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Invertebrate Models of Alcoholism

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Behavioral Neurobiology of Alcohol Addiction

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 13))

Abstract

For invertebrates to become useful models for understanding the genetic and physiological mechanisms of alcoholism related behaviors and the predisposition towards alcoholism, several general requirements must be fulfilled. The animal should encounter ethanol in its natural habitat, so that the central nervous system of the organism will have evolved mechanisms for responding to ethanol exposure. How the brain adapts to ethanol exposure depends on its access to ethanol, which can be regulated metabolically and/or by physical barriers. Therefore, a model organism should have metabolic enzymes for ethanol degradation similar to those found in humans. The neurons and supporting glial cells of the model organism that regulate behaviors affected by ethanol should share the molecular and physiological pathways found in humans, so that results can be compared. Finally, the use of invertebrate models should offer advantages over traditional model systems and should offer new insights into alcoholism-related behaviors. In this review we will summarize behavioral similarities and identified genes and mechanisms underlying ethanol-induced behaviors in invertebrates. This review mainly focuses on the use of the nematode Caenorhabditis elegans, the honey bee Apis mellifera and the fruit fly Drosophila melanogaster as model systems. We will discuss insights gained from those studies in conjunction with their vertebrate model counterparts and the implications for future research into alcoholism and alcohol-induced behaviors.

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Abbreviations

ADH:

Alcohol dehydrogenase

ALDH:

Aldehyde dehydrogenase

GABA:

Gamma-aminobutyric acid

NPY:

Neuropeptide Y

NPF:

Neuropeptide F

PKA:

cAMP Dependent protein kinase A

EGF:

Epidermal growth factor

GRASP:

Green-fluorescent protein function across synaptic partners

QTL:

Quantitative trait loci

DSM-IV:

Fourth edition of the diagnostic and statistical manual of mental disorders

References

  • Abramson CI, Stone SM, Ortez RA, Luccardi A, Vann KL, Hanig KD, Rice J (2000) The development of an ethanol model using social insects I: behavior studies of the honey bee (Apis mellifera L.). Alcohol Clin Exp Res 24(8):1153–1166

    Article  CAS  PubMed  Google Scholar 

  • Abramson CI, Kandolf A, Sheridan A, Donohue D, Bozic J, Meyers JE, Benbassat D (2004a) Development of an ethanol model using social insects: III. Preferences for ethanol solutions. Psychol Rep 94(1):227–239

    Article  PubMed  Google Scholar 

  • Abramson CI, Place AJ, Aquino IS, Fernandez A (2004b) Development of an ethanol model using social insects: IV. Influence of ethanol on the aggression of Africanized honey bees (Apis mellifera L.). Psychol Rep 94(3 Pt 2):1107–1115

    PubMed  Google Scholar 

  • Ammons AD, Hunt GJ (2008a) Identification of Quantitative Trait Loci and candidate genes influencing ethanol sensitivity in honey bees. Behav Genet 38(5):531–553

    Article  PubMed  Google Scholar 

  • Ammons AD, Hunt GJ (2008b) Characterization of honey bee sensitivity to ethanol vapor and its correlation with aggression. Alcohol 42(2):129–136

    Article  CAS  PubMed  Google Scholar 

  • Bainton RJ, Tsai LT, Singh CM, Moore MS, Neckameyer WS, Heberlein U (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10(4):187–194

    Article  CAS  PubMed  Google Scholar 

  • Bell RL, Rodd ZA, Lumeng L, Murphy JM, McBride WJ (2006) The alcohol-preferring P rat and animal models of excessive alcohol drinking. Addict Biol 11(3–4):270–288

    Article  PubMed  Google Scholar 

  • Bennett B, Downing C, Parker C, Johnson TE (2006) Mouse genetic models in alcohol research. Trends Genet 22(7):367–374

    Article  CAS  PubMed  Google Scholar 

  • Berger KH, Heberlein U, Moore MS (2004) Rapid and chronic: two distinct forms of ethanol tolerance in Drosophila. Alcohol Clin Exp Res 28(10):1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Berry MD (2004) Mammalian central nervous system trace amines. Pharmacologic amphetamines, physiologic neuromodulators. J Neurochem 90(2):257–271

