Mutations in many genes affect aggressive behavior in Drosophila melanogaster

BMC Biology

Volumn 7, Issue , 2009, Pages

  Edwards, Alexis C ^a,c   Zwarts, Liesbeth ^b   Yamamoto, Akihiko ^a   Callaerts, Patrick ^b   Mackay, Trudy F C ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BINDING PROTEIN; CASEIN KINASE IALPHA; GENE PRODUCT; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LAMININ; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; SPINOPHILIN; SYNTAXIN 4;

AGGRESSION; ALLELE; ARTICLE; CELL ACTIVITY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; GENE FUNCTION; GENE MUTATION; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC TRAIT; MORPHOLOGY; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM FUNCTION; NONHUMAN; PLEIOTROPY; PREDICTION; REVERTANT; SPECIES DIFFERENCE; ANIMAL; ANIMAL BEHAVIOR; GENE; GENE EXPRESSION REGULATION; GENETICS; TRANSPOSON;

ANIMALIA; BASIDIOMYCOTA; DROSOPHILA MELANOGASTER;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA MELANOGASTER; GENES, INSECT; MUTAGENESIS, INSERTIONAL;

EID: 67650766675     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-7-29     Document Type: Article

References (73)

1. Brunner HG Nelen MR van Zandvoort P Abeling NG van Gennip AH Wolters EC Kuniper MA Ropers HH van Oost BA X-linked borderline mental retardation with prominent behavioral disturbance: Phenotype, genetic localization, and evidence for disturbed monoamine metabolism Am J Hum Genet 1993, 52:1032-1039. 1682278 8503438
2. Haller J Makara GB Kruk MR Catecholaminergic involvement in the control of aggression: Hormones, the peripheral sympathetic, and central noradrenergic systems Neurosci Biobehav Rev 1998, 22:85-97. 10.1016/ S0149-7634(97)00023-7 9491941
3. Manuck SB Flory JD Ferrell RE Dent KM Mann JJ Muldoon MF Aggression and anger-related traits associated with a polymorphism of the tryptophan hydroxylase gene Biol Psychiatry 1999, 45:603-614. 10.1016/ S0006-3223(98)00375-8 10088047
4. Nelson RJ Chiavegatto S Molecular basis of aggression Trends Neurosci 2001, 24:713-719. 10.1016/S0166-2236(00)01996-2 11718876
5. Han DH Park DB Na C Kee BS Lee YS Association of aggressive behavior in Korean male schizophrenic patients with polymorphisms in the serotonin transporter promoter and catecholamine-O-methyltransferase genes Psychiatr Res 2004, 129:29-37. 10.1016/j.psychres.2004.06.013
6. de Almeida RM Ferrari PF Parmigiani S Miczek KA Escalated aggressive behavior: Dopamine, serotonin and GABA Eur J Pharmacol 526:51-64. 10.1016/j.ejphar.2005.10.004 16325649
7. Alia-Klein N Goldstein RZ Kriplani A Logan J Tomasi D Williams B Telang F Shumay E Biegon A Craig IW Henn F Wang GJ Volkow ND Fowler JS Brain monoamine oxidase A activity predicts trait aggression J Neurosci 2008, 28:5099-5104. 2430409 18463263 10.1523/JNEUROSCI.0925-08.2008
8. Jacobs ME Influence of beta-alanine on mating and territorialism in Drosophila melanogaster Behavior Genetics 1978, 8:487-502. 10.1007/ BF01067478 103533
9. Edwards DH Kravitz EA Serotonin, social status, and aggression Curr Opin Neurobiol 1997, 7:812-819. 10.1016/S0959-4388(97)80140-7 9464985
10. Huber R Smith K Delago A Isaksson K Kravitz EA Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat Proc Nat Acad Sci 1997, 94:5939-5942. 20885 9159179 10.1073/pnas.94.11.5939
11. Baier A Wittek B Brembs B Drosophila as a new model organism for the neurobiology of aggression? J Exp Biol 2002, 205:1233-1240. 11948200
12. Certel SJ Savella MG Schlegel DC Kravitz EA Modulation of Drosophila male behavioral choice Proc Nat Acad Sci 2007, 104:4706-4711. 1810337 17360588 10.1073/pnas.0700328104
13. Dierick HA Greenspan RJ Serotonin and neuropeptide F have opposite modulatory effects on fly aggression Nat Genet 2007, 39:678-682. 10.1038/ ng2029 17450142
