Dynamic Proteomics of Nucleus Accumbens in Response to Acute Psychological Stress in Environmentally Enriched and Isolated Rats

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Fan, Xiuzhen ^a   Li, Dingge ^a   Lichti, Cheryl F ^a   Green, Thomas A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HEAT SHOCK PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN 14 3 3; PROTEIN KINASE B; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UBIQUITIN;

ACUTE STRESS; ANIMAL EXPERIMENT; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENERGY METABOLISM; ENVIRONMENTAL ENRICHMENT; ENZYME ACTIVITY; GENE TARGETING; IMMOBILIZATION STRESS; MALE; MENTAL STRESS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEUS ACCUMBENS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEOMICS; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; KINETICS; MALE; MODELS, BIOLOGICAL; NUCLEUS ACCUMBENS; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; SIGNAL TRANSDUCTION; SOCIAL ENVIRONMENT; SOCIAL ISOLATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRESS, PSYCHOLOGICAL;

EID: 84883612911     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073689     Document Type: Article

References (61)

1. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, et al. (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62: 593-602.
2. Little A, (2009) Treatment-resistant depression. Am Fam Physician 80: 167-172.
3. Nestler EJ, Hyman SE, (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13: 1161-1169.
4. 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.
5. Calcagnetti DJ, Schechter MD, (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51: 667-672.
6. Rebec GV, 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.
7. Crowder WF, Hutto CW Jr, (1992) Operant place conditioning measures examined using two nondrug reinforcers. Pharmacol Biochem Behav 41: 817-824.
8. Bevins RA, Besheer J, Palmatier MI, 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.
9. Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, et al. (2010) The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33: 267-276.
10. Nestler EJ, Carlezon WA Jr, (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
11. 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.
12. Green TA, Theobald DE, Bardo MT, Nester EJ (2006) Effect of environmental enrichment on transcription factors in the nucleus accumbens under basal conditions and after acute or repeated cocaine administration. College on the Problems of Drug Dependence. Scottsdale, AZ.
13. Green TA, Alibhai IN, Hommel JD, DiLeone RJ, Kumar A, et al. (2006) Induction of inducible cAMP early repressor expression in nucleus accumbens by stress or amphetamine increases behavioral responses to emotional stimuli. J Neurosci 26: 8235-8242.
14. Green TA, Alibhai IN, Unterberg S, Neve RL, Ghose S, et al. (2008) Induction of activating transcription factors (ATFs) ATF2, ATF3, and ATF4 in the nucleus accumbens and their regulation of emotional behavior. J Neurosci 28: 2025-2032.
15. 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.
16. Larson EB, Graham DL, Arzaga RR, Buzin N, Webb J, et al. (2011) Overexpression of CREB in the nucleus accumbens shell increases cocaine reinforcement in self-administering rats. J Neurosci 31: 16447-16457.
17. Zhu J, Green T, Bardo MT, Dwoskin LP, (2004) Environmental enrichment enhances sensitization to GBR 12935-induced activity and decreases dopamine transporter function in the medial prefrontal cortex. Behav Brain Res 148: 107-117.
18. Carlezon WA, Jr. Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, et al. (1998) Regulation of cocaine reward by CREB. Science 282: 2272-2275.
19. 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.
20. Chen X, Herbert J, (1995) Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64: 675-685.
21. Green TA, Crooks PA, Bardo MT, Dwoskin LP, (2001) Contributory role for nornicotine in nicotine neuropharmacology: nornicotine-evoked [3H]dopamine overflow from rat nucleus accumbens slices. Biochem Pharmacol 62: 1597-1603.
22. 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.
23. Schuberth C, Buchberger A, (2005) Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 7: 999-1006.
24. Forsberg L, Larsson C, Sofiadis A, Lewensohn R, Hoog A, et al. (2006) Pre-fractionation of archival frozen tumours for proteomics applications. J Biotechnol 126: 582-586.
25. 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 31: 3573-3579.
26. Fan X, Wang J, Soman KV, Ansari GA, Khan MF, (2011) Aniline-induced nitrosative stress in rat spleen: proteomic identification of nitrated proteins. Toxicol Appl Pharmacol 255: 103-112.
27. 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.
28. Zheng J, Ramirez VD, (2000) Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. Br J Pharmacol 130: 1115-1123.
29. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, et al. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102: 4459-4464.
30. Lee SA, Tsao TT, Yang KC, Lin H, Kuo YL, et al. (2012) Construction and analysis of the protein-protein interaction networks for schizophrenia, bipolar disorder, and major depression. BMC Bioinformatics 12Suppl 13: S20.
