Octopamine neuron dependent aggression requires dVGLUT from dual-transmitting neurons

Autoři: Lewis M. Sherer aff001;  Elizabeth Catudio Garrett aff001;  Hannah R. Morgan aff002;  Edmond D. Brewer aff002;  Lucy A. Sirrs aff002;  Harold K. Shearin aff003;  Jessica L. Williams aff003;  Brian D. McCabe aff004;  R. Steven Stowers aff003;  Sarah J. Certel aff001
Působiště autorů: Cellular, Molecular and Microbial Biology Graduate Program, University of Montana, Missoula, Montana, United States of America aff001;  Division of Biological Sciences, Center for Structural and Functional Neuroscience, University of Montana, Missoula, Montana, United States of America aff002;  Cell Biology and Neuroscience Department, Montana State University, Bozeman, Montana, United States of America aff003;  Brain Mind Institute, Swiss Federal Institute of Technology (EPFL), Lausanne, Switzerland aff004
Vyšlo v časopise: Octopamine neuron dependent aggression requires dVGLUT from dual-transmitting neurons. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008609
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008609


Neuromodulators such as monoamines are often expressed in neurons that also release at least one fast-acting neurotransmitter. The release of a combination of transmitters provides both “classical” and “modulatory” signals that could produce diverse and/or complementary effects in associated circuits. Here, we establish that the majority of Drosophila octopamine (OA) neurons are also glutamatergic and identify the individual contributions of each neurotransmitter on sex-specific behaviors. Males without OA display low levels of aggression and high levels of inter-male courtship. Males deficient for dVGLUT solely in OA-glutamate neurons (OGNs) also exhibit a reduction in aggression, but without a concurrent increase in inter-male courtship. Within OGNs, a portion of VMAT and dVGLUT puncta differ in localization suggesting spatial differences in OA signaling. Our findings establish a previously undetermined role for dVGLUT in OA neurons and suggests that glutamate uncouples aggression from OA-dependent courtship-related behavior. These results indicate that dual neurotransmission can increase the efficacy of individual neurotransmitters while maintaining unique functions within a multi-functional social behavior neuronal network.

Klíčová slova:

Aggression – Behavior – Drosophila melanogaster – Glutamate – Motor neurons – Neurons – Synaptic vesicles – Neurotransmitter receptor signaling


1. Dale H. Pharmacology and Nerve-endings (Walter Ernest Dixon Memorial Lecture): (Section of Therapeutics and Pharmacology). Proc R Soc Med. 1935;28(3):319–32. Epub 1935/01/01. 19990108; PubMed Central PMCID: PMC2205701.

2. Eccles JC, Fatt P, Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol. 1954;126(3):524–62. Epub 1954/12/10. doi: 10.1113/jphysiol.1954.sp005226 13222354; PubMed Central PMCID: PMC1365877.

3. Strata P, Harvey R. Dale's principle. Brain Res Bull. 1999;50(5–6):349–50. Epub 2000/01/22. doi: 10.1016/s0361-9230(99)00100-8 10643431.

4. Hnasko TS, Edwards RH. Neurotransmitter corelease: mechanism and physiological role. Annu Rev Physiol. 2012;74:225–43. Epub 2011/11/08. doi: 10.1146/annurev-physiol-020911-153315 22054239; PubMed Central PMCID: PMC4090038.

5. Nassel DR. Substrates for Neuronal Cotransmission With Neuropeptides and Small Molecule Neurotransmitters in Drosophila. Front Cell Neurosci. 2018;12:83. Epub 2018/04/14. doi: 10.3389/fncel.2018.00083 29651236; PubMed Central PMCID: PMC5885757.

6. Nusbaum MP, Blitz DM, Marder E. Functional consequences of neuropeptide and small-molecule co-transmission. Nat Rev Neurosci. 2017;18(7):389–403. Epub 2017/06/09. doi: 10.1038/nrn.2017.56 28592905; PubMed Central PMCID: PMC5547741.

7. Vaaga CE, Borisovska M, Westbrook GL. Dual-transmitter neurons: functional implications of co-release and co-transmission. Curr Opin Neurobiol. 2014;29:25–32. Epub 2014/05/13. doi: 10.1016/j.conb.2014.04.010 24816154; PubMed Central PMCID: PMC4231002.

8. El Mestikawy S, Wallen-Mackenzie A, Fortin GM, Descarries L, Trudeau LE. From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat Rev Neurosci. 2011;12(4):204–16. Epub 2011/03/19. doi: 10.1038/nrn2969 21415847.

9. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, et al. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci. 2002;22(13):5442–51. Epub 2002/07/05. doi: 10.1523/JNEUROSCI.22-13-05442.2002 12097496.

10. Ottersen OP, Storm-Mathisen J. Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol. 1984;229(3):374–92. Epub 1984/11/01. doi: 10.1002/cne.902290308 6150049.