    Article  CAS  PubMed  Google Scholar 

  • Bettinger JC, McIntire SL (2004) State-dependency in C. elegans. Genes Brain Behav 3(5):266–272

    Article  CAS  PubMed  Google Scholar 

  • Bitterman ME, Menzel R, Fietz A, Schafer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97(2):107–119

    Article  CAS  PubMed  Google Scholar 

  • Blatt J, Roces F (2002) The control of the proventriculus in the honeybee (Apis mellifera carnica L.) II. Feedback mechanisms. J Insect Physiol 48(7):683–691

    Article  CAS  PubMed  Google Scholar 

  • Bolla RI, Weaver C, Koslowski P, Fitzsimmons K, Winter RE (1987) Characterization of a nonparasitic isolate of Bursaphelenchus xylophilus. J Nematol 19(3):304–310

    CAS  PubMed Central  PubMed  Google Scholar 

  • Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP, Bonini JA, Pathirana S, Boyle N, Pu XS, Kouranova E, Lichtblau H, Ochoa FY, Branchek TA, Gerald C (2001) Trace amines: Identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci USA 98(16):8966–8971

    Article  CAS  PubMed  Google Scholar 

  • Bouga M, Kilias G, Harizanis PC, Papasotiropoulos V, Alahiotis S (2005) Allozyme variability and phylogenetic relationships in honey bee (Hymenoptera: Apidae: Apis mellifera) populations from Greece and Cyprus. Biochem Genet 43(9–10):471–483

    Article  CAS  PubMed  Google Scholar 

  • Bozic J, DiCesare J, Wells H, Abramson CI (2007) Ethanol levels in honeybee hemolymph resulting from alcohol ingestion. Alcohol 41(4):281–284

    Article  CAS  PubMed  Google Scholar 

  • Brodie MS, Scholz A, Weiger TM, Dopico AM (2007) Ethanol interactions with calcium-dependent potassium channels. Alcohol Clin Exp Res 31(10):1625–1632

    Article  CAS  PubMed  Google Scholar 

  • Cohan FM, Hoffmann AA (1986) Genetic divergence under uniform selection. II. Different responses to selection for knockdown resistance to ethanol among Drosophila melanogaster populations and their replicate lines. Genetics 114(1):145–164

    CAS  PubMed  Google Scholar 

  • Colbert HA, Bargmann CI (1995) Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14(4):803–812

    Article  CAS  PubMed  Google Scholar 

  • Colombo G, Addolorato G, Agabio R, Carai MA, Pibiri F, Serra S, Vacca G, Gessa GL (2004) Role of GABA(B) receptor in alcohol dependence: reducing effect of baclofen on alcohol intake and alcohol motivational properties in rats and amelioration of alcohol withdrawal syndrome and alcohol craving in human alcoholics. Neurotox Res 6(5):403–414

    Article  PubMed  Google Scholar 

  • Corl AB, Rodan AR, Heberlein U (2005) Insulin signaling in the nervous system regulates ethanol intoxication in Drosophila melanogaster. Nat Neurosci 8:18–19

    Article  CAS  PubMed  Google Scholar 

  • Corl AB, Berger KH, Ophir-Shohat G, Gesch J, Simms JA, Bartlett SE, Heberlein U (2009) Happyhour, a Ste20 family kinase, implicates EGFR signaling in ethanol-induced behaviors. Cell 137(5):949–960

    Article  CAS  PubMed  Google Scholar 

  • Cowmeadow RB, Krishnan HR, Atkinson NS (2005) The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol Clin Exp Res 29(10):1777–1786

    Article  CAS  PubMed  Google Scholar 

  • 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(5):745–753

    Article  CAS  PubMed  Google Scholar 

  • Davenport AP, Evans PD (1984) Stress-induced changes in the octopamine levels of insect hemolymph. Insect Biochem 14(2):135–143

    Article  CAS  Google Scholar 

  • Davies AG, McIntire SL (2004) Using C. elegans to screen for targets of ethanol and behavior-altering drugs. Biol Proced Online 6113–6119