14. Hoyer SC Eckart A Herrel A Zars T Fischer SA Hardie SL Heisenberg M Octopamine in male aggression of Drosophila Curr Biol 2008, 18:159-167. 10.1016/j.cub.2007.12.052 18249112
15. Miczek KA Fish EW De Bold JF Neurosteroids, GABAA receptors, and escalated aggressive behavior Horm Behav 2003, 44:242-257. 10.1016/ j.yhbeh.2003.04.002 14609546
16. Nelson RJ Demas GE Huang PL Fishman MC Dawson VL Dawson TM Snyder SH Behavioral abnormalities in male mice lacking neuronal nitric oxide synthase Nature 1995, 378:383-386. 10.1038/378383a0 7477374
17. Rujescu D Giegling I Mandelli L Schneider B Hartmann AM Schnabel A Maurer K Moller HJ Serretti A NOS-I and -III gene variants are differentially associated with facets of suicidal behavior and aggression-related traits Am J Med Genet B Neuropsychiatr Genet 2008, 147B:42-48. 10.1002/ajmg.b.30569 17579350
18. Gammie SC Auger AP Jessen HM Vanzo RJ Awad TA Stevenson SA Altered gene expression in mice selected for high maternal aggression Genes Brain Behav 2007, 6:432-443. 1994650 16939635 10.1111/j.1601-183X.2006.00271.x
19. Karl T Herzog H Behavioral profiling of NPY in aggression and neuropsychiatric diseases Peptides 2007, 28:326-333. 10.1016/ j.peptides.2006.07.027 17196302
20. Karl T Lin S Schwarzer C Sainsbury A Couzens M Wittmann W Boey D von Horsten S Herzog H Y1 receptors regulate aggressive behavior by modulating serotonin pathways Proc Nat Acad Sci 2004, 101:12742-12747. 515123 15314215 10.1073/pnas.0404085101
21. Chan YB Kravitz EA Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster Proc Nat Acad Sci 2007, 104:19577-19582. 2148331 18042702 10.1073/pnas.0709803104
22. Lee G Hall JC A newly uncovered phenotype associated with the fruitless gene of Drosophila melanogaster: Aggression-like head interactions between mutant males Behav Genet 2000, 30:263-275. 10.1023/ A:1026541215546 11206081
23. Vrontou E Nilsen SP Demir E Kravitz EA Dickson BJ Fruitless regulates aggression and dominance in Drosophila Nat Neurosci 2006, 9:1469-1471. 10.1038/nn1809 17115036
24. Hoffmann AA Heritable variation for territorial success in two Drosophila melanogaster populations Anim Behav 1988, 36:1180-1189. 10.1016/S0003-3472(88)80077-0
25. Hoffmann AA Geographic variation in the territorial success of Drosophila melanogaster males Behav Genet 1989, 19:241-255. 10.1007/ BF01065908 2497722
26. Dierick HA Greenspan RJ Molecular analysis of flies selected for aggressive behavior Nat Genet 2006, 38:1023-1031. 10.1038/ng1864 16906161
27. Edwards AC Rollmann SM Morgan TJ Mackay TF Quantitative genomics of aggressive behavior in Drosophila melanogaster PLoS Genet 2006, 2:e154. 1564424 17044737 10.1371/journal.pgen.0020154
28. Rollmann S Zwarts L Edwards A Yamamoto A Callaerts P Norga K Mackay TF Anholt R Pleiotropic effects of Drosophila neuralized on complex behaviors and brain structure Genetics 2008, 179:1327-1336. 2475736 18562639 10.1534/genetics.108.088435
29. Edwards AC Mackay TF Quantitative trait loci for aggressive behavior in Drosophila melanogaster Genetics
30. Norga KK Gurganus MC Dilda CL Yamamoto A Lyman RF Patel PH Rubin GM Hoskins RA Mackay TF Bellen HJ Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development Curr Biol 2003, 13:1388-1396. 10.1016/S0960-9822(03)00546-3 12932322
31. Harbison ST Yamamoto AH Fanara JJ Norga KK Mackay TF Quantitative trait loci affecting starvation resistance in Drosophila melanogaster Genetics 2004, 166:1807-1823. 1470806 15126400 10.1534/genetics.166.4.1807
32. Harbison ST Sehgal A Quantitative genetic analysis of sleep in Drosophila melanogaster Genetics 2008, 178:2341-2360. 2323820 18430954 10.1534/genetics.107.081232
33. Sambandan D Yamamoto A Fanara JJ Mackay TF Anholt RR Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster Genetics 2006, 174:1349-1363. 1667092 17028343 10.1534/ genetics.106.060574
