Differential phosphoproteome regulation of nucleus accumbens in environmentally enriched and isolated rats in response to acute stress

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Fan, Xiuzhen ^a   Li, Dingge ^a   Zhang, Yafang ^a   Green, Thomas A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; COLORIMETRY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; NUCLEUS ACCUMBENS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOME; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PHYSIOLOGICAL;

EID: 84894238097     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079893     Document Type: Article

References (54)

1. Martins-de-Souza D, Guest PC, Vanattou-Saifoudine N, Rahmoune H, Bahn S (2012) Phosphoproteomic differences in major depressive disorder postmortem brains indicate effects on synaptic function. Eur Arch Psychiatry Clin Neurosci 262: 657-666.
2. Hammen C (2005) Stress and depression. Annu Rev Clin Psychol 1: 293-319.
3. Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298: 1685-1687. (Pubitemid 47606658)
4. Shirayama Y, Chaki S (2006) Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr Neuropharmacol 4: 277-291. (Pubitemid 44524464)
5. Chauvet C, Lardeux V, Goldberg SR, Jaber M, Solinas M (2009) Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacology. 34: 2767-2778.
6. Zhu J, Bardo MT, Green TA, Wedlund P, Dwoskin LP (2007) Nicotine increases dopamine clearance in medial prefrontal cortex in rats raised in an enriched environment. J Neurochem 103: 2575-2588.
7. Green TA, Gehrke BJ, Bardo MT (2002) Environmental enrichment decreases intravenous amphetamine self-administration in rats: dose-response functions for fixed- and progressive-ratio schedules. Psychopharmacology (Berl) 162: 373-378. (Pubitemid 35001899)
8. Green TA, Cain ME, Thompson M, Bardo MT (2003) Environmental enrichment decreases nicotine-induced hyperactivity in rats. Psychopharmacology (Berl) 170: 235-241. (Pubitemid 37491602)
9. Green TA, Alibhai IN, Roybal CN, Winstanley CA, Theobald DE, et al. (2010) Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry 67: 28-35.
10. Green TA, Alibhai IN, Unterberg S, Neve RL, Ghose S, et al. (2008) Induction of activating ranscription factors (ATFs) ATF2, ATF3, and ATF4 in the nucleus accumbens and their regulation of emotional behavior. J Neurosci, 28: 2025-2032. (Pubitemid 351317626)
11. Pavlovsky AA, Boehning D, Li D, Zhang Y, Fan X, et al. (2013) Psychological stress, cocaine and natural reward each induce endoplasmic reticulum stress genes in rat brain. Neuroscience 246: 160-169.
12. Jha S, Dong B, Sakata K (2011) Enriched environment treatment reverses depression-like behavior and restores reduced hippocampal neurogenesis and protein levels of brain-derived neurotrophic factor in mice lacking its expression through promoter IV. Transl Psychiatry 13: 1: e40.
13. Bevins RA, Besheer J, Palmatier M I, Jensen HC, Pickett KS, et al. (2002) Novel-object place conditioning: behavioral and dopaminergic processes in expression of novelty reward. Behav Brain Res 129: 41-50. (Pubitemid 34059224)
14. Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51: 667-672.
15. Crowder WF, Hutto CW Jr (1992) Operant place conditioning measures examined using two nondrug reinforcers. Pharmacol Biochem Behav 41: 817-824.
16. Louilot A, Le Moal M, Simon H (1986) Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations. An in vivo voltammetric study in free moving rats. Brain Res 397: 395-400.
17. Rebec G V, Christensen JR, Guerra C, Bardo MT (1997) Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty. Brain Res 776: 61-67. (Pubitemid 28018458)
18. Badrinarayan A, Wescott SA, Vander Weele CM, Saunders BT, Couturier BE, et al. (2012) Aversive Stimuli Differentially Modulate Real-Time Dopamine Transmission Dynamics within the Nucleus Accumbens Core and Shell. J Neurosci 32: 15779-15790.
19. Hikida T, Yawata S, Yamaguchi T, Danjo T, Sasaoka T, et al. (2013) Pathway-specific modulation of nucleus accumbens in reward and aversive behavior via selective transmitter receptors. Proc Natl Acad Sci U S A 110: 342-7.
20. Roitman MF, Wheeler RA, Carelli RM (2005) Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output. Neuron 45: 587-597. (Pubitemid 40249870)
21. Salamone JD (1994) The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav Brain Res 61: 117-133.
22. Bewernick BH, Hurlemann R, Matusch A, Kayser S, Grubert C, et al. (2010) Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry 67: 110-116.
23. Lin J, Xie Z, Zhu H, Qian J (2010) Understanding protein phosphorylation on a systems level. Brief Funct Genomics. 9: 32-42.
24. Qi X, Lin W, Li J, Pan Y, Wang W (2006) The depressive-like behaviors are correlated with decreased phosphorylation of mitogen-activated protein kinases in rat brain following chronic forced swim stress. Behav Brain Res 175: 233-240. (Pubitemid 44750226)
25. Green TA, Theobald DE, Bardo M, Nester EJ (2006) Effect of environmental enrichment on transcription factors in the nucleus accumbens under basal conditions and after acute or repeated cocaine administration. CPDD meeting 72.p285. Availible: http://www.cpdd.vcu.edu/Pages/Meetings/MeetProgAbSearchAll. html. Accessed 2013 Oct 12.
