Conditional Knockout of Tumor Overexpressed Gene in Mouse Neurons Affects RNA Granule Assembly, Granule Translation, LTP and Short Term Habituation

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Barbarese, Elisa ^a   Ifrim, Marius F ^a,b   Hsieh, Lawrence ^a   Guo, Caiying ^a,c   Tatavarty, Vedakumar ^a,d   Maggipinto, Michael J ^a   Korza, George ^a   Tutolo, Jessica W ^a   Giampetruzzi, Anthony ^a   Le, Hien ^a   Ma, Xin Ming ^a   Levine, Eric ^a   Bishop, Brian ^a   Kim, Duck O ^a   Kuwada, Shigeyuki ^a   Carson, John H ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BINDING PROTEIN; MESSENGER RNA; TUMOR OVEREXPRESSED GENE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL GRANULE; CONTROLLED STUDY; HABITUATION; HIPPOCAMPUS; HYPERACTIVITY; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; RNA ANALYSIS; RNA TRANSLATION; SENSITIVITY ANALYSIS;

ANIMALS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; CYTOSKELETON; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENE KNOCKOUT TECHNIQUES; HABITUATION, PSYCHOPHYSIOLOGIC; LONG-TERM POTENTIATION; MALE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PROTEIN BIOSYNTHESIS; RNA; SYNAPSES;

EID: 84881146010     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069989     Document Type: Article

References (65)

