Constitutive knockout of Kalirin-7 leads to increased rates of cocaine self-administration

Molecular Pharmacology

Volumn 84, Issue 4, 2013, Pages 582-590

  Kiraly, Drew D ^a,c   Nemirovsky, Natali E ^b   LaRese, Taylor P ^a   Tomek, Seven E ^b   Yahn, Stephanie L ^b   Olive, M Foster ^b   Eipper, Betty A ^a   Mains, Richard E ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KALIRIN 7; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC SPINE; GENE EXPRESSION; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALS; BEHAVIOR, ADDICTIVE; COCAINE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SELF ADMINISTRATION; UP-REGULATION;

EID: 84884687150     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.087106     Document Type: Article

References (59)

1. Benavides DR, Quinn JJ, Zhong P, Hawasli AH, DiLeone RJ, Kansy JW, Olausson P, Yan Z, Taylor JR, and Bibb JA (2007) Cdk5 modulates cocaine reward, motivation, and striatal neuron excitability. J Neurosci 27:12967-12976. (Pubitemid 350159589)
2. Brown TE, Lee BR, Mu P, Ferguson D, Dietz D, Ohnishi YN, Lin Y, Suska A, Ishikawa M, and Huang YH et al. (2011) A silent synapse-based mechanism for cocaine-induced locomotor sensitization. J Neurosci 31:8163-8174.
3. Deroche-Gamonet V, Belin D, and Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014-1017. (Pubitemid 39071778)
4. Ducci F and Goldman D (2012) The genetic basis of addictive disorders. Psychiatr Clin North Am 35:495-519.
5. Eipper-Mains JE, Kiraly DD, Duff MO, Horowitz MJ, McManus CJ, Eipper BA, Graveley BR, and Mains RE (2013) Effects of cocaine and withdrawal on the mouse nucleus accumbens transcriptome. Genes Brain Behav 12:21-33.
6. Epstein DH, Preston KL, Stewart J, and Shaham Y (2006) Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl) 189:1-16. (Pubitemid 44607255)
7. Fujita Y, Morinobu S, Takei S, Fuchikami M, Matsumoto T, Yamamoto S, and Yamawaki S (2012) Vorinostat, a histone deacetylase inhibitor, facilitates fear extinction and enhances expression of the hippocampal NR2B-containing NMDA receptor gene. J Psychiatr Res 46:635-643.
8. Gangarossa G, Espallergues J, de Kerchove d'Exaerde A, El Mestikawy S, Gerfen CR, Hervé D, Girault JA, and Valjent E (2013) Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens. Front Neural Circuits 7:22 DOI: 10.3389/fncir.2013.00022.
9. Giza JI, Jung Y, Jeffrey RA, Neugebauer NM, Picciotto MR, and Biederer T (2013) The synaptic adhesion molecule SynCAM 1 contributes to cocaine effects on synapse structure and psychostimulant behavior. Neuropsychopharmacology 38:628-638.
10. Guo X, Liu Z, Wang X, and Zhang H (2012) Large scale association analysis for drug addiction: results from SNP to gene. ScientificWorldJournal 2012:939584 DOI: 10.1100/2012/939584.
11. Huang YH, Lin Y, Mu P, Lee BR, Brown TE, Wayman G, Marie H, Liu W, Yan Z, and Sorg BA et al. (2009) In vivo cocaine experience generates silent synapses. Neuron 63:40-47.
12. Hutsler JJ and Zhang H (2010) Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 1309:83-94.
13. Hyman SE, Malenka RC, and Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565-598. (Pubitemid 44476856)
14. Kalivas PW (2009) The glutamate homeostasis hypothesis of addiction. Nat Rev Neurosci 10:561-572.
15. Kauer JA and Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8:844-858. (Pubitemid 350006216)
16. Kelley AE and Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306-3311. (Pubitemid 37465733)
17. Kiraly DD, Eipper-Mains JE, Mains RE, and Eipper BA (2010a) Synaptic plasticity, a symphony in GEF. ACS Chem Neurosci 1:348-365.