    Google Scholar 

  • Davies AG, Pierce-Shimomura JT, Kim H, VanHoven MK, Thiele TR, Bonci A, Bargmann CI, McIntire SL (2003) A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 115(6):655–666

    Article  CAS  PubMed  Google Scholar 

  • Davies AG, Bettinger JC, Thiele TR, Judy ME, McIntire SL (2004) Natural variation in the npr-1 gene modifies ethanol responses of wild strains of C. elegans. Neuron 42(5):731–743

    Article  CAS  PubMed  Google Scholar 

  • Davis JR, Li Y, Rankin CH (2008) Effects of developmental exposure to ethanol on Caenorhabditis elegans. Alcohol Clin Exp Res 32(5):853–867

    Article  CAS  PubMed  Google Scholar 

  • de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94(5):679–689

    Article  PubMed  Google Scholar 

  • Deroche-Gamonet V, Belin D, Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014–1017

    Article  CAS  PubMed  Google Scholar 

  • Devineni AV, Heberlein U (2009) Preferential ethanol consumption in Drosophila models features of addiction. Curr Biol 19(24):2126–2132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dhawan R, Dusenbery DB, Williams PL (1999) Comparison of lethality, reproduction, and behavior as toxicological endpoints in the nematode Caenorhabditis elegans. J Toxicol Environ Health A 58(7):451–462

    Article  CAS  PubMed  Google Scholar 

  • Diamond I, Gordon AS (1997) Cellular and molecular neuroscience of alcoholism. Physiol Rev 77(1):1–20

    CAS  PubMed  Google Scholar 

  • Dierks A, Fischer K (2008) Feeding responses and food preferences in the tropical, fruit-feeding butterfly, Bicyclus anynana. J Insect Physiol 54(9):1363–1370

    Article  CAS  PubMed  Google Scholar 

  • Dudley R (2002) Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover? Addiction 97(4):381–388

    Article  PubMed  Google Scholar 

  • Dzitoyeva S, Dimitrijevic N, Manev H (2003) Gamma-aminobutyric acid B receptor 1 mediates behavior-impairing actions of alcohol in Drosophila: adult RNA interference and pharmacological evidence. Proc Natl Acad Sci USA 100(9):5485–5490

    Article  CAS  PubMed  Google Scholar 

  • Eckenhoff RG, Yang BJ (1994) Absence of pressure antagonism of ethanol narcosis in C. elegans. Neuroreport 6(1):77–80

    Article  CAS  PubMed  Google Scholar 

  • Feinberg EH, Vanhoven MK, Bendesky A, Wang G, Fetter RD, Shen K, Bargmann CI (2008) GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57(3):353–363

    Article  CAS  PubMed  Google Scholar 

  • Foa L, Gasperini R (2009) Developmental roles for Homer: more than just a pretty scaffold. J Neurochem 108(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Fry JD, Saweikis M (2006) Aldehyde dehydrogenase is essential for both adult and larval ethanol resistance in Drosophila melanogaster. Genet Res 87(2):87–92

    Article  CAS  PubMed  Google Scholar 

  • Fukuda M (2008) Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol Life Sci 65(18):2801–2813

    Article  CAS  PubMed  Google Scholar 

  • Geer BW, Langevin ML, McKechnie SW (1985) Dietary ethanol and lipid synthesis in Drosophila melanogaster. Biochem Genet 23(7–8):607–622

    Article  CAS  PubMed  Google Scholar 

  • Geer BW, Heinstra PW, McKechnie SW (1993) The biological basis of ethanol tolerance in Drosophila. Comp Biochem Physiol B 105(2):203–229

    Article  CAS  PubMed  Google Scholar 

  • Ghezzi A, Pohl JB, Wang Y, Atkinson NS (2010) BK channels play a counter-adaptive role in drug tolerance and dependence. Proc Natl Acad Sci USA 107(37):16360–16365

    Article  CAS  PubMed  Google Scholar 

  • Gibson JB, Oakeshott JG (1981) Genetics of biochemical and behavioural aspects of alcohol metabolism. Aust N Z J Med 11(2):128–131

