Altered gene expression and spine density in nucleus accumbens of adolescent and adult male mice exposed to emotional and physical stress

Developmental Neuroscience

Volumn 36, Issue 3-4, 2014, Pages 250-260

  Warren, Brandon L ^a   Sial, Omar K ^a   Alcantara, Lyonna F ^a   Greenwood, Maria A ^a   Brewer, Jacob S ^a   Rozofsky, John P ^a   Parise, Eric M ^a   Bolaños Guzmán, Carlos A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Adolescence; Dendritic spines; Depression; Extracellular signal related kinase 2; Nucleus accumbens; Social defeat; FosB

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR FOSB;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; EARLY LIFE STRESS; EMOTIONAL STRESS; ENZYME PHOSPHORYLATION; EXPOSURE; GENE EXPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PERINATAL PERIOD; PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOCIAL INTERACTION; WESTERN BLOTTING; AGING; ANIMAL; C57BL MOUSE; GROWTH, DEVELOPMENT AND AGING; HUMAN RELATION; MENTAL STRESS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PSYCHOLOGY; DENSITY; GENETIC TRANSCRIPTION; RNA TRANSLATION; SOCIAL ASPECT; SPINE;

AGING; ANIMALS; DENDRITIC SPINES; GENE EXPRESSION; INTERPERSONAL RELATIONS; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NUCLEUS ACCUMBENS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84906940066     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000362875     Document Type: Article

References (83)