34. Yamamoto A Zwarts L Callaerts P Norga K Mackay TF Anholt RR Neurogenetic networks for startle-induced locomotion in Drosophila melanogaster Proc Nat Acad Sci 2008, 105:12393-12398. 2527922 18713854 10.1073/ pnas.0804889105
35. Bellen HJ Levis RW Liao G He Y Carlson JW Tsang G Evans-Holm M Hiesinger PR Schulze KL Rubin GM Hoskins RA Spradling AC The BDGP gene disruption project: Single transposon insertions associated with 40% of Drosophila genes Genetics 2004, 167:761-781. 1470905 15238527 10.1534/ genetics.104.026427
36. Dennis G Jr Sherman BT Hosack DA Yang J Gao W Lane HC Lempicki RA DAVID: database for annotation, visualization, and integrated discovery Genome Biol 2003, 4:P3. 10.1186/gb-2003-4-5-p3 12734009
37. Al-Shahrour F Minguez P Tarraga J Montaner D Alloza E Vaquerizas JM Conde L Blaschke C Vera J Dopazo J BABELOMICS: A systems biology perspective in the functional annotation of genome-scale experiments Nucleic Acids Res 2006, 34:W472-476. 1538844 16845052 10.1093/nar/gkl172
38. Chintapalli VR Wang J Dow JA Using FlyAtlas to identify better Drosophila melanogaster models of human disease Nat Genet 2007, 39:715-720. 10.1038/ng2049 17534367
39. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 2001, 25:402-408. 10.1006/meth.2001.1262 11846609
40. Tautz D Pfeifle C A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback Chromosoma 1989, 98:81-85. 10.1007/BF00291041 2476281
41. Anholt RR Lyman RF Mackay TF Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster Genetics 1996, 143:293-301. 1207262 8722782
42. Lyman RF Lawrence F Nuzhdin SV Mackay TF Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster Genetics 1996, 143:277-292. 1207261 8722781
43. Mackay TF Heinsohn SL Lyman RF Moehring AJ Morgan TJ Rollmann SM Genetics and genomics of Drosophila mating behavior Proc Nat Acad Sci 2005, 102(Suppl 1):6622-6629. 1131870 15851659 10.1073/pnas.0501986102
44. Morozova TV Anholt RR Mackay TF Transcriptional response to alcohol exposure in Drosophila melanogaster Genome Biol 2006, 7:R95. 1794562 17054780 10.1186/gb-2006-7-10-r95
45. Morozova TV Anholt RR Mackay TF Phenotypic and transcriptional response to selection for alcohol sensitivity in Drosophila melanogaster Genome Biol 2007, 8:R231. 2246305 17973985 10.1186/gb-2007-8-10-r231
46. Jordan KW Carbone MA Yamamoto A Morgan TJ Mackay TF Quantitative genomics of locomotor behavior in Drosophila melanogaster Genome Biol 2007, 8:R172. 2375002 17708775 10.1186/gb-2007-8-8-r172
47. Toma DP White KP Hirsch J Greenspan RJ Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait Nat Genet 2002, 31:349-353. 12042820
48. Cirelli C LaVaute TM Tononi G Sleep and wakefulness modulate gene expression in Drosophila J Neurochem 2005, 94:1411-1419. 10.1111/ j.1471-4159.2005.03291.x 16001966
49. Burn TC Vigoreaux JO Tobin SL Alternative 5C actin transcripts are localized in different patterns during Drosophila embryogenesis Dev Biol 1989, 131:345-355. 10.1016/S0012-1606(89)80008-9 2492241
50. Tobin SL Cook PJ Burn TC Transcripts of individual Drosophila actin genes are differentially distributed during embryogenesis Dev Genet 1990, 11:15-26. 10.1002/dvg.1020110104 1694472
51. Cubas P Modolell J Ruiz-Gomez M The helix-loop-helix extramacrochaetae protein is required for proper specification of many cell types in the Drosophila embryo Development 1994, 120:2555-2566. 7956831
52. Binari RC Staveley BE Johnson WA Godavarti R Sasisekharan R Manoukian AS Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling Development 1997, 124:2623-2632. 9217004
53. Haerry TE Heslip TR Marsh JL O'Connor MB Defects in glucuronate biosynthesis disrupt wingless signaling in Drosophila Development 1997, 124:3055-3064. 9272947
54. Wilson RJ Goodman JL Strelets VB FlyBase: Integration and improvements to query tools Nucleic Acids Res 2008, 36:D588-593. 2238994 18160408 10.1093/nar/gkm930
