Neuron-specific Sumo1-3 knockdown in mice impairs episodic and fear memories

Journal of Psychiatry and Neuroscience

Volumn 39, Issue 4, 2014, Pages 259-266

  Wang, Liangli ^a   Rodriguiz, Ramona M ^b   Wetsel, William C ^a,b,c   Sheng, Huaxin ^a   Zhao, Shengli ^c   Liu, Xiaozhi ^a   Paschen, Wulf ^a   Yang, Wei ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; MICRORNA; SUMO 1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CELL CULTURE; CONTROLLED STUDY; DENDRITIC SPINE; EMOTIONALITY; FEAR; GENE EXPRESSION; GENE SILENCING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NEUROPSYCHIATRY; NONHUMAN; QUANTITATIVE ANALYSIS; SEQUENCE ANALYSIS; SUMOYLATION; SYNAPTIC TRANSMISSION; ANIMAL; ANXIETY; ASSOCIATION; BRAIN; C57BL MOUSE; CONDITIONING; EMOTION; FLUORESCENT ANTIBODY TECHNIQUE; MEMORY; METABOLISM; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; STARTLE REFLEX; TRANSGENIC MOUSE;

ANIMALS; ANXIETY; BRAIN; CONDITIONING (PSYCHOLOGY); CUES; EMOTIONS; FEAR; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; IN SITU HYBRIDIZATION; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; NEURONS; NEUROPSYCHOLOGICAL TESTS; REFLEX, STARTLE;

EID: 84904122311     PISSN: 11804882     EISSN: 14882434     Source Type: Journal    
DOI: 10.1503/jpn.130148     Document Type: Article

References (40)

1. Matunis MJ, Wu J, Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J Cell Biol 1998;140:499-509.
2. Hay RT. SUMO: a history of modification. Mol Cell 2005;18:1-12.
3. Yang W, Sheng H, Warner DS, et al. Transient focal cerebral ischemia induces a dramatic activation of small ubiquitin-like modifier conjugation. J Cereb Blood Flow Metab 2008;28:892-6.
4. Tirard M, Hsiao HH, Nikolov M, et al. In vivo localization and identification of SUMOylated proteins in the brain of His6-HASUMO1 knock-in mice. Proc Natl Acad Sci U S A 2012;109:21122-7.
5. Wang L, Ma Q, Yang W, et al. Moderate hypothermia induces marked increase in levels and nuclear accumulation of SUMO2/ 3-conjugated proteins in neurons. J Neurochem 2012;123:349-59.
6. Craig TJ, Henley JM. Protein SUMOylation in spine structure and function. Curr Opin Neurobiol 2012;22:480-7.
7. Plant LD, Dowdell EJ, Dementieva IS, et al. SUMO modification of cell surface Kv2.1 potassium channels regulates the activity of rat hippocampal neurons. J Gen Physiol 2011;137:441-54.
8. Craig TJ, Jaafari N, Petrovic MM, et al. Homeostatic synaptic scaling is regulated by protein SUMOylation. J Biol Chem 2012;287:22781-8.
9. Martin S, Nishimune A, Mellor JR, et al. SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 2007;447:321-5.
10. Turrigiano GG. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008;135:422-35.
11. Loriol C, Khayachi A, Poupon G, et al. Activity-dependent regulation of the sumoylation machinery in rat hippocampal neurons. Biol Cell 2013;105:30-45.
12. Yang W, Wang L, Roehn G, et al. Small ubiquitin-like modifier 1-3 is activated in human astrocytic brain tumors and is required for glioblastoma cell survival. Cancer Sci 2013;104:70-7.
13. Wang L, Budolfson K, Wang F. Pik3c3 deletion in pyramidal neur-ons results in loss of synapses, extensive gliosis and progressive neurodegeneration. Neuroscience 2011;172:427-42.
14. Pogorelov VM, Rodriguiz RM, Insco ML, et al. Novelty seeking and stereotypic activation of behavior in mice with disruption of the Dat1 gene. Neuropsychopharmacology 2005;30:1818-31.
15. Porton B, Rodriguiz RM, Phillips LE, et al. Mice lacking synapsin III show abnormalities in explicit memory and conditioned fear. Genes Brain Behav 2010;9:257-68.
16. Grove M, Demyanenko G, Echarri A, et al. ABI2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol Cell Biol 2004;24:10905-22.
17. Feng G, Mellor RH, Bernstein M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000;28:41-51.
18. Vidal M, Morris R, Grosveld F, et al. Tissue-specific control elements of the Thy-1 gene. EMBO J 1990;9:833-40.
19. Chen Q, Cichon J, Wang W, et al. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 2012;76:297-308.
20. Walker MP, Tian L, Matera AG. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS ONE 2009;4:e6171.
21. Shalizi A, Gaudilliere B, Yuan Z, et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 2006;311:1012-7.
22. Chao HW, Hong CJ, Huang TN, et al. SUMOylation of the MAGUK protein CASK regulates dendritic spinogenesis. J Cell Biol 2008;182:141-55.
23. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274-85.
24. Fendt M, Fanselow MS. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 1999;23:743-60.
25. Dickins RA, McJunkin K, Hernando E, et al. Tissue-specific and reversible RNA interference in transgenic mice. Nat Genet 2007; 39:914-21.
26. McJunkin K, Mazurek A, Premsrirut PK, et al. Reversible suppression of an essential gene in adult mice using transgenic RNA interference. Proc Natl Acad Sci U S A 2011;108:7113-8.
27. Xia XG, Zhou H, Xu Z. Multiple shRNAs expressed by an inducible pol II promoter can knock down the expression of multiple target genes. Biotechniques 2006;41:64-8.
28. Premsrirut PK, Dow LE, Kim SY, et al. A rapid and scalable system for studying gene function in mice using conditional RNA inter ference. Cell 2011;145:145-58.
29. Mueller C, Tang Q, Gruntman A, et al. Sustained miRNAmediated knockdown of mutant AAT with simultaneous augmentation of wild-type AAT has minimal effect on global liver miRNA profiles. Mol Ther 2012;20:590-600.
30. Sun D, Melegari M, Sridhar S, et al. Multi-miRNA hairpin method that improves gene knockdown efficiency and provides linked multi-gene knockdown. Biotechniques 2006;41:59-63.
31. Yang W, Paschen W. Gene expression and cell growth are modified by silencing SUMO2 and SUMO3 expression. Biochem Biophys Res Commun 2009;382:215-8.
32. Demarque MD, Nacerddine K, Neyret-Kahn H, et al. Sumoylation by Ubc9 regulates the stem cell compartment and structure and function of the intestinal epithelium in mice. Gastroenterology 2011; 140:286-96.
33. Yang W, Sheng H, Warner DS, et al. Transient global cerebral ischemia induces a massive increase in protein sumoylation. J Cereb Blood Flow Metab 2008;28:269-79.
34. Treit D, Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 1988;31:959-62.
35. Dere E, Huston JP, De Souza Silva MA. The pharmacology, neuro-anatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 2007;31:673-704.
36. Lyons GE, Micales BK, Schwarz J, et al. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 1995;15:5727-38.
37. Chapman PF, Ramsay MF, Krezel W, et al. Synaptic plasticity in the amygdala: comparisons with hippocampus. Ann N Y Acad Sci 2003;985:114-24.
38. Moser MB, Trommald M, Andersen P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci U S A 1994;91:12673-5.
39. Ostroff LE, Cain CK, Bedont J, et al. Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proc Natl Acad Sci U S A 2010;107:9418-23.
40. Schafe GE, Nadel NV, Sullivan GM, et al. Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 1999;6:97-110.