Alcohol resistance in Drosophila is modulated by the Toll innate immune pathway

Genes, Brain and Behavior

Volumn 15, Issue 4, 2016, Pages 382-394

  Troutwine, B R ^a   Ghezzi, A ^a   Pietrzykowski, A Z ^b   Atkinson, N S ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b University of Massachusetts Amherst   (United States)

Author keywords

Addiction; Alcohol resistance; Alcohol sensitivity; Alcoholism; Ethanol; Innate immunity; Mutations; Neuroimmune; NF B; RNAi; Tolerance

Indexed keywords

ALCOHOL; TOLL LIKE RECEPTOR; DROSOPHILA PROTEIN;

ALCOHOL TOLERANCE; ALCOHOL USE DISORDER; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENETIC MANIPULATION; INNATE IMMUNITY; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEDATION; ANIMAL; ANIMAL MODEL; DRINKING BEHAVIOR; DRUG EFFECTS; DRUG TOLERANCE; GENETICS; IMMUNOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ALCOHOL DRINKING; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; DRUG TOLERANCE; ETHANOL; FEMALE; IMMUNITY, INNATE; MODELS, ANIMAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84962850866     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12288     Document Type: Article

References (84)

1. Anderson, K.V. & Nüsslein-Volhard, C. (1984) Information for the dorsal-ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311, 223-227.
2. Ausubel, F. (1994) Current Protocols in Molecular Biology. Wiley, New York, NY.
3. Bajo, M., Madamba, S.G., Roberto, M., Blednov, Y.A., Sagi, V.N., Roberts, E., Rice, K.C., Harris, R.A. & Siggins, G.R. (2014) Innate immune factors modulate ethanol interaction with GABAergic transmission in mouse central amygdala. Brain Behav Immun 40, 191-202.
4. Bettencourt, R., Asha, H., Dearolf, C. & Ip, Y.T. (2004) Hemolymph-dependent and -independent responses in Drosophila immune tissue. J Cell Biochem 92, 849-863.
5. Bouchery, E.E., Harwood, H.J., Sacks, J.J., Simon, C.J. & Brewer, R.D. (2011) Economic costs of excessive alcohol consumption in the U.S., 2006. Am J Prev Med 41, 516-524.
6. Brazma, A., Hingamp, P., Quackenbush, J. et al. (2001) Minimum information about a microarray experiment (MIAME) - toward standards for microarray data. Nat Genet 29, 365-371.
7. Buchon, N., Silverman, N. & Cherry, S. (2014) Immunity in Drosophila melanogaster - from microbial recognition to whole-organism physiology. Nat Rev Immunol 14, 796-810.
8. Cowmeadow, R.B., Krishnan, H.R. & Atkinson, N.S. (2005) The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol Clin Exp Res 29, 1777-1786.
9. Crews, F.T., Qin, L., Sheedy, D., Vetreno, R.P. & Zou, J. (2013) High mobility group box 1/Toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry 73, 602-612.
10. Duffy, J.B. (2002) GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 34, 1-15.
11. Dushay, M.S., Asling, B. & Hultmark, D. (1996) Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc Natl Acad Sci U S A 93, 10343-10347.
12. Enoch, M.-A. (2013) Genetic influences on the development of alcoholism. Curr Psychiatry Rep 15, 412.
13. Fang, Y., Soares, L. & Bonini, N.M. (2013) Design and implementation of in vivo imaging of neural injury responses in the adult Drosophila wing. Nat Protoc 8, 810-819.
14. Farris, S.P., Arasappan, D., Hunicke-Smith, S., Harris, R.A. & Mayfield, R.D. (2014) Transcriptome organization for chronic alcohol abuse in human brain. Mol Psychiatry 20, 1438-1447.
15. Flatscher-Bader, T., van der Brug, M., Hwang, J.W., Gochee, P.A., Matsumoto, I., Niwa, S.-I. & Wilce, P.A. (2005) Alcohol-responsive genes in the frontal cortex and nucleus accumbens of human alcoholics. J Neurochem 93, 359-370.
16. Geisler, R., Bergmann, A., Hiromi, Y. & Nüsslein-Volhard, C. (1992) cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the IκB gene family of vertebrates. Cell 71, 613-621.