26. Blackburn AC, Doe WF, Buffinton GD (1999) Protein carbonyl formation on mucosal proteins in vitro and in dextran sulfate-induced colitis. Free Radic. Biol. Med. 27: 262-270. (Pubitemid 29395417)
27. Schuberth C, Buchberger A (2005) Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation, Nature Cell Biology 7: 999-1006. (Pubitemid 41486274)
28. Forsberg L, Larsson C, Sofiadis A, Lewensohn R, Hoog A, et al. (2006) Prefractionation of archival frozen tumours for proteomics applications. J Biotechnol 126: 582-586. (Pubitemid 44634824)
29. Fic E, Kedracka-Krok S, Jankowska U, Pirog A, Dziedzicka-Wasylewska M (2010) Comparison of protein precipitation methods for various rat brain structures prior to proteomic analysis. Electrophoresis 3: 3573-3579.
30. Silva E, O'Gorman M, Becker S, Auer G, Eklund A, et al. (2010) In the eye of the beholder: does the master see the SameSpots as the novice? J Proteome Res 9: 1522-1532.
31. Zheng J, Ramirez VD (2000) Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. Br J Pharmacol 130: 1115-1123. (Pubitemid 30453547)
32. Blom N, Gammeltoft S, Brunak S (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology: 294: 1351-1362. (Pubitemid 30008805)
33. Cohen P (2001) The role of protein phosphorylation in human health and disease. Eur. J. Biochem 268: 5001-5010.
34. Morrison RS, Kinoshita Y, Johnson MD, Uo T, Ho JT, et al. (2002) Proteomic analysis in the neurosciences. Mol Cell Proteomics 1: 553-560.
35. Martins-de-Souza D, Harris LW, Guest PC, Turck CW, Bahn S (2010) The role of proteomics in depression research. Eur Arch Psychiatry Clin Neurosci 260: 499-506.
36. X, Li D, Lichti CF, Green TA (2013) Dynamic Proteomics of Nucleus Accumbens in Response to Acute Psychological Stress in Environmentally Enriched and Isolated Rats. PLoS ONE 8(9): e73689.
37. Chen Z, Hagler J, Palombella VJ, Melandri F, Scherer D, et al. (1995) Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9: 1586-1597.
38. Orford K, Crockett C, Jensen JP, Weissman AM, Byers SW (1997) Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J Biol Chem. 272: 24735-24738. (Pubitemid 27415637)
39. Bech-Otschir D, Kraft R, Huang X, Henklein P, Kapelari B, et al. (2001) COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J 20: 1630-1639. (Pubitemid 32299400)
40. Palmer AK, Fraga D, Paul L Edmiston PL (2008) Regulation of Creatine Kinase Activity by Phosphorylation of Serine-199 by AMP-Activated Kinase The FASEB Journal. 22: 1012.10.
41. Quest AF, Soldati T, Hemmer W, Perriard JC, Eppenberger HM, et al. (1990) Phosphorylation of chicken brain-type creatine kinase affects a physiologically important kinetic parameter and gives rise to protein microheterogeneity in vivo. FEBS Lett 269: 457-64. (Pubitemid 20273847)
42. Lin YS, Cheng TH, Chang CP, Chen HM, Chern Y (2013) Enhancement of brain-type creatine kinase activity ameliorates neuronal deficits in Huntington's disease. Biochim Biophys Acta. 1832: 742-753.
43. Duric V, Banasr M, Licznerski P, Schmidt HD, Stockmeier CA, et al. (2010) A negative regulator of MAP kinase causes depressive behavior. Nat Med 16: 1328-1332.
44. Einat H, Yuan P, Gould TD, Li J, Du J, et al. (2003) The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J Neurosci 23: 7311-7316. (Pubitemid 36999520)
45. Meller E, Shen C, Nikolao TA, Jensen C, Tsimberg Y, et al. (2003). Region-specific effects of acute and repeated restraint stress on the phosphorylation of mitogen-activated protein kinases. Brain Res 979: 57-64. (Pubitemid 36792156)
46. Iio W, Matsukawac N, Tsukaharac T, Koharia D, Toyoda A (2011) Effects of chronic social defeat stress on MAP kinase cascade. Neurosci Lett 504: 281-284.
47. Bruchas MR, Xu M, Chavkin C (2008) Repeated swim stress induces kappa opioid-mediated activation of extracellular signal-regulated kinase 1/2. Neuroreport 19: 1417-22.
48. Hutchinson EK, Avery AC, Vandewoude S (2012) Environmental enrichment during rearing alters corticosterone levels, thymocyte numbers, and aggression in female BALB/c mice. J Am Assoc Lab Anim Sci 51: 18-24.
49. Stairs DJ, Prendergast MA, Bardo MT (2011) Environmental-induced differences in corticosterone and glucocorticoid receptor blockade of amphetamine self-administration in rats. Psychopharmacology (Berl). 218: 293-301.
50. Hutchinson KM, McLaughlin KJ, Wright RL, Bryce Ortiz J, Anouti DP, et al. (2012) Environmental enrichment protects against the effects of chronic stress on cognitive and morphological measures of hippocampal integrity. Neurobiol Learn Mem. 97: 250-260.
51. Kearns RR, Spencer RL (2013) An unexpected increase in restraint duration alters the expression of stress response habituation. Physiol Behav (in press).
52. Naujokat C, Saric T (2007) Concise review: role and function of the Ubiquitin-proteasome system inmammalian stem and progenitor cells. Stem Cells 25: 2408-2418. (Pubitemid 47582733)
53. Schwarz DC, Hochstrasser M (2003) A superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem. Sci. 28: 321-328.
54. Johnson ES (2004) Protein modification by SUMO. Annu. Rev.Biochem. 73: 355-382.