1. McEwen BS: Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 2003; 9: 149-154.
2. Roberts JE, Gotlib IH: Lifetime episodes of dysphoria: Gender, early childhood loss and personality. Br J Clin Psychol 1997; 36(pt 2): 195-208.
3. Gilmer WS, McKinney WT: Early experience and depressive disorders: Human and nonhuman primate studies. J Affect Disord 2003; 75: 97-113.
4. Anda RF, Brown DW, Felitti VJ, Dube SR, Giles WH: Adverse childhood experiences and prescription drug use in a cohort study of adult HMO patients. BMC Public Health 2008; 8: 198.
5. Teicher MH, Samson JA, Polcari A, Mc- Greenery CE: Sticks, stones, and hurtful words: Relative effects of various forms of childhood maltreatment. Am J Psychiatry 2006; 163: 993-1000.
6. Dube SR, Anda RF, Whitfield CL, Brown DW, Felitti VJ, Dong M, Giles WH: Longterm consequences of childhood sexual abuse by gender of victim. Am J Prev Med 2005; 28: 430-438.
7. Edwards VJ, Holden GW, Felitti VJ, Anda RF: Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: Results from the Adverse Childhood Experiences Study. Am J Psychiatry 2003; 160: 1453-1460.
8. Rees CA: Understanding emotional abuse. Arch Dis Child 2010; 95: 59-67.
9. Dubowitz H, Newton RR, Litrownik AJ, Lewis T, Briggs EC, Thompson R, English D, Lee LC, Feerick MM: Examination of a conceptual model of child neglect. Child Maltreat 2005; 10: 173-189.
10. Hornor G: Emotional maltreatment. J Pediatr Health Care 2012; 26: 436-442.
11. Spertus IL, Yehuda R, Wong CM, Halligan S, Seremetis SV: Childhood emotional abuse and neglect as predictors of psychological and physical symptoms in women presenting to a primary care practice. Child Abuse Negl 2003; 27: 1247-1258.
12. Wright MO, Crawford E, Del Castillo D: Childhood emotional maltreatment and later psychological distress among college students: The mediating role of maladaptive schemas. Child Abuse Negl 2009; 33: 59-68.
13. Warren BL, Vialou VF, Iniguez SD, Alcantara LF, Wright KN, Feng J, Kennedy PJ, Laplant Q, Shen L, Nestler EJ, Bolanos-Guzman CA: Neurobiological sequelae of witnessing stressful events in adult mice. Biol Psychiatry 2013; 73: 7-14.
14. Bolanos CA, Nestler EJ: Neurotrophic mechanisms in drug addiction. Neuromolecular Med 2004; 5: 69-83.
15. Koob GF: Negative reinforcement in drug addiction: The darkness within. Curr Opin Neurobiol 2013; 23: 559-563.
16. Russo SJ, Bolanos CA, Theobald DE, DeCarolis NA, Renthal W, Kumar A, Winstanley CA, Renthal NE, Wiley MD, Self DW, Russell DS, Neve RL, Eisch AJ, Nestler EJ: IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 2007; 10: 93-99.
17. Nestler EJ, Carlezon WA Jr: The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 2006; 59: 1151-1159.
18. Russo SJ, Nestler EJ: The brain reward circuitry in mood disorders. Nat Rev Neurosci 2013; 14: 609-625.
19. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM: Neurobiology of depression. Neuron 2002; 34: 13-25.
20. Warren BL, Iniguez SD, Alcantara LF, Wright KN, Parise EM, Weakley SK, Bolanos- Guzman CA: Juvenile administration of concomitant methylphenidate and fluoxetine alters behavioral reactivity to reward- And mood-related stimuli and disrupts ventral tegmental area gene expression in adulthood. J Neurosci 2011; 31: 10347-10358.
21. Iniguez SD, Vialou V, Warren BL, Cao JL, Alcantara LF, Davis LC, Manojlovic Z, Neve RL, Russo SJ, Han MH, Nestler EJ, Bolanos- Guzman CA: Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J Neurosci 2010; 30: 7652-7663.
22. Fumagalli F, Molteni R, Calabrese F, Frasca A, Racagni G, Riva MA: Chronic fluoxetine administration inhibits extracellular signal-regulated kinase 1/2 phosphorylation in rat brain. J Neurochem 2005; 93: 1551-1560.
23. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ: CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 2002; 99: 11435-11440.
24. Carlezon WA Jr, Duman RS, Nestler EJ: The many faces of CREB. Trends Neurosci 2005; 28: 436-445.
25. Berton O, Covington HE 3rd, Ebner K, Tsankova NM, Carle TL, Ulery P, Bhonsle A, Barrot M, Krishnan V, Singewald GM, Singewald N, Birnbaum S, Neve RL, Nestler EJ: Induction of δFosB in the periaqueductal gray by stress promotes active coping responses. Neuron 2007; 55: 289-300.
26. Vialou V, Maze I, Renthal W, LaPlant QC, Watts EL, Mouzon E, Ghose S, Tamminga CA, Nestler EJ: Serum response factor promotes resilience to chronic social stress through the induction of δFosB. J Neurosci 2010; 30: 14585-14592.
27. Vialou V, Robison AJ, Laplant QC, Covington HE 3rd, Dietz DM, Ohnishi YN, Mouzon E, Rush AJ 3rd, Watts EL, Wallace DL, Iniguez SD, Ohnishi YH, Steiner MA, Warren BL, Krishnan V, Bolanos CA, Neve RL, Ghose S, Berton O, Tamminga CA, Nestler EJ: δFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 2010; 13: 745-752.
28. Wallace DL, Vialou V, Rios L, Carle-Florence TL, Chakravarty S, Kumar A, Graham DL, Green TA, Kirk A, Iniguez SD, Perrotti LI, Barrot M, DiLeone RJ, Nestler EJ, Bolanos- Guzman CA: The influence of δFosB in the nucleus accumbens on natural reward-related behavior. J Neurosci 2008; 28: 10272-10277.
29. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon WA Jr: Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 2001; 21: 7397-7403.
30. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, Iniguez SD, Cao JL, Kirk A, Chakravarty S, Kumar A, Krishnan V, Neve RL, Cooper DC, Bolanos CA, Barrot M, Mc- Clung CA, Nestler EJ: CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 2009; 12: 200-209.
31. Poo MM: Neurotrophins as synaptic modulators. Nat Rev Neurosci 2001; 2: 24-32.
32. Russo SJ, Murrough JW, Han MH, Charney DS, Nestler EJ: Neurobiology of resilience. Nat Neurosci 2012; 15: 1475-1484.
33. Spear LP: Heightened stress responsivity and emotional reactivity during pubertal maturation: Implications for psychopathology. Dev Psychopathol 2009; 21: 87-97
34. Andersen SL, Teicher MH: Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 2008; 31: 183-191
35. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM: The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev 2003; 27: 33-44
36. Leussis MP, Andersen SL: Is adolescence a sensitive period for depression?. Behavioral and neuroanatomical findings from a social stress model. Synapse 2008; 62: 22-30
37. Spear LP: The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000; 24: 417-463
38. Paus T, Keshavan M, Giedd JN: Why do many psychiatric disorders emerge during adolescence?. Nat Rev Neurosci 2008; 9: 947-957
39. Council NR: Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research. Washington, National Academy Press, 2003
40. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ: Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006; 311: 864-868
41. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, Graham A, Lutter M, Lagace DC, Ghose S, Reister R, Tannous P, Green TA, Neve RL, Chakravarty S, Kumar A, Eisch AJ, Self DW, Lee FS, Tamminga CA, Cooper DC, Gershenfeld HK, Nestler EJ: Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007; 131: 391-404
42. Krishnan V, Han MH, Mazei-Robison M, Iniguez SD, Ables JL, Vialou V, Berton O, Ghose S, Covington HE 3rd, Wiley MD, Henderson RP, Neve RL, Eisch AJ, Tamminga CA, Russo SJ, Bolanos CA, Nestler EJ: Akt signaling within the ventral tegmental area regulates cellular and behavioral responses to stressful stimuli. Biol Psychiatry 2008; 64: 691-700
43. Golden SA, Covington HE 3rd, Berton O, Russo SJ: A standardized protocol for repeated social defeat stress in mice. Nat Protoc 2011; 6: 1183-1191
44. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ: Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 2006; 9: 519-525
45. Wilkinson MB, Xiao G, Kumar A, LaPlant Q, Renthal W, Sikder D, Kodadek TJ, Nestler EJ: Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J Neurosci 2009; 29: 7820-7832
46. LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iniguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolanos CA, Kabbaj M, Xiao G, Neve RL, Hurd YL, Oosting RS, Fan G, Morrison JH, Nestler EJ: Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010; 13: 1137-1143
47. Iniguez SD, Charntikov S, Baella SA, Herbert MS, Bolanos-Guzman CA, Crawford CA: Post-training cocaine exposure facilitates spatial memory consolidation in C57BL/6 mice. Hippocampus 2012; 22: 802-813
48. Gibb R, Kolb B: A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 1998; 79: 1-4
49. Yadid G, Overstreet DH, Zangen A: Limbic dopaminergic adaptation to a stressful stimulus in a rat model of depression. Brain Res 2001; 896: 43-47
50. Zuo Y, Lin A, Chang P, Gan WB: Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 2005; 46: 181-189
51. Roberts TF, Tschida KA, Klein ME, Mooney R: Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 2010; 463: 948-952
52. Hyman SE, Malenka RC: Addiction and the brain: The neurobiology of compulsion and its persistence. Nat Rev Neurosci 2001; 2: 695-703
53. Nestler EJ, Aghajanian GK: Molecular and cellular basis of addiction. Science 1997; 278: 58-63
54. Faure A, Reynolds SM, Richard JM, Berridge KC: Mesolimbic dopamine in desire and dread: Enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens. J Neurosci 2008; 28: 7184-7192
55. Everitt BJ, Wolf ME: Psychomotor stimulant addiction: A neural systems perspective. J Neurosci 2002; 22: 3312-3320
56. Di Chiara G: Nucleus accumbens shell and core dopamine: Differential role in behavior and addiction. Behav Brain Res 2002; 137: 75-114
57. Mehra A, Lee KH, Hatzimanikatis V: Insights into the relation between mRNA and protein expression patterns. I. Theoretical considerations. Biotechnol Bioeng 2003; 84: 822-833
58. Lee PS, Shaw LB, Choe LH, Mehra A, Hatzimanikatis V, Lee KH: Insights into the relation between mRNA and protein expression patterns. II. Experimental observations in Escherichia coli . Biotechnol Bioeng 2003; 84: 834-841
59. Lu L, Koya E, Zhai H, Hope BT, Shaham Y: Role of ERK in cocaine addiction. Trends Neurosci 2006; 29: 695-703