17. Grant, B.F., Goldstein, R.B., Saha, T.D., Chou, S.P., Jung, J., Zhang, H., Pickering, R.P., Ruan, W.J., Smith, S.M., Huang, B. & Hasin, D.S. (2015) Epidemiology of DSM-5 alcohol use disorder: results from the National Epidemiologic Survey on alcohol and related conditions III. JAMA Psychiatry 72, 757-766.
18. Gross, I., Georgel, P., Kappler, C., Reichhart, J.-M. & Hoffmann, J.A. (1996) Drosophila immunity: a comparative analysis of the Rel proteins dorsal and Dif in the induction of the genes encoding diptericin and cecropin. Nucleic Acids Res 24, 1238-1245.
19. Hashimoto, Y., Tabuchi, Y., Sakurai, K., Kutsuna, M., Kurokawa, K., Awasaki, T., Sekimizu, K., Nakanishi, Y. & Shiratsuchi, A. (2009) Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J Immunol 183, 7451-7460.
20. Heath, A.C., Madden, P.A., Bucholz, K.K., Dinwiddie, S.H., Slutske, W.S., Bierut, L.J., Rohrbaugh, J.W., Statham, D.J., Dunne, M.P., Whitfield, J.B. & Martin, N.G. (1999) Genetic differences in alcohol sensitivity and the inheritance of alcoholism risk. Psychol Med 29, 1069-1081.
21. Hecht, P.M. & Anderson, K.V. (1993) Genetic characterization of tube and pelle, genes required for signaling between Toll and dorsal in the specification of the dorsal-ventral pattern of the Drosophila embryo. Genetics 135, 405-417.
22. Hedengren, M., Dushay, M.S., Ando, I., Ekengren, S., Wihlborg, M. & Hultmark, D. (1999) Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Mol Cell 4, 827-837.
23. Hetru, C., Troxler, L. & Hoffmann, J.A. (2003) Drosophila melanogaster antimicrobial defense. J Infect Dis 187 (Suppl), S327-S334.
24. de Hoon, M.J.L., Imoto, S., Nolan, J. & Miyano, S. (2004) Open source clustering software. Bioinformatics 20, 1453-1454.
25. Hu, X., Yagi, Y., Tanji, T., Zhou, S. & Ip, Y.T. (2004) Multimerization and interaction of Toll and Spätzle in Drosophila. Proc Natl Acad Sci U S A 101, 9369-9374.
26. Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37, 1-13.
27. Huang, D.W., Sherman, B.T. & Lempicki, R.A. (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57.
28. Huang, H.-R., Chen, Z.J., Kunes, S., Chang, G.-D. & Maniatis, T. (2010) Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc Natl Acad Sci U S A 107, 8322-8327.
29. Imler, J.-L. (2014) Overview of Drosophila immunity: a historical perspective. Dev Comp Immunol 42, 3-15.
30. Iwamoto, K., Bundo, M., Yamamoto, M., Ozawa, H., Saito, T. & Kato, T. (2004) Decreased expression of NEFH and PCP4/PEP19 in the prefrontal cortex of alcoholics. Neurosci Res 49, 379-385.
31. Kacsoh, B.Z., Lynch, Z.R., Mortimer, N.T. & Schlenke, T.A. (2013) Fruit flies medicate offspring after seeing parasites. Science 339, 947-950.
32. Kong, E.C., Allouche, L., Chapot, P.A., Vranizan, K., Moore, M.S., Heberlein, U. & Wolf, F.W. (2010) Ethanol-regulated genes that contribute to ethanol sensitivity and rapid tolerance in Drosophila. Alcohol Clin Exp Res 34, 302-316.
33. Krishnan, H.R., Al-Hasan, Y.M., Pohl, J.B., Ghezzi, A. & Atkinson, N.S. (2012) A role for dynamin in triggering ethanol tolerance. Alcohol Clin Exp Res 36, 24-34.
34. Lau, G.W., Goumnerov, B.C., Walendziewicz, C.L., Hewitson, J., Xiao, W., Mahajan-Miklos, S., Tompkins, R.G., Perkins, L.A. & Rahme, L.G. (2003) The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun 71, 4059-4066.
35. Lemaitre, B., Meister, M., Govind, S., Georgel, P., Steward, R., Reichhart, J.M. & Hoffmann, J.A. (1995) Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J 14, 536-545.
36. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. & Hoffmann, J. (1996) The dorsoventral regulatory gene cassette controls the potent antifungal response in Drosophila adults. Cell 86, 973-983.
37. Letsou, A., Alexander, S., Orth, K. & Wasserman, S.A. (1991) Genetic and molecular characterization of tube, a Drosophila gene maternally required for embryonic dorsoventral polarity. Proc Natl Acad Sci U S A 88, 810-814.
38. Lewohl, J.M., Wang, L., Miles, M.F., Zhang, L., Dodd, P.R. & Harris, R.A. (2000) Gene expression in human alcoholism: microarray analysis of frontal cortex. Alcohol Clin Exp Res 24, 1873-1882.