    Article  CAS  PubMed  Google Scholar 

  • Giles AC, Rankin CH (2009) Behavioral and genetic characterization of habituation using Caenorhabditis elegans. Neurobiol Learn Mem 92(2):139–146

    Article  PubMed  Google Scholar 

  • Gilliam M (1979) Microbiology of pollen and bee bread—the yeasts. Apidologie 10(1):43–53

    Article  Google Scholar 

  • Glasner JD, Kocher TD, Collins JJ (1995) Caenorhabditis elegans contains genes encoding two new members of the Zn-containing alcohol dehydrogenase family. J Mol Evol 41(1):46–53

    Article  CAS  PubMed  Google Scholar 

  • Godenschwege TA, Reisch D, Diegelmann S, Eberle K, Funk N, Heisenberg M, Hoppe V, Hoppe J, Klagges BR, Martin JR, Nikitina EA, Putz G, Reifegerste R, Reisch N, Rister J, Schaupp M, Scholz H, Schwarzel M, Werner U, Zars TD, Buchner S, Buchner E (2004) Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 20(3):611–622

    Article  PubMed  Google Scholar 

  • Goodrich KR, Zjhra ML, Ley CA, Raguso RA (2006) When flowers smell fermented: The chemistry and ontogeny of yeasty floral scent in pawpaw (Asimina triloba : Annonaceae). Int J Plant Sci 167(1):33–46

    Article  CAS  Google Scholar 

  • Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61(3):373–384

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Graham ME, Edwards MR, Holden-Dye L, Morgan A, Burgoyne RD, Barclay JW (2009) UNC-18 modulates ethanol sensitivity in Caenorhabditis elegans. Mol Biol Cell 20(1):43–55

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grell EH, Jacobson KB, Murphy JB (1968) Alterations of genetics material for analysis of alcohol dehydrogenase isozymes of Drosophila melanogaster. Ann N Y Acad Sci 151(1):441–455

    Article  CAS  PubMed  Google Scholar 

  • Heinz A (2002) Dopaminergic dysfunction in alcoholism and schizophrenia—psychopathological and behavioral correlates. Eur Psychiat 17(1):9–16

    Article  CAS  Google Scholar 

  • Hill JK, Hamer KC, Tangah J, Dawood M (2001) Ecology of tropical butterflies in rainforest gaps. Oecologia 128(2):294–302

    Article  Google Scholar 

  • Holmes RS (1994) Alcohol dehydrogenases: a family of isozymes with differential functions. Alcohol and alcoholism (Oxford, Oxfordshire) 2127–2130

    Google Scholar 

  • Hong M, Choi MK, Lee J (2008) The anesthetic action of ethanol analyzed by genetics in Caenorhabditis elegans. Biochem Biophys Res Commun 367(1):219–225

    Article  CAS  PubMed  Google Scholar 

  • Ikemoto MJ, Inoue K, Akiduki S, Osugi T, Imamura T, Ishida N, Ohtomi M (2002) Identification of addicsin/GTRAP3–18 as a chronic morphine-augmented gene in amygdala. Neuroreport 13(16):2079–2084

    Article  CAS  PubMed  Google Scholar 

  • Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, Benzer S (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci USA 104(20):8253–8256

    Article  CAS  PubMed  Google Scholar 

  • Jones WD (2009) The expanding reach of the GAL4/UAS system into the behavioral neurobiology of Drosophila. BMB Rep 42(11):705–712

    Article  CAS  PubMed  Google Scholar 

  • Kapfhamer D, Bettinger JC, Davies AG, Eastman CL, Smail EA, Heberlein U, McIntire SL (2008) Loss of RAB-3/A in Caenorhabditis elegans and the mouse affects behavioral response to ethanol. Genes Brain Behav 7(6):669–676

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kasanetz F, Deroche-Gamonet V, Berson N, Balado E, Lafourcade M, Manzoni O, Piazza PV (2010) Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328:1709–1712

    Article  CAS  PubMed  Google Scholar 

  • Kayser E-B, Morgan PG, Hoppel CL, Sedensky MM (2001) Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J Biol Chem 276:205551–220558

