Activity-dependent expression of miR-132 regulates immediate-early gene induction during olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx

Neurobiology of Learning and Memory

Volumn 120, Issue , 2015, Pages 41-51

  Mukilan, Murugan ^a   Ragu Varman, Durairaj ^a   Sudhakar, Sivasubramaniam ^b   Rajan, Koilmani Emmanuvel ^a  

^a BHARATHIDASAN UNIVERSITY   (India)

^b MANONMANIAM SUNDARANAR UNIVERSITY   (India)

Author keywords

CREB; Cynopterus sphinx; Immediate early genes; MiR 132; Olfactory memory

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; MICRORNA; MICRORNA 132; MICRORNA 148A; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG; NERVE PROTEIN; POSTSYNAPTIC DENSITY PROTEINS;

ACTIVITY DEPENDENT GENE EXPRESSION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BAT; BRAIN LEVEL; CONTROLLED STUDY; CYNOPTERUS SPHINX; EGR 1 GENE; ENZYME ACTIVATION; EXPERIMENTAL BEHAVIORAL TEST; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; IMMEDIATE EARLY GENE; LEARNING; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY MEMORY; ONCOGENE C FOS; ONCOGENE C JUN; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; LONG TERM MEMORY; MEMORY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CHIROPTERA; GENE EXPRESSION; GENES, IMMEDIATE-EARLY; LEARNING; MEMORY; MICRORNAS; NERVE TISSUE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RETENTION (PSYCHOLOGY); SMELL;

EID: 84924366602     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.02.010     Document Type: Article

References (68)