1. Al-Bassam J, Larsen NA, Hyman AA, Harrison SC, (2007) Crystal structure of a TOG domain: Conserved features of XMAP215/Dis1-family TOG domains and implications for tubulin binding. Structure 15: 355-362.
2. Al-Bassam J, Chang F, (2011) Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol 21: 604-614.
3. Gard DL, Kirschner MW, (1987) A microtubule-associated protein from xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol 105: 2203-2215.
4. Widlund PO, Stear JH, Pozniakovsky A, Zanic M, Reber S, et al. (2011) XMAP215 polymerase activity is built by combining multiple tubulin-binding TOG domains and a basic lattice-binding region. Proc Natl Acad Sci U S A 108: 2741-2746.
5. Charrasse S, Schroeder M, Gauthier-Rouviere C, Ango F, Cassimeris L, et al. (1998) The TOGp protein is a new human microtubule-associated protein homologous to the xenopus XMAP215. J Cell Sci 111 (Pt 10): 1371-1383.
6. Cassimeris L, Morabito J, (2004) TOGp, the human homolog of XMAP215/Dis1, is required for centrosome integrity, spindle pole organization, and bipolar spindle assembly. Mol Biol Cell 15: 1580-1590.
7. Kosturko LD, Maggipinto MJ, D'Sa C, Carson JH, Barbarese E, (2005) The microtubule-associated protein tumor overexpressed gene binds to the RNA trafficking protein heterogeneous nuclear ribonucleoprotein A2. Mol Biol Cell 16: 1938-1947.
8. Gao Y, Tatavarty V, Korza G, Levin MK, Carson JH, (2008) Multiplexed dendritic targeting of alpha calcium calmodulin-dependent protein kinase II, neurogranin, and activity-regulated cytoskeleton-associated protein RNAs by the A2 pathway. Mol Biol Cell 19: 2311-2327.
9. Hirokawa N, (2006) mRNA transport in dendrites: RNA granules, motors, and tracks. J Neurosci 26: 7139-7142.
10. Kiebler MA, Bassell GJ, (2006) Neuronal RNA granules: Movers and makers. Neuron 51: 685-690.
11. Tatavarty V, Ifrim MF, Levin M, Korza G, Barbarese E, et al. (2012) Single-molecule imaging of translational output from individual RNA granules in neurons. Mol Biol Cell 23: 918-929.
12. Bramham CR, Worley PF, Moore MJ, Guzowski JF, (2008) The immediate early gene arc/arg3.1: Regulation, mechanisms, and function. J Neurosci 28: 11760-11767.
13. Steward O, Schuman EM, (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24: 299-325.
14. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, et al. (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52: 445-459.
15. Shepherd JD, Rumbaugh G, Wu J, Chowdhury S, Plath N, et al. (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52: 475-484.
16. Deacon RM, (2006) Burrowing in rodents: A sensitive method for detecting behavioral dysfunction. Nat Protoc 1: 118-121.
17. Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, et al. (2009) Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 204: 361-373.
18. Deacon RM, Rawlins JN, (2005) Hippocampal lesions, species-typical behaviours and anxiety in mice. Behav Brain Res 156: 241-249.
19. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, et al. (1996) Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87: 1317-1326.
20. Tang SH, Silva FJ, Tsark WM, Mann JR, (2002) A cre/loxP-deleter transgenic line in mouse strain 129S1/SvImJ. Genesis 32: 199-202.
21. Goslin K, Banker G, (1989) Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108: 1507-1516.
22. Grutzendler J, Tsai J, Gan WB, (2003) Rapid labeling of neuronal populations by ballistic delivery of fluorescent dyes. Methods 30: 79-85.
23. Kiraly DD, Ma XM, Mazzone CM, Xin X, Mains RE, et al. (2010) Behavioral and morphological responses to cocaine require kalirin7. Biol Psychiatry 68: 249-255.
24. Grossman AW, Elisseou NM, McKinney BC, Greenough WT, (2006) Hippocampal pyramidal cells in adult Fmr1 knockout mice exhibit an immature-appearing profile of dendritic spines. Brain Res 1084: 158-164.
25. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, second edition. San Diego, CA: Academic Press. 296 p.
26. Bortolotto ZA, Amici M, Anderson WW, Isaac JT, Collingridge GL (2011) Synaptic plasticity in the hippocampal slice preparation. Curr Protoc Neurosci Chapter 6: Unit 6.13.
27. Crawley JN, Paylor R, (1997) A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm Behav 31: 197-211.
28. D'Hooge R, Hartmann D, Manil J, Colin F, Gieselmann V, et al. (1999) Neuromotor alterations and cerebellar deficits in aged arylsulfatase A-deficient transgenic mice. Neurosci Lett 273: 93-96.
29. Cook MN, Williams RW, Flaherty L, (2001) Anxiety-related behaviors in the elevated zero-maze are affected by genetic factors and retinal degeneration. Behav Neurosci 115: 468-476.
30. Bannon AW, Seda J, Carmouche M, Francis JM, Norman MH, et al. (2000) Behavioral characterization of neuropeptide Y knockout mice. Brain Res 868: 79-87.
31. Baarendse PJ, van Grootheest G, Jansen RF, Pieneman AW, Ogren SO, et al. (2008) Differential involvement of the dorsal hippocampus in passive avoidance in C57bl/6J and DBA/2J mice. Hippocampus 18: 11-19.
32. Etkin A, Alarcon JM, Weisberg SP, Touzani K, Huang YY, et al. (2006) A role in learning for SRF: Deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron 50: 127-143.
