The relationship between duration of initial alcohol exposure and persistence of molecular tolerance is markedly nonlinear

Journal of Neuroscience

Volumn 31, Issue 7, 2011, Pages 2436-2446

  Velázquez Marrero, Cristina ^a   Wynne, Patricia ^b   Bernardo, Alexandra ^a   Palacio, Stephanie ^a   Martin, Gilles ^b   Treistman, Steven N ^a  

^a UNIVERSITY OF PUERTO RICO MEDICAL SCIENCES CAMPUS   (Puerto Rico)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; MESSENGER RNA;

ALCOHOL CONSUMPTION; ALCOHOL TOLERANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CORPUS STRIATUM; EXON; HUMAN; HUMAN CELL; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REWARD; RNA SPLICING;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELL SURVIVAL; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CORPUS STRIATUM; DNA, RECOMBINANT; ETHANOL; EXONS; HUMANS; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; NEURONS; NONLINEAR DYNAMICS; RATS; RATS, SPRAGUE-DAWLEY; RNA SPLICING; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS; UP-REGULATION;

EID: 79951846089     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5429-10.2011     Document Type: Article

References (50)

1. Ahmed SH, Koob GF (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282:298-300. (Pubitemid 28487203)
2. Behrens R, Nolting A, Reimann F, Schwarz M, Waldschütz R, Pongs O (2000) hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett 474:99-106. (Pubitemid 30320840)
3. Ben-Shahar O, Moscarello JM, Ettenberg A (2006) One hour, but not 6 hours, of daily access to self-administered cocaine results in elevated levels of the dopamine transporter. Brain Res 1095:148-153. (Pubitemid 43866013)
4. Borlikova GG, Le Merrer J, Stephens DN (2006) Previous experience of ethanol withdrawal increases withdrawal-induced c-fos expression in limbic areas, but not withdrawal-induced anxiety and prevents withdrawal-induced elevations in plasma corticosterone. Psychopharmacology (Berl) 185:188-200. (Pubitemid 43363615)
5. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serumfree medium combination. J Neurosci Res 35:567-576. (Pubitemid 23215708)
6. Chen L, Tian L, MacDonald SH, McClafferty H, Hammond MS, Huibant JM, Ruth P, Knaus HG, Shipston MJ (2005) Functionally diverse complement of large conductance calcium- and voltage-activated potassium channel (BK) alpha-subunits generated from a single site of splicing. J Biol Chem 280:33599-33609. (Pubitemid 41397161)
7. Coe IR, Dohrman DP, Constantinescu A, Diamond I, Gordon AS (1996) Activation of cyclic AMP-dependent protein kinase reverses tolerance of a nucleoside transporter to ethanol. J Pharmacol Exp Ther 276:365-369. (Pubitemid 126660469)
8. Cowmeadow RB, Krishnan HR, Atkinson NS (2005) The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol Clin Exp Res 29:1777-1786. (Pubitemid 41579127)
9. Cowmeadow RB, Krishnan HR, Ghezzi A, Al'Hasan YM, Wang YZ, Atkinson NS (2006) Ethanol tolerance caused by slowpoke induction in Drosophila. Alcohol Clin Exp Res 30:745-753.
10. Crabbe JC, Rigter H, Uijlen J, Strijbos C (1979) Rapid development of tolerance to the hypothermic effect of ethanol in mice. J Pharmacol Exp Ther 208:128-133. (Pubitemid 9136467)
11. Crippens D, White ML, George MA, Jaworski JN, Brunner LJ, Lancaster FE, Gonzales RA (1999) Gender differences in blood levels, but not brain levels, of ethanol in rats. Alcohol Clin Exp Res 23:414-420. (Pubitemid 29144833)
12. Dohrman DP, Chen HM, Gordon AS, Diamond I (2002) Ethanol-induced translocation of protein kinase A occurs in two phases: control by different molecular mechanisms. Alcohol Clin Exp Res 26:407-415. (Pubitemid 34225848)
13. Feinberg-Zadek PL, Treistman SN (2007) Beta-subunits are important modulators of the acute response to alcohol in human BK channels. Alcohol Clin Exp Res 31:737-744. (Pubitemid 46587667)
14. Ghezzi A, Al-Hasan YM, Larios LE, Bohm RA, Atkinson NS (2004) slo K(+) channel gene regulation mediates rapid drug tolerance. Proc Natl Acad Sci 101:17276-17281. (Pubitemid 39627810)
15. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100. (Pubitemid 11012976)
16. Hanner M, Vianna-Jorge R, Kamassah A, Schmalhofer WA, Knaus HG, Kaczorowski GJ, Garcia ML (1998) The beta subunit of the high conductance calcium-activated potassium channel. Identification of residues involved in charybdotoxin binding. J Biol Chem 273:16289-16296. (Pubitemid 28311406)
17. 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. (Pubitemid 44476856)
18. Jiang Z, Wallner M, Meera P, Toro L (1999) Human and rodent MaxiK channel beta-subunit genes: cloning and characterization. Genomics 55:57-67. (Pubitemid 29058895)
19. Kalant H (1998) Research on tolerance: what can we learn from history? Alcohol Clin Exp Res 22:67-76.
20. Kelz MB, Chen J, Carlezon WA Jr, Whisler K, Gilden L, Beckmann AM, Steffen C, Zhang YJ, Marotti L, Self DW, Tkatch T, Baranauskas G, Surmeier DJ, Neve RL, Duman RS, Picciotto MR, Nestler EJ (1999) Expression of the transcription factor δFosB in the brain controls sensitivity to cocaine. Nature 401:272-276.
21. Khanna JM, Chau A, Shah G (1996) Characterization of the Phenomenon of rapid tolerance to ethanol. Alcohol 13:621-628. (Pubitemid 26404184)
22. Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, Moss SJ (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci U S A 102:14871-14876. (Pubitemid 41457148)
23. 2+-dependent BK(Ca) channel gating. J Gen Physiol 126:227-241.
24. Lê AD, Kalant H (1992) Influence of intoxicated practice on the development of acute tolerance to the motor impairment effect of ethanol. Psychopharmacology (Berl) 106:572-576.
25. Leveque JC, Macías W, Rajadhyaksha A, Carlson RR, Barczak A, Kang S, Li XM, Coyle JT, Huganir RL, Heckers S, Konradi C (2000) Intracellular modulation of NMDA receptor function by antipsychotic drugs. J Neurosci 20:4011-4020. (Pubitemid 30365671)
26. Lin HH, Chang SJ, Shie HJ, Lai CC (2006) Ethanol inhibition of NMDA-induced responses and acute tolerance to the inhibition in rat rostral ventrolateral medulla in vivo: involvement of cAMP-dependent protein kinases. Neuropharmacology 51:747-755. (Pubitemid 44286931)
27. Lippiat JD, Standen NB, Harrow ID, Phillips SC, Davies NW (2003) Properties of BK(Ca) channels formed by bicistronic expression of hSloalpha and beta1-4 subunits in HEK293 cells. J Membr Biol 192:141-148. (Pubitemid 37011503)
28. Martin G, Puig S, Pietrzykowski A, Zadek P, Emery P, Treistman S (2004) Somatic localization of a specific large-conductance calcium-activated potassium channel subtype controls compartmentalized ethanol sensitivity in the nucleus accumbens. J Neurosci 24:6563-6572. (Pubitemid 38971705)
29. Martin GE, Hendrickson LM, Penta KL, Friesen RM, Pietrzykowski AZ, Tapper AR, Treistman SN (2008) Identification of a BK channel auxiliary protein controlling molecular and behavioral tolerance to alcohol. Proc Natl Acad Sci U S A 105:17543-17548.
30. McManus OB (1991) Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr 23:537-560.
31. 2+-activated K+ channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci U S A 97:5562-5567.
32. Meredith GE, Agolia R, Arts MP, Groenewegen HJ, Zahm DS (1992) Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience 50:149-162.
33. Nestler EJ, Barrot M, Self DW (2001) Delta FosB: A sustained molecular switch for addiction. Proc Natl Acad Sci U S A 98:11042-11046. (Pubitemid 32928680)
34. Pandey SC, Roy A, Mittal N (2001) Effects of chronic ethanol intake and its withdrawal on the expression and phosphorylation of the creb gene transcription factor in rat cortex. J Pharmacol Exp Ther 296:857-868. (Pubitemid 32187358)
35. Pandey SC, Roy A, Zhang H (2003) The decreased phosphorylation of cyclic adenosine monophosphate (cAMP) response element binding (CREB) protein in the central amygdala acts as a molecular substrate for anxiety related to ethanol withdrawal in rats. Alcohol Clin Exp Res 27:396-409. (Pubitemid 36343284)
36. Petrik D, Brenner R (2007) Regulation of STREX exon large conductance, calcium-activated potassium channels by the beta4 accessory subunit. Neuroscience 149:789-803. (Pubitemid 350122887)
37. Pietrzykowski AZ, Martin GE, Puig SI, Knott TK, Lemos JR, Treistman SN (2004) Alcohol tolerance in large-conductance, calcium-activated potassium channels of CNS terminals is intrinsic and includes two components: decreased ethanol potentiation and decreased channel density. J Neurosci 24:8322-8332. (Pubitemid 39280811)
38. Pietrzykowski AZ, Friesen RM, Martin GE, Puig SI, Nowak CL, Wynne PM, Siegelmann HT, Treistman SN (2008) Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59:274-287. (Pubitemid 352033687)
39. Renthal W, Carle TL, Maze I, Covington, HE 3rd, Truong HT, Alibhai I, Kumar A, Montgomery RL, Olson EN, Nestler EJ (2008) Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J Neurosci 28:7344-7349.
40. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28:261-271.
41. Schuckit MA (1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151:184-189.
42. Treistman SN, Martin GE (2009) BK Channels: mediators and models for alcohol tolerance. Trends Neurosci 32:629-637.
43. Vergara C, Latorre R, Marrion NV, Adelman JP (1998) Calcium-activated potassium channels. Curr Opin Neurobiol 8:321-329. (Pubitemid 28288566)
44. 2+ binding sites in a voltage-gated calcium-modulated channel. Implications for survival of K+ permeability. J Gen Physiol 114:365-376.
45. Wang Y, Krishnan HR, Ghezzi A, Yin JC, Atkinson NS (2007) Druginduced epigenetic changes produce drug tolerance. PLoS Biol 5:e265.
46. Wang Y, Ghezzi A, Yin JC, Atkinson NS (2009) CREB regulation of BK channel gene expression underlies rapid drug tolerance. Genes Brain Behav 8:369-376.
47. Wang X, Dayanithi G, Lemos JR, Nordmann JJ, Treistman SN (1991) Calcium currents and peptide release from neurohypophysial terminals are inhibited by ethanol. J Pharmacol Exp Ther 259:705 711.
48. Xia XM, Zeng X, Lingle CJ (2002) Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature 418:880-884. (Pubitemid 34966307)
49. Xie J, McCobb DP (1998) Control of alternative splicing of potassium channels by stress hormones. Science 280:443-446. (Pubitemid 28208168)
50. Yuan C, O'Connell RJ, Wilson A, Pietrzykowski AZ, Treistman SN (2008) Acute alcohol tolerance is intrinsic to the BKCa protein, but is modulated by the lipid environment. J Biol Chem 283:5090-5098.