31. Beasley CL, Pennington K, Behan A, Wait R, Dunn MJ, et al. (2006) Proteomic analysis of the anterior cingulate cortex in the major psychiatric disorders: Evidence for disease-associated changes. Proteomics 6: 3414-3425.
32. Liu Y, Yang N, Hao W, Zhao Q, Ying T, et al. (2011) Dynamic proteomic analysis of protein expression profiles in whole brain of Balb/C mice subjected to unpredictable chronic mild stress: implications for depressive disorders and future therapies. Neurochem Int 58: 904-913.
33. Carboni L, Piubelli C, Pozzato C, Astner H, Arban R, et al. (2006) Proteomic analysis of rat hippocampus after repeated psychosocial stress. Neuroscience 137: 1237-1246.
34. Mallei A, Giambelli R, Gass P, Racagni G, Mathe AA, et al. (2011) Synaptoproteomics of learned helpless rats involve energy metabolism and cellular remodeling pathways in depressive-like behavior and antidepressant response. Neuropharmacology 60: 1243-1253.
35. Khawaja X, Xu J, Liang JJ, Barrett JE, (2004) Proteomic analysis of protein changes developing in rat hippocampus after chronic antidepressant treatment: Implications for depressive disorders and future therapies. J Neurosci Res 75: 451-460.
36. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM, (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J 281 (Pt 1): 21-40.
37. Gardner A, Boles RG, (2011) Beyond the serotonin hypothesis: mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 35: 730-743.
38. Gardner A, Johansson A, Wibom R, Nennesmo I, von Dobeln U, et al. (2003) Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 76: 55-68.
39. Fattal O, Link J, Quinn K, Cohen BH, Franco K, (2007) Psychiatric comorbidity in 36 adults with mitochondrial cytopathies. CNS Spectr 12: 429-438.
40. Calamia V, de Andres MC, Oreiro N, Ruiz-Romero C, Blanco FJ, (2011) Hsp90beta inhibition modulates nitric oxide production and nitric oxide-induced apoptosis in human chondrocytes. BMC Musculoskelet Disord 12: 237.
41. Cooper LC, Prinsloo E, Edkins AL, Blatch GL, (2011) Hsp90alpha/beta associates with the GSK3beta/axin1/phospho-beta-catenin complex in the human MCF-7 epithelial breast cancer model. Biochem Biophys Res Commun 413: 550-554.
42. Gancedo C, Flores CL (2008) Moonlighting proteins in yeasts. Microbiol Mol Biol Rev 72: 197-210, table of contents.
43. Steinacker P, Aitken A, Otto M, (2011) 14-3-3 proteins in neurodegeneration. Semin Cell Dev Biol 22: 696-704.
44. Muslin AJ, Tanner JW, Allen PM, Shaw AS, (1996) Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84: 889-897.
45. Darling DL, Yingling J, Wynshaw-Boris A, (2005) Role of 14-3-3 proteins in eukaryotic signaling and development. Curr Top Dev Biol 68: 281-315.
46. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.
47. Cole AR, Noble W, van Aalten L, Plattner F, Meimaridou R, et al. (2007) Collapsin response mediator protein-2 hyperphosphorylation is an early event in Alzheimer's disease progression. J Neurochem 103: 1132-1144.
48. Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, et al. (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10: 165-179.
49. Rogemond V, Auger C, Giraudon P, Becchi M, Auvergnon N, et al. (2008) Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J Biol Chem 283: 14751-14761.
50. Wilson SM, Brittain JM, Piekarz AD, Ballard CJ, Ripsch MS, et al. (2011) Further insights into the antinociceptive potential of a peptide disrupting the N-type calcium channel-CRMP-2 signaling complex. Channels (Austin) 5: 449-456.
51. Brittain JM, Piekarz AD, Wang Y, Kondo T, Cummins TR, et al. (2009) An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J Biol Chem 284: 31375-31390.
52. Brittain JM, Chen L, Wilson SM, Brustovetsky T, Gao X, et al. (2011) Neuroprotection against traumatic brain injury by a peptide derived from the collapsin response mediator protein 2 (CRMP2). J Biol Chem 286: 37778-37792.
53. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, et al. (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10: M111 013284.
54. 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.
55. Dwivedi Y, Rizavi HS, Roberts RC, Conley RC, Tamminga CA, et al. (2001) Reduced activation and expression of ERK1/2 MAP kinase in the post-mortem brain of depressed suicide subjects. J Neurochem 77: 916-928.
56. You Z, Luo C, Zhang W, Chen Y, He J, et al. (2011) Pro- and anti-inflammatory cytokines expression in rat's brain and spleen exposed to chronic mild stress: involvement in depression. Behav Brain Res 225: 135-141.
57. Bruchas MR, Schindler AG, Shankar H, Messinger DI, Miyatake M, et al. (2011) Selective p38alpha MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71: 498-511.
58. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, et al. (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12: 200-209.
59. Bowling SL, Bardo MT, (1994) Locomotor and rewarding effects of amphetamine in enriched, social, and isolate reared rats. Pharmacol Biochem Behav 48: 459-464.
60. Bowling SL, Rowlett JK, Bardo MT, (1993) The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32: 885-893.
61. Gomez AM, Midde NM, Mactutus CF, Booze RM, Zhu J, (2012) Environmental enrichment alters nicotine-mediated locomotor sensitization and phosphorylation of DARPP-32 and CREB in rat prefrontal cortex. PLoS One 7: e44149.