1. Abel T., Nguyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 1997, 88:615-626.
2. Adams J.P., Sweatt J.D. Molecular psychology roles for the ERK MAP kinase cascade in memory. Annual Review of Pharmacology and Toxicology 2002, 42:135-163.
3. Balasingh J., Koilraj J., Kunz T.H. Tent construction by the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodiae) in southern India. Ethology 1995, 3:210-229.
4. Balschun D., Wolfer D.P., Gass P., Mantamadiotis T., Welzl H., Schutz G., et al. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory?. The Journal of Neuroscience 2003, 23:6304-6314.
5. Benito E., Valor L.M., Jimenez-Minchan M., Huber W., Barco A. CAMP response element-binding protein is a primary hub of activity-driven neuronal gene expression. The Journal of Neuroscience 2011, 31:18237-18250.
6. Besnard A., Laroche S., Caboche J. Comparative dynamics of MAPK/ERK signaling components and immediate early genes in the hippocampus and amygdala following contextual fear conditioning and retrieval. Brain Structure and Function 2014, 219:415-430.
7. Bhat H.R. Observations on the food and feeding behavior of Cynopterus sphinx Vahl (Chiroptera, Pteropodidae) at pune, India. Mammalia 1994, 58:363-370.
8. Bredy T.W., Lin Q., Wei W., Baker-Andresen D., Mattick J.S. MicroRNA regulation of neural plasticity and memory. Neurobiology of Learning and Memory 2011, 96:89-94.
9. Brennan P.A., Hancock D., Keverne E.B. The expression of immediate early genes c-fos, egr-1 and c-jun in the accessory olfactory bulb during the formation of an olfactory memory in mice. Neuroscience 1992, 49:277-284.
10. Charra R., Datiche F., Gigot V., Schaal B., Coureaud G. Pheromone-induced odor learning modifies Fos expression in the newborn rabbit brain. Behavioural Brain Research 2013, 237:129-140.
11. Chawla M.K., Penner M.R., Olson K.M., Sutherland V.L., Mittelman-Smith M.A., Barnes C.A. Spatial behavior and seizure-induced changes in c-fos mRNA expression in young and old rats. Neurobiology of Aging 2013, 34:1184-1198.
12. Cheval H., Chagneau C., Levasseur G., Veyrac A., Faucon-Biguet N., Laroche S., et al. Distinctive features of Egr transcription factor regulation and DNA binding activity in CA1 of the hippocampus in synaptic plasticity and consolidation and reconsolidation of fear memory. Hippocampus 2012, 22:631-642.
13. Duvarci S., Nader K., Le Doux J.E. Activation of extracellular signal-regulated kinase-mitogen activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. European Journal of Neuroscience 2005, 21:283-289.
14. Ehrlich I., Klein M., Rumpel S., Malinow R. PSD-95 required for activity-driven synapse stabilization. Proceedings of National Academy of Sciences of the United States of America 2007, 104:4176-4181.
15. English J.D., Sweatt J.D. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. The Journal of Biological Chemistry 1997, 272:19103-19106.
16. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 1993, 260:1661-1664.
17. Ganesh A., Bogdanowicz W., Balamurugan K., Ragu Varman D., Rajan K.E. Egr-1 antisense oligodeoxynucleotide administration into the olfactory bulb impairs olfactory learning in the greater short-nosed fruit bat Cynopterus sphinx. Brain Research 2012, 1471:33-45.
18. Ganesh A., Bogdanowicz W., Haupt M., Marimuthu G., Rajan K.E. Role of olfactory bulb serotonin in olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae). Brain Research 2010, 17:108-117.
19. Guthrie K.M., Anderson A.J., Leon M., Gall C. Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb. Proceedings of National Academy of Sciences of the United States of America 1993, 90:3329-3333.
20. Guzowski J.F., Setlow B., Wagner E.K., McGaugh J.L. Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. The Journal of Neuroscience 2001, 21:5089-5098.
21. Hansen K.F., Karelina K., Sakamota K., Wayman G.A., Impey S., Obrietaan K. MiRNA-132: A dynamic regulator of cognitive capacity. Brain Structure and Function 2013, 218:817-831.
22. Hansen K.F., Sakamoto K., Wayman G.A., Impey S., Obrietan K. Transgenic miR-132 alters neuronal spine density and impairs novel object recognition memory. PLoS ONE 2010, 5:E15497.
23. Hodgkison R., Kalko E.K.V., Ayasse M., Haberlien C., Schulz S., Mustapha W.A., et al. The chemical ecology of fruit bat foraging behaviour in relation to the fruit odors of two species of palaeotrophical bat-dispersed figs. (Ficus hispida and Ficus scortechinii). Journal of Chemical Ecology 2007, 33:2097-2110.
24. Hu Y., Liu M.Y., Liu P., Dong X., Boran A.D. Neuroprotective effects of 3,6'-disinapoyl sucrose through increased BDNF levels and CREB phosphorylation via the CaMKII and ERK1/2 pathway. Journal of Molecular Neuroscience 2014, 53:600-607.
25. Im H.I., Kenny P.J. MicroRNAs in neuronal function and dysfunction. Trends in Neuroscience 2012, 35:325-334.
26. Impey S., Davare M., Lesika A., Fortin D., Ando H., Varlamova O., et al. An activity-induced microRNAs controls dendritic spine formation by regulating Rac-1-PAK signaling. Molecular and Cellular Neuroscience 2010, 43:146-156.
27. Kandel E.R. The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Molecular Brain 2012, 14:5-14.
28. Kunz T.H., Brock C.E. A comparison of mist nets and ultrasonic detectors for monitoring flight activity of bats. Journal of Mammalogy 1972, 56:907-911.
29. Li X., Wu Z., Fu X., Han W. A microRNA component of the neoplastic microenvironment: Microregulators with far-reaching impact. Biomed Research International 2013, 2013:762183.
30. Liu X., Zhan Z., Xu L., Ma F., Li D., Guo Z., et al. MicroRNA-148/152 impairs innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIα. The Journal of Immunology 2010, 185:7244-7251.
31. Luft S., Curio E., Tacud B. The use of olfaction in the foraging behaviour of the golden mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenchaften 2003, 90:84-87.
32. Malenka R.C., Lancaster B., Zucker R.S. Temporal limits on the rise in post synaptic calcium required for the induction of long-term potentiation. Neuron 1992, 9:121-128.
33. Marimuthu G., Rajan K.E., Koilraj A.J., Isaac S., Balasingh J. Observations on the foraging behavior of a tent roosting Megachiropteran bat Cynopterus sphinx. Biotropica 1998, 30:321-324.
34. Meyer D., Bonhoeffer T., Scheuss V. Balance and stability of synaptic structures during synaptic plasticity. Neuron 2014, 82:430-443.