    Article  Google Scholar 

  • Kong EC, Woo K, Li H, Lebestky T, Mayer N, Sniffen MR, Heberlein U, Bainton RJ, Hirsh J, Wolf FW (2010) A pair of dopamine neurons target the D1-like dopamine receptor DopR in the central complex to promote ethanol-stimulated locomotion in Drosophila. PLoS One 5(4):e9954

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kreek MJ, Nielsen DA, LaForge KS (2004) Genes associated with addiction: alcoholism, opiate, and cocaine addiction. Neuromolecular Med 5(1):85–108

    Article  CAS  PubMed  Google Scholar 

  • Lai SL, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9(5):703–709

    Article  CAS  PubMed  Google Scholar 

  • Laviola G, Hannan AJ, Macri S, Solinas M, Jaber M (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31(2):159–168

    Article  PubMed  Google Scholar 

  • Lee HG, Kim YC, Dunning JS, Han KA (2008) Recurring ethanol exposure induces disinhibited courtship in Drosophila. PLoS One 3(1):e1391

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee J, Jee C, McIntire SL (2009) Ethanol preference in C. elegans. Genes Brain Behav 8(6):578–585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li C, Zhao X, Cao X, Chu D, Chen J, Zhou J (2008) The Drosophila homolog of jwa is required for ethanol tolerance. Alcohol Alcohol 43(5):529–536

    Article  CAS  PubMed  Google Scholar 

  • Luo L, Callaway EM, Svoboda K (2008) Genetic dissection of neural circuits. Neuron 57(5):634–660

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maas JW Jr, Vogt SK, Chan GC, Pineda VV, Storm DR, Muglia LJ (2005) Calcium-stimulated adenylyl cyclases are critical modulators of neuronal ethanol sensitivity. J Neurosci 25(16):4118–4126

    Article  CAS  PubMed  Google Scholar 

  • Maleknia SD, Vail TM, Cody RB, Sparkman DO, Bell TL, Adams MA (2009) Temperature-dependent release of volatile organic compounds of eucalypts by direct analysis in real time (DART) mass spectrometry. Rapid Commun Mass Spectrom 23(15):2241–2246

    Article  CAS  PubMed  Google Scholar 

  • Martins E, Mestriner MA, Contel EP (1977) Alcohol dehydrogenase polymorphism in Apis mellifera. Biochem Genetics 15(3–4):357–366

    Article  CAS  Google Scholar 

  • Maze IS, Wright GA, Mustard JA (2006) Acute ethanol ingestion produces dose-dependent effects on motor behavior in the honey bee (Apis mellifera). J Insect Physiol 52(11–12):1243–1253

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McKenzie JA, Parsons PA (1972) Alcohol Tolerance—Ecological parameter in relative success of Drosophila-melanogaster and Drosophila-simulans. Oecologia 10(4):373–388

    Article  Google Scholar 

  • Menzel R, Giurfa M (2006) Dimensions of cognition in an insect, the honeybee. Behav Cogn Neurosci Rev 5:24–40

    Article  PubMed  Google Scholar 

  • Mitchell PH, Bull K, Glautier S, Hopper NA, Holden-Dye L, O’Connor V (2007) The concentration-dependent effects of ethanol on Caenorhabditis elegans behaviour. Pharmacogenomics J 7(6):411–417

    Article  CAS  PubMed  Google Scholar 

  • Mitchell P, Mould R, Dillon J, Glautier S, Andrianakis I, James C, Pugh A, Holden-Dye L, O’Connor V (2010) A differential role for neuropeptides in acute and chronic adaptive responses to alcohol: behavioural and genetic analysis in Caenorhabditis elegans. PLoS One 5:e10422

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Moore MS, DeZazzo J, Luk AY, Tully T, Singh CM, Heberlein U (1998) Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93(6):997–1007

    Article  CAS  PubMed  Google Scholar 

  • Morgan PG, Sedensky MM (1995) Mutations affecting sensitivity to ethanol in the nematode, Caenorhabditis elegans. Alcohol Clin Exp Res 19(6):1423–1429