60. Valjent E, Corbille AG, Bertran-Gonzalez J, Herve D, Girault JA: Inhibition of ERK pathway or protein synthesis during reexposure to drugs of abuse erases previously learned place preference. Proc Natl Acad Sci USA 2006; 103: 2932-2937
61. Iniguez SD, Warren BL, Neve RL, Russo SJ, Nestler EJ, Bolanos-Guzman CA: Viral-mediated expression of extracellular signal-regulated kinase-2 in the ventral tegmental area modulates behavioral responses to cocaine. Behav Brain Res 2010; 214: 460-464
62. Koob GF: A role for brain stress systems in addiction. Neuron 2008; 59: 11-34
63. Miczek KA, Yap JJ, Covington HE 3rd: Social stress, therapeutics and drug abuse: Preclinical models of escalated and depressed intake. Pharmacol Ther 2008; 120: 102-128
64. Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, Levit O, Zangen A: Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem 2008; 107: 522-532
65. Lupien SJ, McEwen BS, Gunnar MR, Heim C: Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009; 10: 434-445
66. Nikulina EM, Lacagnina MJ, Fanous S, Wang J, Hammer RP Jr: Intermittent social defeat stress enhances mesocorticolimbic δFosB/ BDNF co-expression and persistently activates corticotegmental neurons: Implication for vulnerability to psychostimulants. Neuroscience 2012; 212: 38-48
67. Perrotti LI, Hadeishi Y, Ulery PG, Barrot M, Monteggia L, Duman RS, Nestler EJ: Induction of δFosB in reward-related brain structures after chronic stress. J Neurosci 2004; 24: 10594-10602
68. Nikulina EM, Arrillaga-Romany I, Miczek KA, Hammer RP Jr: Long-lasting alteration in mesocorticolimbic structures after repeated social defeat stress in rats: Time course of μ-opioid receptor mRNA and FosB/δFosB immunoreactivity. Eur J Neurosci 2008; 27: 2272-2284
69. Robison AJ, Nestler EJ: Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 2011; 12: 623-637
70. Lobo MK, Zaman S, Damez-Werno DM, Koo JW, Bagot RC, Dinieri JA, Nugent A, Finkel E, Chaudhury D, Chandra R, Riberio E, Rabkin J, Mouzon E, Cachope R, Cheer JF, Han MH, Dietz DM, Self DW, Hurd YL, Vialou V, Nestler EJ: δFosB induction in striatal medium spiny neuron subtypes in response to chronic pharmacological, emotional, and optogenetic stimuli. J Neurosci 2013; 33: 18381-18395
71. Robison AJ, Vialou V, Mazei-Robison M, Feng J, Kourrich S, Collins M, Wee S, Koob G, Turecki G, Neve R, Thomas M, Nestler EJ: Behavioral and structural responses to chronic cocaine require a feedforward loop involving δFosB and calcium/calmodulin-dependent protein kinase ii in the nucleus accumbens shell. J Neurosci 2013; 33: 4295-4307
72. Servillo G, Della Fazia MA, Sassone-Corsi P: Coupling cAMP signaling to transcription in the liver: Pivotal role of CREB and CREM. Exp Cell Res 2002; 275: 143-154
73. Shepard JD, Liu Y, Sassone-Corsi P, Aguilera G: Role of glucocorticoids and cAMP-mediated repression in limiting corticotropin-releasing hormone transcription during stress. J Neurosci 2005; 25: 4073-4081
74. Green TA, Alibhai IN, Hommel JD, DiLeone RJ, Kumar A, Theobald DE, Neve RL, Nestler EJ: Induction of inducible cAMP early repressor expression in nucleus accumbens by stress or amphetamine increases behavioral responses to emotional stimuli. J Neurosci 2006; 26: 8235-8242
75. Barrot M, Wallace DL, Bolanos CA, Graham DL, Perrotti LI, Neve RL, Chambliss H, Yin JC, Nestler EJ: Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci USA 2005; 102: 8357-8362
76. Patterson MA, Szatmari EM, Yasuda R: AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERKdependent manner during long-term potentiation. Proc Natl Acad Sci USA 2010; 107: 15951-15956
77. Grueter BA, Robison AJ, Neve RL, Nestler EJ, Malenka RC: FosB differentially modulates nucleus accumbens direct and indirect pathway function. Proc Natl Acad Sci USA 2013; 110: 1923-1928
78. Pitchers KK, Vialou V, Nestler EJ, Laviolette SR, Lehman MN, Coolen LM: Natural and drug rewards act on common neural plasticity mechanisms with δFosB as a key mediator. J Neurosci 2013; 33: 3434-3442
79. Suzuki S, Zhou H, Neumaier JF, Pham TA: Opposing functions of CREB and MKK1 synergistically regulate the geometry of dendritic spines in visual cortex. J Comp Neurol 2007; 503: 605-617
80. Golden SA, Christoffel DJ, Heshmati M, Hodes GE, Magida J, Davis K, Cahill ME, Dias C, Ribeiro E, Ables JL, Kennedy PJ, Robison AJ, Gonzalez-Maeso J, Neve RL, Turecki G, Ghose S, Tamminga CA, Russo SJ: Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression. Nat Med 2013; 19: 337-344
81. Muhammad A, Carroll C, Kolb B: Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 2012; 216: 103-109
82. Andersen SL: Trajectories of brain development: Point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 2003; 27: 3-18
83. Andersen SL, Navalta CP: Altering the course of neurodevelopment: A framework for understanding the enduring effects of psychotropic drugs. Int J Dev Neurosci 2004; 22: 423-440.