Threonine 149 phosphorylation enhances ΔFosB transcriptional activity to control psychomotor responses to cocaine

Journal of Neuroscience

Volumn 34, Issue 34, 2014, Pages 11461-11469

  Cates, Hannah M ^a   Thibault, Mackenzie ^b   Pfau, Madeline ^a   Heller, Elizabeth ^a   Eagle, Andrew ^b   Gajewski, Paula ^b   Bagot, Rosemary ^a   Colangelo, Christopher ^d   Abbott, Thomas ^d   Rudenko, Gabby ^c   Neve, Rachael ^e   Nestler, Eric J ^a   Robison, Alfred J ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d Keck Biotechnology Services   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Accumbens; CaMKII; Cocaine; Phosphorylation; Transcription; FosB

Indexed keywords

ALANINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; COCAINE; THREONINE; TRANSCRIPTION FACTOR FOSB; ADENOSINE TRIPHOSPHATE; DOPAMINE UPTAKE INHIBITOR; GREEN FLUORESCENT PROTEIN; PROTEIN C FOS; TRANSCRIPTION FACTOR AP 1;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PSYCHOMOTOR PERFORMANCE; SENSITIZATION; TRANSCRIPTION INITIATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENE TRANSFER; GENETICS; METABOLISM; NEUROBLASTOMA; NUCLEUS ACCUMBENS; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE, TUMOR; COCAINE; DOPAMINE UPTAKE INHIBITORS; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; MALE; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; NEUROBLASTOMA; NUCLEUS ACCUMBENS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FOS; PSYCHOMOTOR PERFORMANCE; THREONINE; TRANSCRIPTION FACTOR AP-1;

EID: 84906215189     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1611-14.2014     Document Type: Article

References (37)

