MicroRNA-206 in rat medial prefrontal cortex regulates BDNF expression and alcohol drinking

Journal of Neuroscience

Volumn 34, Issue 13, 2014, Pages 4581-4588

  Tapocik, Jenica D ^a   Barbier, Estelle ^a   Flanigan, Meghan ^a   Solomon, Matthew ^a   Pincus, Alexandra ^a   Pilling, Andrew ^a   Sun, Hui ^a   Schank, Jesse R ^a   King, Courtney ^a   Heilig, Markus ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Addiction; Alcohol dependence; BDNF; Medial prefrontal cortex; microRNA; Self administration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MICRORNA; MICRORNA 206; UNCLASSIFIED DRUG;

ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DRINKING BEHAVIOR; DRUG SELF ADMINISTRATION; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MICROARRAY ANALYSIS; NERVE CELL CULTURE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UPREGULATION;

ADDICTION; ALCOHOL DEPENDENCE; BDNF; MEDIAL PREFRONTAL CORTEX; MICRORNA; SELF-ADMINISTRATION;

ALCOHOL DRINKING; ALCOHOLS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MALE; MICRORNAS; MUTATION; NEURONS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SELF ADMINISTRATION; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 84897911224     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0445-14.2014     Document Type: Article

References (45)

1. Aoki C, Wu K, Elste A, Len GW, Lin SY, McAuliffe G, Black IB (2000) Localization of brain-derived neurotrophic factor and Trk B receptors to postsynaptic densities of adult rat cerebral cortex. J Neurosci Res 59:454-463. CrossRef Medline
2. Beck A, Wüstenberg T, Genauck A, Wrase J, Schlagenhauf F, Smolka MN, Mann K, Heinz A (2012) Effect of brain structure, brain function, and brain connectivity on relapse in alcohol-dependent patients. Arch Gen Psychiatry 69:842-852. CrossRef Medline
3. Berglind WJ, See RE, Fuchs RA, Ghee SM, Whitfield TW Jr, Miller SW, McGinty JF (2007) A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur J Neurosci 26:757-766. CrossRef Medline
4. Berglind WJ, Whitfield TW Jr, La Lumiere RT, Kalivas PW, McGinty JF (2009) A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J Neurosci 29:3715-3719. CrossRef Medline
5. Bramham CR (2008) Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18:524-531. CrossRef Medline
6. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200:125-140. CrossRef Medline
7. Crews FT, Zou J, Qin L (2011) Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25 [Suppl 1]: S4-S12.
8. Fanous S, Guez-Barber DH, Goldart EM, Schrama R, Theberge FR, Shaham Y, Hope BT (2013) Unique gene alterations are induced in FACSpurified Fos-positive neurons activated during cue-induced relapse to heroin seeking. J Neurochem 124:100-108. CrossRef Medline
9. Fumagalli F, Franchi C, Caffino L, Racagni G, Riva MA, Cervo L (2009) Single session of cocaine intravenous self-administration shapes goal-oriented behaviours and upregulates Arc m RNA levels in rat medial prefrontal cortex. Int J Neuropsychopharmacol 12:423-429. CrossRef Medline
10. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, James JJ, Maysuria M, Mitton JD, Oliveri P, Osborn JL, Peng T, Ratcliffe AL, Webster PJ, Davidson EH, Hood L, Dimitrov K (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26:317-325. CrossRef Medline
11. George O, Sanders C, Freiling J, Grigoryan E, Vu S, Allen CD, Crawford E, Mandyam CD, Koob GF (2012) Recruitment of medial prefrontal cortex neurons during alcohol withdrawal predicts cognitive impairment and excessive alcohol drinking. Proc Natl Acad Sci U S A 109:18156-18161. CrossRef Medline
12. Graham DL, Edwards S, Bachtell RK, Di Leone RJ, Rios M, Self DW (2007) Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat Neurosci 10:1029-1037. CrossRef Medline
13. Greco SJ, Rameshwar P (2007) Micro RNAs regulate synthesis of the neurotransmitter substance P in human mesenchymal stem cellderived neuronal cells. Proc Natl Acad Sci U S A 104:15484-15489. CrossRef Medline
14. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23: 742-747. Medline
15. Haas JD, Nistala K, Petermann F, Saran N, Chennupati V, Schmitz S, Korn T, Wedderburn LR, Förster R, Krueger A, Prinz I (2011) Expression of mi RNAs mi R-133b and mi R-206 in the Il17a/f locus is co-regulated with IL-17 production in alphabeta and gammadelta T cells. Plo S One 6:e20171. CrossRef Medline
16. Hensler JG, Ladenheim EE, Lyons WE (2003) Ethanol consumption and serotonin-1A (5-HT1A) receptor function in heterozygous BDNF (+/-) mice. J Neurochem 85:1139-1147. CrossRef Medline
17. Horch HW, Krüttgen A, Portbury SD, Katz LC (1999) Destabilization of cortical dendrites and spines by BDNF. Neuron 23:353-364. CrossRef Medline
18. Im HI, Hollander JA, Bali P, Kenny PJ (2010) Me CP2 controls BDNF expression and cocaine intake through homeostatic interactions with micro RNA-212. Nat Neurosci 13:1120-1127. CrossRef Medline
19. Jeanblanc J, He DY, Carnicella S, Kharazia V, Janak PH, Ron D (2009) Endogenous BDNF in the dorsolateral striatum gates alcohol drinking. J Neurosci 29:13494-13502. CrossRef Medline
20. Kang HJ, Schuman EM (1995) Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus. J Physiol Paris 89:11-22. CrossRef Medline
