Nuclear factor kB signaling regulates neuronal morphology and cocaine reward

Journal of Neuroscience

Volumn 29, Issue 11, 2009, Pages 3529-3537

  Russo, Scott J ^a   Wilkinson, Matthew B ^a   Mazei Robison, Michelle S ^a   Dietz, David M ^a   Maze, Ian ^a   Krishnan, Vaishnav ^b   Renthal, William ^b   Graham, Ami ^b   Birnbaum, Shari G ^b   Green, Thomas A ^b   Robison, Bruce ^b   Lesselyong, Alan ^b   Perrotti, Linda I ^b   Bolaños, Carlos A ^b   Kumar, Arvind ^b   Clark, Michael S ^c   Neumaier, John F ^c   Neve, Rachael L ^d   Bhakar, Asha L ^e   Barker, Philip A ^e   Nestler, Eric J ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COCAINE; GENE PRODUCT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GREEN FLUORESCENT PROTEIN; I KAPPA B ALPHA; I KAPPA B BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF KAPPA B KINASE CA; INHIBITOR OF KAPPA B KINASE DN; PROTEIN P105; PROTEIN P50; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DENDRITIC SPINE; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; MALE; MORPHOLOGY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REWARD; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL STRAIN; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; NERVE CELL; PHYSIOLOGY; RAT; ULTRASTRUCTURE;

ANIMALS; CELLS, CULTURED; COCAINE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; NF-KAPPA B; NUCLEUS ACCUMBENS; PC12 CELLS; RATS; REWARD; SIGNAL TRANSDUCTION;

EID: 63849227432     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6173-08.2009     Document Type: Article

References (55)