55. Stroschein-Stevenson SL Foley E O'Farrell PH Johnson AD Identification of Drosophila gene products required for phagocytosis of Candida albicans PLoS Biol 2006, 4:e4. 1310651 16336044 10.1371/ journal.pbio.0040004
56. Echard A Hickson GR Foley E O'Farrell PH Terminal cytokinesis events uncovered after an RNAi screen Curr Biol 2004, 14:1685-1693.26. 10.1016/ j.cub.2004.08.063 15380073
57. Eggert US Kiger AA Richter C Perlman ZE Perrimon N Mitchison TJ Field CM Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets PLoS Biol 2004, 2:e379. 528723 15547975 10.1371/journal.pbio.0020379
58. Noguchi T Miller KG A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster Development 2003, 130:1805-1816. 10.1242/dev.00406 12642486
59. Ahmed A Chandra S Magarinos M Vaessin H Echinoid mutants exhibit neurogenic phenotypes and show synergistic interactions with the Notch signaling pathway Development 2003, 130:6295-6304. 10.1242/dev.00796 14623819
60. Laplante C Nilson LA Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila Development 2006, 133:3255-3264. 10.1242/dev.02492 16854971
61. Bai J Chiu W Wang J Tzeng T Perrimon N Hsu J The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway Development 2001, 128:591-601. 11171342
62. Prokopenko SN He Y Lu Y Bellen HJ Mutations affecting the development of the peripheral nervous system in Drosophila: A molecular screen for novel proteins Genetics 2000, 156:1691-1715. 1461357 11102367
63. Saito M Awasaki T Hama C Genetic analyses of essential genes in cytological region 61D1-2 to 61F1-2 of Drosophila melanogaster Mol Genet Genomics 2002, 268:446-454. 10.1007/s00438-002-0770-6 12471442
64. Castrillon DH Gonczy P Alexander S Rawson R Eberhart CG Viswanathan S DiNardo S Wasserman SA Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: Characterization of male-sterile mutants generated by single P element mutagenesis Genetics 1993, 135:489-505.20. 1205651 8244010
65. Dubnau J Chiang AS Grady L Barditch J Gossweiler S McNeil J Smith P Buldoc F Scott R Certa U Broger C Tully T The staufen/pumilio pathway is involved in Drosophila long-term memory Curr Biol 2003, 13:286-296. 10.1016/S0960-9822(03)00064-2 12593794
66. Inaki M Kojima T Ueda R Saigo K Requirements of high levels of Hedgehog signaling activity for medial-region cell fate determination in Drosophila legs: Identification of pxb, a putative Hedgehog signaling attenuator gene repressed along the anterior-posterior compartment boundary Mech Dev 2002, 116:3-18. 10.1016/S0925-4773(02)00119-3 12128201
67. Nybakken K Perrimon N Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila Biochim Biophys Acta 2002, 1573:280-291. 12417410
68. Perrimon N Bernfield M Specificities of heparan sulphate proteoglycans in developmental processes Nature 2000, 404:725-728. 10.1038/35008000 10783877
69. Ghabrial A Luschnig S Metzstein MM Krasnow MA Branching morphogenesis of the Drosophila tracheal system Annu Rev Cell Dev Biol 2003, 19:623-647. 10.1146/annurev.cellbio.19.031403.160043 14570584
70. Littleton JT A genomic analysis of membrane trafficking and neurotransmitter release in Drosophila J Cell Biol 2000, 150:F77-82. 10.1083/jcb.150.2.F77 10908590
71. Rollmann SM Magwire MM Morgan TJ Ozsoy ED Yamamoto A Mackay TF Anholt RR Pleiotropic fitness effects of the Tre1-Gr5a region in Drosophila melanogaster Nat Genet 2006, 38:824-829. 10.1038/ng1823 16783380
72. Fedorowicz GM Fry JD Anholt RR Mackay TF Epistatic interactions between smell-impaired loci in Drosophila melanogaster Genetics 1998, 148:1885-1891. 1460070 9560402
73. Anholt RR Dilda CL Chang S Fanara JJ Kulkarni NH The genetic architecture of odor-guided behavior in Drosophila: Epistasis and the transcriptome Nat Genet 35:180-184. 10.1038/ng1240 12958599