35. Miller B.H., Zeier Z., Xi L., Lanz T.A., Deng S., Strathmann J., et al. MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proceedings of National Academy of Sciences of the United States of America 2012, 109:3125-3130.
36. Miyashita T., Kubik S., Lewandowski G., Guzowski J.F. Networks of neurons, networks of genes: An integrated view of memory consolidation. Neurobiology of Learning and Memory 2008, 89:269-284.
37. Mohamed H.A., Yao W., Fioravante D., Smolen P., Byrne J.H. CAMP response elements in aplysia creb1, creb2, and Ap-uch promoters: Implications for feedback loops modulating long term memory. The Journal of Biological Chemistry 2005, 280:27035-27043.
38. Nathan P.T., Doss D.S., Isaac S.S., Balasingh J., Rajan K.E., Nair N.G., et al. Mist-net capture and field observations on the short-nosed fruit bat (Chiroptera: Pteropodidae) Cynopterus sphinx (Vahl). Journal of the Bombay Natural History Society 2001, 98:373-378.
39. Néant-Fery M., pérés E., Nasrallah C., Kessner M., Gribaudo S., Grrer C., et al. A role for dendritic translation of CaMKIIα mRNA in olfactory plasticity. PLoS One 2012, 7:e40133.
40. Nudelman A.S., DiRocco D.P., Lambert T.J., Garelick M.G., Le J., Nathanson N.M., et al. Neuronal activity rapidly induces transcription of the CREB-regulated micro RNA-132, in vivo. Hippocampus 2010, 20:492-498.
41. Pantazopoulos H., Dolatshad H., Davis F.C. A fear inducing odor alters PER2 and c-Fos expression in brain regions involved in fear memory. PLoS One 2011, 6:e20658.
42. Peng S., Zhang Y., Ren B., Zhang J., Wang H. Effect of ketamine administration on memory consolidation, p-CREB and c-fos expression in the hippocampal slices of minor rats. Molecular Biology Reports 2011, 38:2401-2407.
43. Peng S., Zhang Y., Zhang J., Wang H., Ren B. ERK in learning and memory: A review of recent research. International Journal of Molecular Sciences 2010, 11:222-232.
44. Pollak D.D., Herkner K., Hoeger H., Lubec G. Behavioral testing upregulates pCaMKII, BDNF, PSD-95 and egr-1 in hippocampus of FVB/N mice. Behavioural Brain Research 2005, 163:128-135.
45. Rajan K.E., Marimuthu G. Localization of prey by the Indian false vampire bat Megaderma lyra. Mammalia 1999, 63:149-158.
46. Ratcliffe J.M., Ter Hofstede H.M. Roosts as information centres: Social learning and food preferences of bats. Biology Letters 2005, 1:72-74.
47. Redmond L., Kashani A.H., Ghosh A. Calcium regulation of dendritic growth via CaM kinase IV and CREB mediated transcription. Neuron 2002, 34:999-1010.
48. Reinecke K., Herdegen T., Eminel S., Aldenhoff J.B., Schiffelholz T. Knockout of c-Jun N-terminal kinases 1, 2 or 3 isoforms induces behavioural changes. Behavioural Brain Research 2013, 245:88-95.
49. Sánchez F., Korine C., Steeghs M., Laarhoven L.J., Cristescu S.M., Harren F.J.M., et al. Ethanol and methanol as possible odor cues for Egyptian fruit bats (Rousettus aegyptiacus). Journal of Chemical Ecology 2006, 32:1289-1300.
50. Scott H.L., Tamagnini F., Narduzzo K.E., Howarth J.L., Lee Y.B., Wong L.F., et al. Micro RNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. European Journal of Neuroscience 2012, 36:2941-2948.
51. Selbach M., Schwanhäusser B., Thierfelder T., Fang Z., Khanin R., Rajewsy N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63.
52. Smalheiser N.R., Lugli G. MicroRNAs regulation of synaptic plasticity. NeuroMolecular Medicine 2009, 11:133-140.
53. Smalheiser N.R., Lugli G., Lenon A.L., Davis J.M., Torvik V.I., Larson J. Olfactory discrimination training up-regulates and reorganizes expression of microRNAs in adult mouse hippocampus. ASN Neuro 2010, 2:e00028.
54. Soule J., Penke Z., Kanhema T., Alme M.N., Laroche S., Bramham C.R. Object-place recognition learning triggers rapid induction of plasticity-related immediate early genes and synaptic proteins in the rat dendate gyrus. Neural Plasticity 2008, 2008:269097.
55. Thiels E., Klann E. Extracellular signal-regulated kinase, synaptic plasticity and memory. Reviews in the Neurosciences 2001, 12:327-345.
56. Thomas G.M., Huganir R.L. MAPK cascade signaling and synaptic plasticity. Nature Reviews Neuroscience 2004, 5:173-183.
57. Tognini P., Pizzorusso T. MicroRNA 212/132 family: Molecular transducer of neuronal function and plasticity. The International Journal of Biochemistry & Cell Biology 2012, 44:6-10.
58. Tognini P., Putignano E., Coatti A., Pizzorusso T. Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nature Neuroscience 2011, 14:1237-1239.
59. Veyrac A., Besnard A., Caboche J., Davis S., Laroche S. The transcription factor Zif268/Egr1, brain plasticity, and memory. Progress in Molecular Biology and Translational Science 2014, 122:89-129.
60. Veyrac A., Wang G., Baum M.J., Bakker J. The main and accessory olfactory systems of female mice are activated differentially by dominant versus subordinate male urinary odors. Brain Research 2011, 1402:20-29.
61. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proceedings of National Academy of Sciences of the United States of America 2005, 102:16426-16431.
62. 2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. The Journal of Neuroscience 2001, 21:5484-5493.
63. Wanet A., Tacheny A., Arnould T., Renard P. MiR-212/132 expression and functions: Within and beyond the neuronal compartment. Nucleic Acids Research 2012, 40:4742-4753.
64. Wang Z., Yan P., Hui T., Zhang J. Epigenetic upregulation of PSD-95 contributes to the rewarding behavior by morphine conditioning. European Journal of Pharmacology 2014, 732:123-129.
65. Wayman G.A., Davare M., Ando H., Fortin D., Varlamova O., Cheng H.Y., et al. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proceedings of National Academy of Sciences of the United States of America 2008, 105:9093-9098.
66. Yuan Q., Harley C.W., Darby-king A., Neve R.L., McLean J.H. Early odor preference learning in the rat: Bidirectional effects of camp response element-binding protein (CREB) and mutant CREB support a causal role for phosphorylated CREB. The Journal of Neuroscience 2003, 23:4760-4765.
67. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annual Review of Neuroscience 2001, 24:1071-1089.
68. Zhang J.J., Okutani F., Inoue S., Kaba H. Activation of the cyclic AMP response element binding protein signaling pathway in the olfactory bulb is required for the acquisition of olfactory aversive learning in young rats. Neuroscience 2003, 117:707-713.