21. Lee ST, Chu K, Jung KH, Kim JH, Huh JY, Yoon H, Park DK, Lim JY, Kim JM, Jeon D, Ryu H, Lee SK, Kim M, Roh JK (2012) mi R-206 regulates brainderived neurotrophic factor in Alzheimer disease model. Ann Neurol 72:269-277. CrossRef Medline
22. Lewohl JM, Nunez YO, Dodd PR, Tiwari GR, Harris RA, Mayfield RD (2011) Up-regulation of micro RNAs in brain of human alcoholics. Alcohol Clin Exp Res 35:1928-1937. CrossRef Medline
23. Lu L, Dempsey J, Liu SY, Bossert JM, Shaham Y (2004) A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J Neurosci 24:1604-1611. CrossRef Medline
24. Mayfield RD, Harris RA, Schuckit MA (2008) Genetic factors influencing alcohol dependence. Br J Pharmacol 154:275-287. Medline
25. McGough NN, He DY, Logrip ML, Jeanblanc J, Phamluong K, Luong K, Kharazia V, Janak PH, Ron D (2004) RACK1 and brain-derived neurotrophic factor: a homeostatic pathway that regulates alcohol addiction. J Neurosci 24:10542-10552. CrossRef Medline
26. Meinhardt MW, Hansson AC, Perreau-Lenz S, Bauder-Wenz C, Stählin O, Heilig M, Harper C, Drescher KU, Spanagel R, Sommer WH (2013) Rescue of infralimbic m Glu R2 deficit restores control over drug-seeking behavior in alcohol dependence. J Neurosci 33:2794-2806. CrossRef Medline
27. Melendez RI, McGinty JF, Kalivas PW, Becker HC (2012) Brain regionspecific gene expression changes after chronic intermittent ethanol exposure and early withdrawal in C57BL/6J mice. Addict Biol 17:351-364. CrossRef Medline
28. Messaoudi E, Ying SW, Kanhema T, Croll SD, Bramham CR (2002) Brainderived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22:7453-7461. Medline
29. Messaoudi E, Kanhema T, Soulé J, Tiron A, Dagyte G, da Silva B, Bramham CR (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. CrossRef Medline
30. Miura P, Amirouche A, Clow C, Bélanger G, Jasmin BJ (2012) Brainderived neurotrophic factor expression is repressed during myogenic differentiation by mi R-206. J Neurochem 120:230-238. CrossRef Medline
31. Nagappan G, Lu B (2005) Activity-dependent modulation of the BDNF receptor Trk B: mechanisms and implications. Trends Neurosci 28:464-471. CrossRef Medline
32. Pandey SC, Zhang H, Ugale R, Prakash A, Xu T, Misra K (2008) Effector immediate-early gene arc in the amygdala plays a critical role in alcoholism. J Neurosci 28:2589-2600. CrossRef Medline
33. Poo MM (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32. CrossRef Medline
34. Rimondini R, Arlinde C, Sommer W, Heilig M (2002) Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J 16:27-35. CrossRef Medline
35. Rodríguez JJ, Davies HA, Silva AT, De Souza IE, Peddie CJ, Colyer FM, Lancashire CL, Fine A, Errington ML, Bliss TV, Stewart MG (2005) Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arg3.1 protein expression in spines, dendrites and glia. Eur J Neurosci 21:2384-2396. CrossRef Medline
36. Sadri-Vakili G, Kumaresan V, Schmidt HD, Famous KR, Chawla P, Vassoler FM, Overland RP, Xia E, Bass CE, Terwilliger EF, Pierce RC, Cha JH (2010) Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine. J Neurosci 30:11735-11744. CrossRef Medline
37. Schank JR, Tapocik JD, Barbier E, Damadzic R, Eskay RL, Sun H, Rowe KE, King CE, Yao M, Flanigan ME, Solomon MG, Karlsson C, Cheng K, Rice KC, Heilig M (2013) Tacr1 gene variation and neurokinin 1 receptor expression is associated with antagonist efficacy in genetically selected alcohol-preferring rats. Biol Psychiatry 73:774-781. CrossRef Medline
38. Silahtaroglu AN, Nolting D, Dyrskjøt L, Berezikov E, Møller M, Tommerup N, Kauppinen S (2007) Detection of micro RNAs in frozen tissue sections by fluorescence in situ hybridization using locked nucleic acid probes and tyramide signal amplification. Nat Protoc 2:2520-2528. CrossRef Medline
39. Sommer WH, Rimondini R, Hansson AC, Hipskind PA, Gehlert DR, Barr CS, Heilig MA (2008) Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol Psychiatry 63:139-145. CrossRef Medline
40. Soulé J, Messaoudi E, Bramham CR (2006) Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem Soc Trans 34:600-604. CrossRef Medline
41. Tapocik JD, Solomon M, Flanigan M, Meinhardt M, Barbier E, Schank JR, Schwandt M, Sommer WH, Heilig M (2013) Coordinated dysregulation of m RNAs and micro RNAs in the rat medial prefrontal cortex following a history of alcohol dependence. Pharmacogenomics J 13:286-296. CrossRef Medline
42. Tu Y, Kroener S, Abernathy K, Lapish C, Seamans J, Chandler LJ, Woodward JJ (2007) Ethanol inhibits persistent activity in prefrontal cortical neurons. J Neurosci 27:4765-4775. CrossRef Medline
43. Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW Jr, Logrip ML, Rivier C, Repunte-Canonigo V, Zorrilla EP, Sanna PP, Heilig M, Koob GF (2012) Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci 32:7563-7571. CrossRef Medline
44. Williams AH, Valdez G, Moresi V, Qi X, McAnally J, Elliott JL, Bassel-Duby R, Sanes JR, Olson EN (2009) Micro RNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326: 1549-1554. CrossRef Medline
45. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR (2002) Brain-derived neurotrophic factor induces longterm potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532-1540. Medline