    Article  CAS  PubMed  Google Scholar 

  • Mustard JA, Edgar EA, Mazade RE, Wu C, Lillvis JL, Wright GA (2008) Acute ethanol ingestion impairs appetitive olfactory learning and odor discrimination in the honey bee. Neurobiol Learn Mem 90(4):633–643

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nestler EJ (2002) Common molecular and cellular substrates of addiction and memory. Neurobiol Learn Mem 78(3):637–647

    Article  CAS  PubMed  Google Scholar 

  • Ogueta M, Cibik O, Eltrop R, Schneider A, Scholz H (2010) The influence of ADH function on ethanol preference and tolerance in adult Drosophila melanogaster. Chem Senses 35(9):813–822

    Article  CAS  PubMed  Google Scholar 

  • Olsen SR, Wilson RI (2008) Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci 31(10):512–520

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Park SK, Sedore SA, Cronmiller C, Hirsh J (2000) Type II cAMP-dependent protein kinase-deficient Drosophila are viable but show developmental, circadian, and drug response phenotypes. J Biol Chem 275(27):20588–20596

    Article  CAS  PubMed  Google Scholar 

  • Parr J, Large A, Wang X, Fowler SC, Ratzlaff KL, Ruden DM (2001) The inebri-actometer: a device for measuring the locomotor activity of Drosophila exposed to ethanol vapor. J Neurosci Methods 107(1–2):93–99

    Article  CAS  PubMed  Google Scholar 

  • Petriv OI, Rachubinski RA (2004) Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J Biol Chem 279(19):19996–20001

    Article  CAS  PubMed  Google Scholar 

  • Premont RT, Gainetdinov RR, Caron MG (2001) Following the trace of elusive amines. Proc Natl Acad Sci USA 98(17):9474–9475

    Article  CAS  PubMed  Google Scholar 

  • Ramazani RB, Krishnan HR, Bergeson SE, Atkinson NS (2007) Computer automated movement detection for the analysis of behavior. J Neurosci Methods 162(1–2):171–179

    Article  PubMed Central  PubMed  Google Scholar 

  • Ranger CM, Reding ME, Persad AB, Herms DA (2010) Ability of stress-related volatiles to attract and induce attacks by Xylosandrus germanus and other ambrosia beetles. Agr Forest Entomol 12(2):177–185

    Article  Google Scholar 

  • Riley BP, Kalsi G, Kuo PH, Vladimirov V, Thiselton DL, Vittum J, Wormley B, Grotewiel MS, Patterson DG, Sullivan PF, van den Oord E, Walsh D, Kendler KS, Prescott CA (2006) Alcohol dependence is associated with the ZNF699 gene, a human locus related to Drosophila hangover, in the Irish Affected Sib Pair Study of Alcohol Dependence (IASPSAD) sample. Mol Psychiatry 11(11):1025–1031

    Article  CAS  PubMed  Google Scholar 

  • Rodan AR, Kiger JA Jr, Heberlein U (2002) Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J Neurosci 22(21):9490–9501

    CAS  PubMed  Google Scholar 

  • Rothenfluh A, Threlkeld RJ, Bainton RJ, Tsai LT, Lasek AW, Heberlein U (2006) Distinct behavioral responses to ethanol are regulated by alternate RhoGAP18B isoforms. Cell 127(1):199–211

    Article  CAS  PubMed  Google Scholar 

  • Saeki S, Yamamoto M, Iino Y (2001) Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 204(Pt 10):1757–1764

    CAS  PubMed  Google Scholar 

  • Scholz H (2005) Influence of the biogenic amine tyramine on ethanol-induced behaviors in Drosophila. J Neurobiol 63(3):199–214

    Article  CAS  PubMed  Google Scholar 

  • Scholz H (2009) Intoxicated fly brains: neurons mediating ethanol-induced behaviors. J Neurogenet 23(1–2):111–119

    Article  CAS  PubMed  Google Scholar 

  • Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28(1):261–271

    Article  CAS  PubMed  Google Scholar 

  • Scholz H, Franz M, Heberlein U (2005) The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436(7052):845–847

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schuckit MA (1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151(2):184–189