1. Ahmed SH, Koob GF (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282:298-300.
2. Ahmed SH, Lin D, Koob GF, Parsons LH (2003) Escalation of cocaine self-administration does not depend on altered cocaine-induced nucleus accumbens dopamine levels. J Neurochem 86:102-113.
3. Ang E, Chen J, Zagouras P, Magna H, Holland J, Schaeffer E, Nestler EJ (2001) Induction of nuclear factor- kB in nucleus accumbens by chronic cocaine administration. J Neurochem 79:221-224.
4. Asanuma M, Cadet JL (1998) Methamphetamine-induced increase in striatal NF-kB DNA-binding activity is attenuated in superoxide dismutase transgenic mice. Brain Res Mol Brain Res 60:305-309.
5. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 99:11435-11440.
6. Bhakar AL, Tannis LL, Zeindler C, Russo MP, Jobin C, Park DS, MacPherson S, Barker PA (2002) Constitutive nuclear factor-kB activity is required for central neuron survival. J Neurosci 22:8466-8475.
7. Bibb JA, Chen J, Taylor JR, Svenningsson P, Nishi A, Snyder GL, Yan Z, Sagawa ZK, Ouimet CC, Nairn AC, Nestler EJ, Greengard P (2001) Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410:376-380.
8. Bolaños CA, Nestler EJ (2004) Neurotrophic mechanisms in drug addiction. Neuromolecular Med 5:69-83.
9. Boudreau AC, Wolf ME (2005) Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25:9144-9151.
10. Chen LF, Greene WC (2004) Shaping the nuclear action of NF- kB. Nat Rev Mol Cell Biol 5:392-401.
11. Clark MS, Sexton TJ, McClain M, Root D, Kohen R, Neumaier JF (2002) Overexpression of 5-HT1B receptor in dorsal raphe nucleus using Herpes Simplex Virus gene transfer increases anxiety behavior after inescapable stress. J Neurosci 22:4550-4562.
12. Dietrich JB, Mangeol A, Revel MO, Burgun C, Aunis D, Zwiller J (2005) Acute or repeated cocaine administration generates reactive oxygen species and induces antioxidant enzyme activity in dopaminergic rat brain structures. Neuropharmacology 48:965-974.
13. Dietz DM, Dietz KC, Nestler EJ, Russo SJ (2009) Molecular mechanisms of psychostimulant-induced structural plasticity. Pharmacopsychiatry 42:S1-S10.
14. Ferrario CR, Gorny G, Crombag HS, Li Y, Kolb B, Robinson TE (2005) Neural and behavioral plasticity associated with the transition from controlled to escalated cocaine use. Biol Psychiatry 58:751-759.
15. Foehr ED, Lin X, O'Mahony A, Geleziunas R, Bradshaw RA, Greene WC (2000) NF- kB signaling promotes both cell survival and neurite process formation in nerve growth factor-stimulated PC12 cells. J Neurosci 20:7556-7563.
16. Freeman AY, Pierce RC (2002) Neutralization of neutrophin-3 in the ventral tegmental area or nucleus accumbens differentially modulates cocaine-induced behavioral plasticity in rats. Synapse 46:57-65.
17. Graham DL, Edwards S, Bachtell RK, DiLeone 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.
18. 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.
19. Gutierrez H, Hale VA, Dolcet X, Davies A (2005) NF-kB signalling regulates the growth of neural processes in the developing PNS and CNS. Development 132:1713-1726.
20. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565-598.
21. Jedynak JP, Uslaner JM, Esteban JA, Robinson TE (2007) Methamphetamine-induced structural plasticity in the dorsal striatum. Eur J Neurosci 25:847-853.
22. Kassed CA, Willing AE, Garbuzova-Davis S, Sanberg PR, Pennypacker KR (2002) Lack of NF-kB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning. Exp Neurol 176:277-288.
23. 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, et al. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131:391-404.
24. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, Neve RL, SelfDW, Nestler EJ (2005) Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48:303-314.
25. Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117:721-733.
26. Lee KW, Kim Y, Kim AM, Helmin K, Nairn AC, Greengard P (2006) Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc Natl Acad Sci U S A 103:3399-3404.
27. Li Y, Acerbo MJ, Robinson TE (2004) The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20:1647-1654.
28. Lin WW, Karin M (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 117:1175-1183.
29. -ΔΔC(T) method. Methods 25:402-408.
30. Mattson MP (2005) NF-kB in the survival and plasticity of neurons. Neurochem Res 30:883-893.
31. Mattson MP, Meffert MK (2006) Roles for NF-kB in nerve cell survival, plasticity, and disease. Cell Death Differ 13:852-860.
32. Meffert MK, Baltimore D (2005) Physiological functions for brain NF-kappaB. Trends Neurosci 28:37-43.
33. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D (2003) NF-kB functions in synaptic signaling and behavior. Nat Neurosci 6:1072-1078.
34. Mercurio F, Manning AM (1999) NF-kB as a primary regulator of the stress response. Oncogene 18:6163-6171.
35. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young DB, Barbosa M, Mann M, Manning A, Rao A (1997) IKK-1 and IKK-2: cytokine-activated IkB kinases essential for NF-kB activation. Science 278:860-866.
36. Messer CJ, Eisch AJ, Carlezon WA Jr, Whisler K, Shen L, Wolf DH, Westphal H, Collins F, Russell DS, Nestler EJ (2000) Role for GDNF in biochemical and behavioral adaptations to drugs of abuse. Neuron 26:247-257.
37. Nestler EJ (2008) Review. Transcriptional mechanisms of addiction: role of ΔFosB. Philos Trans R Soc Lond B Biol Sci 363:3245-3255.
38. Norrholm SD, Bibb JA, Nestler EJ, Ouimet CC, Taylor JR, Greengard P (2003) Cocaine-induced proliferation of dendritic spines in nucleus accumbens is dependent on the activity of cyclin-dependent kinase-5. Neuroscience 116:19-22.
39. O'Neill LA, Kaltschmidt C (1997) NF-kB: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20:252-258.
40. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, Greengard P, Nairn AC, Nestler EJ, Cowan CW (2008) Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59:621-633.
41. Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517-529.
42. Rex CS, Lin CY, Kramár EA, Chen LY, Gall CM, Lynch G (2007) Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27:3017-3029.
43. Robinson TE, Kolb B (1997) Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491-8497.
44. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47 [Suppl 1]:33-46.
45. 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 (2007) IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat Neurosci 10:93-99.
46. Russo SJ, Mazei-Robison MS, Ables JL, Nestler EJ (2009) Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56:73-82.
47. Shippenberg TS, Heidbreder C (1995) Sensitization to the conditioned rewarding effects of cocaine: pharmacological and temporal characteristics. J Pharmacol Exp Ther 273:808-815.
48. Taylor JR, Lynch WJ, Sanchez H, Olausson P, Nestler EJ, Bibb JA (2007) Inhibition of Cdk5 in the nucleus accumbens enhances the locomotor-activating and incentive-motivational effects of cocaine. Proc Natl Acad Sci U S A 104:4147-4152.
49. Thomas MJ, Malenka RC (2003) Synaptic plasticity in the mesolimbic dopamine system. Philos Trans R Soc Lond B Biol Sci 358:815-819.
50. Toda S, Shen HW, Peters J, Cagle S, Kalivas PW (2006) Cocaine increases actin cycling: effects in the reinstatement model of drug seeking. J Neurosci 26:1579-1587.
51. Ungless MA, Whistler JL, Malenka RC, Bonci A (2001 ) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583-587.
52. von Bohlen und Halbach O, Minichiello L, Unsicker K (2008) TrkB but not trkC receptors are necessary for postnatal maintenance of hippocampal spines. Neurobiol Aging 29:1247-1255.
53. Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, Milner TA, Hempstead BL, Lu B (2005) Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8:1069-1077.
54. Yao WD, Gainetdinov RR, Arbuckle MI, Sotnikova TD, Cyr M, Beaulieu JM, Torres GE, Grant SG, Caron MG (2004) Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41:625-638.
55. Yu Z, Zhou D, Bruce-Keller AJ, Kindy MS, Mattson MP (1999) Lack of the p50 subunit of nuclear factor-kB increases the vulnerability of hippocampal neurons to excitotoxic injury. J Neurosci 19:8856-8865.