39. Li, R., Yu, C., Li, Y., Lam, T.-W., Yiu, S.-M., Kristiansen, K. & Wang, J. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967.
40. van der Linde, K. & Lyons, L.C. (2011) Circadian modulation of acute alcohol sensitivity but not acute tolerance in Drosophila. Chronobiol Int 28, 397-406.
41. Liu, J., Lewohl, J.M., Dodd, P.R., Randall, P.K., Harris, R.A. & Mayfield, R.D. (2004) Gene expression profiling of individual cases reveals consistent transcriptional changes in alcoholic human brain. J Neurochem 90, 1050-1058.
42. Liu, J., Lewohl, J.M., Harris, R.A., Dodd, P.R. & Mayfield, R.D. (2007) Altered gene expression profiles in the frontal cortex of cirrhotic alcoholics. Alcohol Clin Exp Res 31, 1460-1466.
43. Liu, J., Lewohl, J.M., Harris, R.A., Iyer, V.R., Dodd, P.R., Randall, P.K. & Mayfield, R.D. (2006) Patterns of gene expression in the frontal cortex discriminate alcoholic from nonalcoholic individuals. Neuropsychopharmacology 31, 1574-1582.
44. Luce-Fedrow, A., Von Ohlen, T., Boyle, D., Ganta, R.R. & Chapes, S.K. (2008) Use of Drosophila S2 cells as a model for studying Ehrlichia chaffeensis infections. Appl Environ Microbiol 74, 1886-1891.
45. Mansfield, B.E., Dionne, M.S., Schneider, D.S. & Freitag, N.E. (2003) Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell Microbiol 5, 901-911.
46. Marek, L.R. & Kagan, J.C. (2012) Phosphoinositide binding by the Toll adaptor dMyD88 controls antibacterial responses in Drosophila. Immunity 36, 612-622.
47. Mayfield, R.D., Lewohl, J.M., Dodd, P.R., Herlihy, A., Liu, J. & Harris, R.A. (2002) Patterns of gene expression are altered in the frontal and motor cortices of human alcoholics. J Neurochem 81, 802-813.
48. McGuire, S.E., Mao, Z. & Davis, R.L. (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE, 2004, pl6.
49. Meng, X., Khanuja, B.S. & Ip, Y.T. (1999) Toll receptor-mediated Drosophila immune response requires Dif, an NF-kappaB factor. Genes Dev 13, 792-797.
50. Milan, N.F., Kacsoh, B.Z. & Schlenke, T.A. (2012) Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Curr Biol 22, 488-493.
51. Moncrieffe, M.C., Grossmann, J.G. & Gay, N.J. (2008) Assembly of oligomeric death domain complexes during Toll receptor signaling. J Biol Chem 283, 33447-33454.
52. Morozova, T.V., Anholt, R.R.H. & Mackay, T.F.C. (2007) Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster. Genome Biol 8, R231.
53. Morozova, T.V., Huang, W., Pray, V.A., Whitham, T., Anholt, R.R.H. & Mackay, T.F.C. (2015) Polymorphisms in early neurodevelopmental genes affect natural variation in alcohol sensitivity in adult Drosophila. BMC Genomics 16, 865.
54. Morozova, T.V., Mackay, T.F.C. & Anholt, R.R.H. (2011) Transcriptional networks for alcohol sensitivity in Drosophila melanogaster. Genetics 187, 1193-1205.
55. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5, 621-628.
56. Osterwalder, T., Yoon, K.S., White, B.H. & Keshishian, H. (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 98, 12596-12601.
57. Paddibhatla, I., Lee, M.J., Kalamarz, M.E., Ferrarese, R. & Govind, S. (2010) Role for sumoylation in systemic inflammation and immune homeostasis in Drosophila larvae. PLoS Pathog 6, e1001234.
58. Petersen, U.M., Björklund, G., Ip, Y.T. & Engström, Y. (1995) The dorsal-related immunity factor, Dif, is a sequence-specific trans-activator of Drosophila cecropin gene expression. EMBO J 14, 3146-3158.
59. Ponomarev, I., Wang, S., Zhang, L., Harris, R.A. & Mayfield, R.D. (2012) Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J Neurosci 32, 1884-1897.
60. Robinson, G., Most, D., Ferguson, L.B., Mayfield, J., Harris, R.A. & Blednov, Y.A. (2014) Neuroimmune pathways in alcohol consumption: evidence from behavioral and genetic studies in rodents and humans. Int Rev Neurobiol 118, 13-39.
61. Roman, G., Endo, K., Zong, L. & Davis, R.L. (2001) P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci U S A 98, 12602-12607.