33. Wysocki CJ, Nyby J, Whitney G, Beauchamp GK, Katz Y, (1982) The vomeronasal organ: Primary role in mouse chemosensory gender recognition. Physiol Behav 29: 315-327.
34. Panksepp JB, Jochman KA, Kim JU, Koy JJ, Wilson ED, et al. (2007) Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS One 2: e351.
35. Scattoni ML, Crawley J, Ricceri L, (2009) Ultrasonic vocalizations: A tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 33: 508-515.
36. Liu P, Jenkins NA, Copeland NG, (2003) A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13: 476-484.
37. 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.
38. Gould TD, O'Donnell KC, Picchini AM, Dow ER, Chen G, et al. (2008) Generation and behavioral characterization of beta-catenin forebrain-specific conditional knock-out mice. Behav Brain Res 189: 117-125.
39. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
40. Yao Y, Kelly MT, Sajikumar S, Serrano P, Tian D, et al. (2008) PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28: 7820-7827.
41. Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK, (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76: 4A-5A.
42. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T, (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44: 759-767.
43. Riekkinen P Jr, Riekkinen M, Sirvio J, (1993) Cholinergic drugs regulate passive avoidance performance via the amygdala. J Pharmacol Exp Ther 267: 1484-1492.
44. Bainbridge NK, Koselke LR, Jeon J, Bailey KR, Wess J, et al. (2008) Learning and memory impairments in a congenic C57BL/6 strain of mice that lacks the M2 muscarinic acetylcholine receptor subtype. Behav Brain Res 190: 50-58.
45. Brenes JC, Padilla M, Fornaguera J, (2009) A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behav Brain Res 197: 125-137.
46. Deshmukh SS, Bhalla US, (2003) Representation of odor habituation and timing in the hippocampus. J Neurosci 23: 1903-1915.
47. Jiang YH, Pan Y, Zhu L, Landa L, Yoo J, et al. (2010) Altered ultrasonic vocalization and impaired learning and memory in angelman syndrome mouse model with a large maternal deletion from Ube3a to Gabrb3. PLoS One 5: e12278.
48. Young DM, Schenk AK, Yang SB, Jan YN, Jan LY, (2010) Altered ultrasonic vocalizations in a tuberous sclerosis mouse model of autism. Proc Natl Acad Sci U S A 107: 11074-11079.
49. Higashida H, Yokoyama S, Munesue T, Kikuchi M, Minabe Y, et al. (2011) CD38 gene knockout juvenile mice: A model of oxytocin signal defects in autism. Biol Pharm Bull 34: 1369-1372.
50. Han SP, Friend LR, Carson JH, Korza G, Barbarese E, et al. (2010) Differential subcellular distributions and trafficking functions of hnRNP A2/B1 spliceoforms. Traffic 11: 886-898.
51. Han T, Smith R, (2010) Functional diversity of the hnRNPs: past, present and perspectives. Biochem J 430: 379-92.
52. Zhang G, Neubert TA, Jordan BA, (2012) RNA binding proteins accumulate at the postsynaptic density with synaptic activity. J Neurosci 32: 599-609.
53. Barbarese E, Koppel DE, Deutscher MP, Smith CL, Ainger K, et al. (1995) Protein translation components are colocalized in granules in oligodendrocytes. J Cell Sci 108 (Pt 8): 2781-2790.
54. Khan MA, Goss DJ, (2005) Translation initiation factor (eIF) 4B affects the rates of binding of the mRNA m7G cap analogue to wheat germ eIFiso4F and eIFiso4F.PABP. Biochemistry 44: 4510-4516.
55. Fluitt A, Pienaar E, Viljoen H, (2007) Ribosome kinetics and aa-tRNA competition determine rate and fidelity of peptide synthesis. Comput Biol Chem 31: 335-346.
56. Chou T, (2003) Ribosome recycling, diffusion, and mRNA loop formation in translational regulation. Biophys J 85: 755-773.
57. Klann E, Dever TE, (2004) Biochemical mechanisms for translational regulation in synaptic plasticity. Nat Rev Neurosci 5: 931-942.
58. Messaoudi E, Kanhema T, Soule J, Tiron A, Dagyte G, et al. (2007) Sustained arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27: 10445-10455.
59. Miyakawa T, Yared E, Pak JH, Huang FL, Huang KP, et al. (2001) Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus 11: 763-775.
60. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, et al. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
61. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT, (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52: 461-474.
62. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, et al. (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
63. Sanderson DJ, McHugh SB, Good MA, Sprengel R, Seeburg PH, et al. (2010) Spatial working memory deficits in GluA1 AMPA receptor subunit knockout mice reflect impaired short-term habituation: Evidence for wagner's dual-process memory model. Neuropsychologia 48: 2303-2315.
64. Gu J, Firestein BL, Zheng JQ, (2008) Microtubules in dendritic spine development. J Neurosci 28: 12120-12124.
65. Hu X, Ballo L, Pietila L, Viesselmann C, Ballweg J, et al. (2011) BDNF-induced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J Neurosci 31: 15597-15603.