18. Kiraly DD, Lemtiri-Chlieh F, Levine ES, Mains RE, and Eipper BA (2011) Kalirin binds the NR2B subunit of the NMDA receptor, altering its synaptic localization and function. J Neurosci 31:12554-12565.
19. Kiraly DD, Ma XM, Mazzone CM, Xin X, Mains RE, and Eipper BA (2010b) Behavioral and morphological responses to cocaine require kalirin7. Biol Psychiatry 68:249-255.
20. Knackstedt LA and Kalivas PW (2009) Glutamate and reinstatement. Curr Opin Pharmacol 9:59-64.
21. Koob GF and Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217-238.
22. LaPlant Q, Vialou V, Covington HE, 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, and Iñiguez SD et al. (2010) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137-1143.
23. Lee BR and Dong Y (2011) Cocaine-induced metaplasticity in the nucleus accumbens: silent synapse and beyond. Neuropharmacology 61:1060-1069.
24. Lee KW, Kim Y, Kim AM, Helmin K, Nairn AC, and 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 USA 103:3399-3404. (Pubitemid 43346480)
25. Lee MC, Yasuda R, and Ehlers MD (2010) Metaplasticity at single glutamatergic synapses. Neuron 66:859-870.
26. Lemtiri-Chlieh F, Zhao L, Kiraly DD, Eipper BA, Mains RE, and Levine ES (2011) Kalirin-7 is necessary for normal NMDA receptor-dependent synaptic plasticity. BMC Neurosci 12:126 DOI: 10.1186/1471-2202-12-126.
27. Lin YC and Koleske AJ (2010) Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 33:349-378.
28. Ma XM, Wang Y, Ferraro F, Mains RE, and Eipper BA (2008a) Kalirin-7 is an essential component of both shaft and spine excitatory synapses in hippocampal interneurons. J Neurosci 28:711-724. (Pubitemid 351159022)
29. Ma XM, Huang JP, Wang Y, Eipper BA, and Mains RE (2003) Kalirin, a multifunctional Rho GEF, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. J Neurosci 23:10593-10603. (Pubitemid 37485273)
30. Ma XM, Huang JP, Xin X, Yan Y, Mains RE, and Eipper BA (2012) A role for kalirin in the response of rat medium spiny neurons to cocaine. Mol Pharmacol 82:738-745.
31. Ma XM, Johnson RC, Mains RE, and Eipper BA (2001) Expression of kalirin, a neuronal GDP/GTP exchange factor of the trio family, in the central nervous system of the adult rat. J Comp Neurol 429:388-402. (Pubitemid 32010046)
32. Ma XM, Kiraly DD, Gaier ED, Wang Y, Kim E-J, Levine ES, Eipper BA, and Mains RE (2008b) Kalirin-7 is required for synaptic structure and function. J Neurosci 28:12368-12382.
33. Ma YY, Guo CY, Yu P, Lee DY, Han JS, and Cui CL (2006) The role of NR2B containing NMDA receptor in place preference conditioned with morphine and natural reinforcers in rats. Exp Neurol 200:343-355. (Pubitemid 44131532)
34. Ma YY, Yu P, Guo CY, and Cui CL (2011) Effects of ifenprodil on morphine-induced conditioned place preference and spatial learning and memory in rats. Neurochem Res 36:383-391.
35. Mains RE, Kiraly DD, Eipper-Mains JE, Ma XM, and Eipper BA (2011) Kalrn promoter usage and isoform expression respond to chronic cocaine exposure. BMC Neurosci 12:20 DOI: 10.1186/1471-2202-12-20
36. Mao LM, Wang W, Chu XP, Zhang GC, Liu XY, Yang YJ, Haines M, Papasian CJ, Fibuch EE, and Buch S et al. (2009) Stability of surface NMDA receptors controls synaptic and behavioral adaptations to amphetamine. Nat Neurosci 12:602-610.
37. May V, Schiller MR, Eipper BA, and Mains RE (2002) Kalirin Dbl-homology guanine nucleotide exchange factor 1 domain initiates new axon outgrowths via RhoG-mediated mechanisms. J Neurosci 22:6980-6990. (Pubitemid 35379156)
38. Meyer DA, Richer E, Benkovic SA, Hayashi K, Kansy JW, Hale CF, Moy LY, Kim Y, O'Callaghan JP, and Tsai LH et al. (2008) Striatal dysregulation of Cdk5 alters locomotor responses to cocaine, motor learning, and dendritic morphology. Proc Natl Acad Sci USA 105:18561-18566.