1. Anderson S. M, Famous KR, Sadri-Vakili G, Kumaresan V, Schmidt HD, Bass CE, Terwilliger EF, Cha JH, Pierce RC (2008) CaMKII: a biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking. Nat Neurosci 11:344-353. CrossRef Medline
2. Been L. E, Hedges VL, Vialou V, Nestler EJ, Meisel RL (2013) DeltaJunD overexpression in the nucleus accumbens prevents sexual reward in female Syrian hamsters. Genes Brain Behav 12:666-672. CrossRef Medline
3. Boudreau A. C, Wolf ME (2005) Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25:9144-9151. CrossRef Medline
4. Carle T. L, Ohnishi YN, Ohnishi YH, Alibhai IN, Wilkinson MB, Kumar A, Nestler E. J (2007) Proteasome-dependent and-independent mechanisms for FosB destabilization: identification of FosB degron domains and implications for DeltaFosB stability. Eur J Neurosci 25:3009-3019. CrossRef Medline
5. Colby C. R, Whisler K, Steffen C, Nestler EJ, Self DW (2003) Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J Neurosci 23:2488-2493. Medline
6. Glover J. N, Harrison SC (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373:257-261. CrossRef Medline
7. Grueter B. A, Robison AJ, Neve RL, Nestler EJ, Malenka RC (2013) FosB differentially modulates nucleus accumbens direct and indirect pathway function. Proc Natl Acad Sci U S A 110:1923-1928. CrossRef Medline
8. Hayashi Y., Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267. CrossRef Medline
9. Hell J. W (2014) CaMKII: claiming center stage in postsynaptic function and organization. Neuron 81:249-265. CrossRef Medline
10. Jorissen H. J, Ulery PG, Henry L, Gourneni S, Nestler EJ, Rudenko G (2007) Dimerization and DNA-binding properties of the transcription factor DeltaFosB. Biochemistry 46:8360-8372. CrossRef Medline
11. Kelz M. B, Chen J, Carlezon WA Jr, Whisler K, Gilden L, Beckmann AM, Steffen C., Zhang YJ, Marotti L, Self DW, Tkatch T, Baranauskas G, Surmeier DJ, Neve RL, Duman RS, Picciotto MR, Nestler EJ (1999) Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401:272-276. CrossRef Medline
12. Lobo M. K, Covington HE, Chaudhury D, Friedman AK, Sun H, Damez-Werno D., Dietz DM, Zaman S, Koo JW, Kennedy PJ, Mouzon E, Mogri M, Neve RL, Deisseroth K, Han MH, Nestler EJ (2010) Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330:385-390. CrossRef Medline
13. Loweth J. A, Baker LK, Guptaa T, Guillory AM, Vezina P (2008) Inhibition of CaMKII in the nucleus accumbens shell decreases enhanced amphetamine intake in sensitized rats. Neurosci Lett 444:157-160. CrossRef Medline
14. Loweth J. A, Singer BF, Baker LK, Wilke G, Inamine H, Bubula N, Alexander JK, CarlezonWAJr, Neve RL, Vezina P (2010) Transient overexpression of alpha-Ca2+/calmodulin-dependent protein kinase II in the nucleus accumbens shell enhances behavioral responding to amphetamine. J Neurosci 30:939-949. CrossRef Medline
15. Loweth J. A, Li D, Cortright JJ, Wilke G, Jeyifous O, Neve RL, Bayer KU, Vezina P (2013) Persistent reversal of enhanced amphetamine intake by transient CaMKII inhibition. J Neurosci 33:1411-1416. CrossRef Medline
16. Maze I., Schaefer A, Dietz D, Covington HE 3rd, Sampath SC, Tarakhovsky A, Greengard P., Nestler EJ (2010) G9a regulates cocaine-induced behavioral and transcriptional plasticity in a cell-type specific manner. Soc Neurosci Abstr 36:574.7.
17. McClung C. A, Nestler EJ (2003) Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6:1208-1215. CrossRef Medline
18. Morgan J. I, Curran T (1995) Immediate-early genes: ten years on. Trends Neurosci 18:66-67. CrossRef Medline
19. Nestler E. J (2008) Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos Trans R Soc Lond B Biol Sci 363:3245-3255. CrossRef Medline
20. Peakman M. C, Colby C, Perrotti LI, Tekumalla P, Carle T, Ulery P, Chao J, Duman C., Steffen C, Monteggia L, Allen MR, Stock JL, Duman RS, Mc-Neish J. D, Barrot M, Self DW, Nestler EJ, Schaeffer E (2003) Inducible, brain region-specific expression of a dominant negative mutant of c-Jun in transgenic mice decreases sensitivity to cocaine. Brain Res 970:73-86. CrossRef Medline
21. Perrotti L. I, Weaver RR, Robison B, Renthal W, Maze I, Yazdani S, Elmore RG, Knapp D. J, Selley DE, Martin BR, Sim-Selley L, Bachtell RK, Self DW, Nestler E. J (2008) Distinct patterns of DeltaFosB induction in brain by drugs of abuse. Synapse 62:358-369. CrossRef Medline
22. Pierce R. C, Wolf ME (2013) Psychostimulant-induced neuroadaptations in nucleus accumbens AMPA receptor transmission. Cold Spring Harb Perspect Med 3:a012021. CrossRef Medline
23. Pierce R. C, Bell K, Duffy P, Kalivas PW (1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16:1550-1560. Medline
24. Pierce R. C, Quick EA, Reeder DC, Morgan ZR, Kalivas PW (1998) Calcium-mediated second messengers modulate the expression of behavioral sensitization to cocaine. J Pharmacol Exp Ther 286:1171-1176. Medline
25. Pitchers K. K, Frohmader KS, Vialou V, Mouzon E, Nestler EJ, Lehman MN, Coolen L. M (2010) DeltaFosB in the nucleus accumbens is critical for reinforcing effects of sexual reward. Genes Brain Behav 9:831-840. CrossRef Medline
26. Pitchers K. K, Vialou V, Nestler EJ, Laviolette SR, Lehman MN, Coolen LM (2013) Natural and drug rewards act on common neural plasticity mechanisms with DeltaFosB as a key mediator. J Neurosci 33:3434-3442. CrossRef Medline
27. Robison A. J, Nestler EJ (2011) Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12:623-637. CrossRef Medline
28. Robison A. J, Vialou V, Sun HS, Labonte B, Golden S, Dias C, Turecki G, Tamminga C., Russo S, Mazei-Robison M, Nestler EJ (2014) Fluoxetine epigenetically alters the CaMKIIalpha promoter in nucleus accumbens to regulate DeltaFosB binding and antidepressant effects. Neuropsychopharmacology 39:1178-1186. Medline
29. Robison A. J, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M, Wee S, Koob G, Turecki G, Neve R, Thomas M, Nestler EJ (2013) Behavioral and structural responses to chronic cocaine require a feedforward loop involving DeltaFosB and calcium/calmodulin-dependent protein kinase ii in the nucleus accumbens shell. J Neurosci 33:4295-4307. CrossRef Medline
30. Singer B. F, Loweth JA, Neve RL, Vezina P (2010) Transient viral-mediated overexpression of alpha-calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell leads to long-lasting functional upregulation of alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate receptors: dopamine type-1 receptor and protein kinase A dependence. Eur J Neurosci 31:1243-1251. CrossRef Medline
31. Ulery P. G, Nestler EJ (2007) Regulation of DeltaFosB transcriptional activity by Ser27 phosphorylation. Eur J Neurosci 25:224-230. CrossRef Medline
32. Ulery P. G, Rudenko G, Nestler EJ (2006) Regulation of DeltaFosB stability by phosphorylation. J Neurosci 26:5131-5142. CrossRef Medline
33. Ulery-Reynolds P. G, Castillo MA, Vialou V, Russo SJ, Nestler EJ (2009) Phosphorylation of DeltaFosB mediates its stability in vivo. Neuroscience 158:369-372. CrossRef
34. Medline Vialou V Robison AJ, Laplant QC, Covington HE 3rd, Dietz DM, Ohnishi YN, Mouzon E, Rush AJ 3rd, Watts EL, Wallace DL, Iñiguez SD, Ohnishi YH, Steiner MA, Warren BL, Krishnan V, Bolaños CA, Neve RL, Ghose S, Berton O., Tamminga CA, et al. (2010) DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 13:745-752. CrossRef Medline
35. Wang L., Lv Z, Hu Z, Sheng J, Hui B, Sun J, Ma L (2010) Chronic cocaineinduced H3 acetylation and transcriptional activation of CaMKIIalpha in the nucleus accumbens is critical for motivation for drug reinforcement. Neuropsychopharmacology 35:913-928. CrossRef Medline
36. Wolf M. E, Ferrario CR (2010) AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci Biobehav Rev 35: 185-211. CrossRef Medline
37. Zachariou V., Bolanos CA, Selley DE, Theobald D, Cassidy MP, Kelz MB, Shaw-Lutchman T., Berton O, Sim-Selley LJ, Dileone RJ, Kumar A, Nestler EJ (2006) An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nat Neurosci 9:205-211. CrossRef Medline