    CAS  PubMed  Google Scholar 

  • Singh CM, Heberlein U (2000) Genetic control of acute ethanol-induced behaviors in Drosophila. Alcohol Clin Exp Res 24(8):1127–1136

    Article  CAS  PubMed  Google Scholar 

  • Sommer W, Hyytia P, Kiianmaa K (2006) The alcohol-preferring AA and alcohol-avoiding ANA rats: neurobiology of the regulation of alcohol drinking. Addict Biol 11:289–309

    Article  PubMed  Google Scholar 

  • Spanagel R, Hölter SM, Allingham K, Landgraf R, Zieglgänsberger W (1996) Acomprosate and alcohol: I. Effects on alcohol intake foloowing alcohol depreivation in the rat. Eur J Pharmacol 305:39–44

    Article  CAS  PubMed  Google Scholar 

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12(6):633–638

    Article  CAS  PubMed  Google Scholar 

  • Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56(1):110–156

    Article  CAS  PubMed  Google Scholar 

  • Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100(1):64–119

    Article  CAS  PubMed  Google Scholar 

  • Tabakoff B Ritzmann RF (1977) The effect of 6-hydroxydopamine on tolerance to and dependence of ethanol. J Pharmacol Exp Ther 203(2): 319–331

    CAS  PubMed  Google Scholar 

  • Thompson G, de Pomerai DI (2005) Toxicity of short-chain alcohols to the nematode Caenorhabditis elegans: a comparison of endpoints. J Biochem Mol Toxicol 19(2):87–95

    Article  CAS  PubMed  Google Scholar 

  • Thorsell A (2007) Neuropeptide Y (NPY) in alcohol intake and dependence. Peptides 28(2):480–483

    Article  CAS  PubMed  Google Scholar 

  • Treistman SN, Martin GE (2009) BK channels: Mediators and models for alcohol tolerance. Trends Neurosci 32(12):629–637

    Article  CAS  PubMed  Google Scholar 

  • Urizar NL, Yang Z, Edenberg HJ, Davis RL (2007) Drosophila homer is required in a small set of neurons including the ellipsoid body for normal ethanol sensitivity and tolerance. J Neurosci 27(17):4541–4551

    Article  CAS  PubMed  Google Scholar 

  • Wen T, Parrish CA, Xu D, Wu Q, Shen P (2005) Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci USA 102(6):2141–2146

    Article  CAS  PubMed  Google Scholar 

  • White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode C. elegans. Philos Trans R Soc Lond B 314:1–340

    Article  CAS  Google Scholar 

  • Wiens F, Zitzmann A, Lachance MA, Yegles M, Pragst F, Wurst FM, von Holst D, Guan SL, Spanagel R (2008) Chronic intake of fermented floral nectar by wild treeshrews. Proc Natl Acad Sci USA 105(30):10426–10431

    Article  CAS  PubMed  Google Scholar 

  • Williamson VM, Long M, Theodoris G (1991) Isolation of Caenorhabditis elegans mutants lacking alcohol dehydrogenase activity. Biochem Genet 29(7–8):313–323

    Article  CAS  PubMed  Google Scholar 

  • Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94(4):469–492

    Article  CAS  PubMed  Google Scholar 

  • Wolf FW, Rodan AR, Tsai LT, Heberlein U (2002) High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila. J Neurosci 22(24):11035–11044

    CAS  PubMed  Google Scholar 

  • Wood WB (1988) Determination of pattern and fate in early embryos of Caenorhabditis elegans. Dev Biol (N Y 1985) 557–578

    Google Scholar 

Download references

Acknowledgments

The present work was supported in part by the DFG 656 and the Heisenberg program of the DFG to HS. We thank Oliver Hendrich for critically reading the manuscript. We have tried to incorporate as many studies as possible, and we apologize for not being able to include all of the papers on this topic.

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Correspondence to Henrike Scholz .

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Scholz, H., Mustard, J.A. (2011). Invertebrate Models of Alcoholism. In: Sommer, W., Spanagel, R. (eds) Behavioral Neurobiology of Alcohol Addiction. Current Topics in Behavioral Neurosciences, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28720-6_128

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