62. Roth, S., Hiromi, Y., Godt, D. & Nüsslein-Volhard, C. (1991) cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development 112, 371-388.
63. Rutschmann, S., Jung, A.C., Hetru, C., Reichhart, J.M., Hoffmann, J.A. & Ferrandon, D. (2000) The Rel protein DIF mediates the antifungal but not the antibacterial host defense in Drosophila. Immunity 12, 569-580.
64. Saldanha, A.J. (2004) Java Treeview - extensible visualization of microarray data. Bioinformatics 20, 3246-3248.
65. Schlenke, T.A., Morales, J., Govind, S. & Clark, A.G. (2007) Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog 3, 1486-1501.
66. Scholz, H., Franz, M. & Heberlein, U. (2005) The hangover gene defines a stress pathway required for ethanol tolerance development. Nature 436, 845-847.
67. Schuckit, M.A. (1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151, 184-189.
68. Schuckit, M.A. & Smith, T.L. (2011) Onset and course of alcoholism over 25 years in middle class men. Drug Alcohol Depend 113, 21-28.
69. Schuckit, M.A., Smith, T.L. & Kalmijn, J. (2004) The search for genes contributing to the low level of response to alcohol: patterns of findings across studies. Alcohol Clin Exp Res 28, 1449-1458.
70. Small, C., Paddibhatla, I., Rajwani, R. & Govind, S. (2012) An introduction to parasitic wasps of Drosophila and the antiparasite immune response. J Vis Exp, 63, e3347.
71. Sokolov, B.P., Jiang, L., Trivedi, N.S. & Aston, C. (2003) Transcription profiling reveals mitochondrial, ubiquitin and signaling systems abnormalities in postmortem brains from subjects with a history of alcohol abuse or dependence. J Neurosci Res 72, 756-767.
72. Song, X., Jin, P., Qin, S., Chen, L. & Ma, F. (2012) The evolution and origin of animal Toll-like receptor signaling pathway revealed by network-level molecular evolutionary analyses. PLoS One 7, e51657.
73. Sorrentino, R.P., Melk, J.P. & Govind, S. (2004) Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 166, 1343-1356.
74. Stöven, S., Ando, I., Kadalayil, L., Engström, Y. & Hultmark, D. (2000) Activation of the Drosophila NF-kappaB factor Relish by rapid endoproteolytic cleavage. EMBO Rep 1, 347-352.
75. Tanji, T., Hu, X., Weber, A.N.R. & Ip, Y.T. (2007) Toll and IMD pathways synergistically activate an innate immune response in Drosophila melanogaster. Mol Cell Biol 27, 4578-4588.
76. Tanji, T., Yun, E.-Y. & Ip, Y.T. (2010) Heterodimers of NF-kappaB transcription factors DIF and Relish regulate antimicrobial peptide genes in Drosophila. Proc Natl Acad Sci U S A 107, 14715-14720.
77. Tauszig-Delamasure, S., Bilak, H., Capovilla, M., Hoffmann, J.A. & Imler, J.-L. (2001) Drosophila MyD88 is required for the response to fungal and Gram-positive bacterial infections. Nat Immunol 3, 91-97.
78. Torroja, L., Chu, H., Kotovsky, I. & White, K. (1999) Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr Biol 9, 489-493.
79. Towb, P., Bergmann, A. & Wasserman, S.A. (2001) The protein kinase Pelle mediates feedback regulation in the Drosophila Toll signaling pathway. Development 128, 4729-4736.
80. Turvey, S.E. & Broide, D.H. (2010) Innate immunity. J Allergy Clin Immunol 125, S24-S32.
81. Weber, A.N.R., Tauszig-Delamasure, S., Hoffmann, J.A., Lelièvre, E., Gascan, H., Ray, K.P., Morse, M.A., Imler, J.-L. & Gay, N.J. (2003) Binding of the Drosophila cytokine Spätzle to Toll is direct and establishes signaling. Nat Immunol 4, 794-800.
82. Yagi, Y. & Ip, Y.T. (2005) Helicase89B is a Mot1p/BTAF1 homologue that mediates an antimicrobial response in Drosophila. EMBO Rep 6, 1088-1094.
83. Zhou, Z., Yuan, Q., Mash, D.C. & Goldman, D. (2011) Substance-specific and shared transcription and epigenetic changes in the human hippocampus chronically exposed to cocaine and alcohol. Proc Natl Acad Sci U S A 108, 6626-6631.
84. Zou, J.Y. & Crews, F.T. (2014) Release of neuronal HMGB1 by ethanol through decreased HDAC activity activates brain neuroimmune signaling. PLoS One 9, e87915.