpirer C, Zhu M, Cao X, Barton MC, Grusby MJ & Zhang WJ (2008). Zinc finger protein ZBTB20 is a key repressor of alpha-fetoprotein gene transcription in liver. Proc Natl Acad Sci U S A 105, 10 859-10 864.
47. Zakharenko SS, Zablow L & Siegelbaum SA (2001). Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4, 711-717.
48. Zhang W, Mi J, Li N, Sui L, Wan T, Zhang J, Chen T & Cao X (2001). Identification and characterization of DPZF, a novel human BTB/POZ zinc finger protein sharing homology to BCL-6. Biochem Biophys Res Commun 282, 1067-1073.
49. Zhang Y, Xie Z, Zhou L, Li L, Zhang H, Zhou G, Ma X, Herrera PL, Liu Z, Grusby MJ & Zhang WJ (2012). The zinc finger protein ZBTB20 regulates transcription of fructose-1, 6-bisphosphatase 1 and β cell function in mice. Gastroenterology 142, 1571-1580.
50. Zorumski CF & Izumi Y (1998). Modulation of LTP induction by NMDA receptor activation and nitric oxide release. Prog Brain Res 118, 173-182.