39. Miyatake R, Furukawa A, and Suwaki H (2002) Identification of a novel variant of the human NR2B gene promoter region and its possible association with schizophrenia. Mol Psychiatry 7:1101-1106. (Pubitemid 36044269)
40. Myers SJ, Dingledine R, and Borges K (1999) Genetic regulation of glutamate receptor ion channels. Annu Rev Pharmacol Toxicol 39:221-241. (Pubitemid 29222558)
41. Nestler EJ (2005) Is there a common molecular pathway for addiction? Nat Neurosci 8:1445-1449.
42. Norrholm SD, Bibb JA, Nestler EJ, Ouimet CC, Taylor JR, and 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. (Pubitemid 36110427)
43. Pascoli V, Besnard A, Hervé D, Pagès C, Heck N, Girault JA, Caboche J, and Vanhoutte P (2011) Cyclic adenosine monophosphate-independent tyrosine phosphorylation of NR2B mediates cocaine-induced extracellular signal-regulated kinase activation. Biol Psychiatry 69:218-227.
44. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, and Davis MM et al. (2008) Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59:621-633.
45. Qiang M, Denny A, Lieu M, Carreon S, and Li J (2011) Histone H3K9 modifications are a local chromatin event involved in ethanol-induced neuroadaptation of the NR2B gene. Epigenetics 6:1095-1104.
46. Qiang M, Rani CS, and Ticku MK (2005) Neuron-restrictive silencer factor regulates the N-methyl-D-aspartate receptor 2B subunit gene in basal and ethanol-induced gene expression in fetal cortical neurons. Mol Pharmacol 67:2115-2125. (Pubitemid 41007792)
47. Rani CS, Qiang M, and Ticku MK (2005) Potential role of cAMP response element-binding protein in ethanol-induced N-methyl-D-aspartate receptor 2B subunit gene transcription in fetal mouse cortical cells. Mol Pharmacol 67:2126-2136. (Pubitemid 41007793)
48. Robinson TE, Gorny G, Mitton E, and Kolb B (2001) Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39:257-266. (Pubitemid 32099681)
49. Robinson TE and Kolb B (1997) Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491-8497. (Pubitemid 27461070)
50. Rodenas-Ruano A, Chávez AE, Cossio MJ, Castillo PE, and Zukin RS (2012) REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat Neurosci 15:1382-1390.
51. Rothenfluh A and Cowan CW (2013) Emerging roles of actin cytoskeleton regulating enzymes in drug addiction: actin or reactin'? Curr Opin Neurobiol 23:507-512.
52. Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, and Nestler EJ (2010) The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33:267-276.
53. SAMSHA (2012) Results from the 2011 National Survey on Drug Use and Health: Summary of National Findings, NSDUH Series H-44.
54. Schmidt HD, Anderson SM, Famous KR, Kumaresan V, and Pierce RC (2005) Anatomy and pharmacology of cocaine priming-induced reinstatement of drug seeking. Eur J Pharmacol 526:65-76. (Pubitemid 41744106)
55. Shiflett MW and Balleine BW (2011) Molecular substrates of action control in corticostriatal circuits. Prog Neurobiol 95:1-13.
56. Thomsen M and Caine SB (2005) Chronic intravenous drug self-administration in rats and mice. Curr Protoc Neurosci 32:9.20.1-9.20.40 DOI: 10.1002/0471142301.ns0920s32.
57. Thomsen M and Caine SB (2007) Intravenous drug self-administration in mice: practical considerations. Behav Genet 37:101-118. (Pubitemid 46150857)
58. van Spronsen M and Hoogenraad CC (2010) Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10:207-214.
59. Yang BZ, Han S, Kranzler HR, Farrer LA, and Gelernter J (2011) A genomewide linkage scan of cocaine dependence and major depressive episode in two populations. Neuropsychopharmacology 36:2422-2430.