11. Root DH, Zhang S, Barker DJ, Miranda-Barrientos J, Liu B, Wang HL, et al. Selective Brain Distribution and Distinctive Synaptic Architecture of Dual Glutamatergic-GABAergic Neurons. Cell Rep. 2018;23(12):3465–79. Epub 2018/06/21. doi: 10.1016/j.celrep.2018.05.063 29924991.

12. Aguilar JI, Dunn M, Mingote S, Karam CS, Farino ZJ, Sonders MS, et al. Neuronal Depolarization Drives Increased Dopamine Synaptic Vesicle Loading via VGLUT. Neuron. 2017;95(5):1074–88 e7. Epub 2017/08/22. doi: 10.1016/j.neuron.2017.07.038 28823729; PubMed Central PMCID: PMC5760215.

13. Lohr KM, Bernstein AI, Stout KA, Dunn AR, Lazo CR, Alter SP, et al. Increased vesicular monoamine transporter enhances dopamine release and opposes Parkinson disease-related neurodegeneration in vivo. Proc Natl Acad Sci U S A. 2014;111(27):9977–82. Epub 2014/07/01. doi: 10.1073/pnas.1402134111 24979780; PubMed Central PMCID: PMC4103325.

14. Trudeau LE, El Mestikawy S. Glutamate Cotransmission in Cholinergic, GABAergic and Monoamine Systems: Contrasts and Commonalities. Front Neural Circuits. 2018;12:113. Epub 2019/01/09. doi: 10.3389/fncir.2018.00113 30618649; PubMed Central PMCID: PMC6305298.

15. Silm K, Yang J, Marcott PF, Asensio CS, Eriksen J, Guthrie DA, et al. Synaptic Vesicle Recycling Pathway Determines Neurotransmitter Content and Release Properties. Neuron. 2019;102(4):786–800 e5. Epub 2019/04/21. doi: 10.1016/j.neuron.2019.03.031 31003725; PubMed Central PMCID: PMC6541489.

16. Zhang Q, Liu B, Wu Q, Liu B, Li Y, Sun S, et al. Differential Co-release of Two Neurotransmitters from a Vesicle Fusion Pore in Mammalian Adrenal Chromaffin Cells. Neuron. 2019;102(1):173–83 e4. Epub 2019/02/19. doi: 10.1016/j.neuron.2019.01.031 30773347.

17. Wrangham RW. Two types of aggression in human evolution. Proc Natl Acad Sci U S A. 2018;115(2):245–53. Epub 2017/12/28. doi: 10.1073/pnas.1713611115 29279379; PubMed Central PMCID: PMC5777045.

18. Thomas AL, Davis SM, Dierick HA. Of Fighting Flies, Mice, and Men: Are Some of the Molecular and Neuronal Mechanisms of Aggression Universal in the Animal Kingdom? PLoS Genet. 2015;11(8):e1005416. Epub 2015/08/28. doi: 10.1371/journal.pgen.1005416 26312756; PubMed Central PMCID: PMC4551476.

19. Craig IW, Halton KE. Genetics of human aggressive behaviour. Hum Genet. 2009;126(1):101–13. Epub 2009/06/10. doi: 10.1007/s00439-009-0695-9 19506905.

20. Hoopfer ED. Neural control of aggression in Drosophila. Curr Opin Neurobiol. 2016;38:109–18. Epub 2016/05/18. doi: 10.1016/j.conb.2016.04.007 27179788.

21. Kravitz EA, Fernandez Mde L. Aggression in Drosophila. Behav Neurosci. 2015;129(5):549–63. doi: 10.1037/bne0000089 26348714.

22. Nelson RJ, Trainor BC. Neural mechanisms of aggression. Nat Rev Neurosci. 2007;8(7):536–46. doi: 10.1038/nrn2174 17585306.

23. Rillich J, Rillich B, Stevenson PA. Differential modulation of courtship behavior and subsequent aggression by octopamine, dopamine and serotonin in male crickets. Horm Behav. 2019. Epub 2019/06/22. doi: 10.1016/j.yhbeh.2019.06.006 31226329.

24. Bruno V, Mancini D, Ghoche R, Arshinoff R, Miyasaki JM. High prevalence of physical and sexual aggression to caregivers in advanced Parkinson's disease. Experience in the Palliative Care Program. Parkinsonism Relat Disord. 2016;24:141–2. Epub 2016/01/21. doi: 10.1016/j.parkreldis.2016.01.010 26786755.

25. Liu CS, Ruthirakuhan M, Chau SA, Herrmann N, Carvalho AF, Lanctot KL. Pharmacological Management of Agitation and Aggression in Alzheimer's Disease: A Review of Current and Novel Treatments. Curr Alzheimer Res. 2016;13(10):1134–44. Epub 2016/05/04. doi: 10.2174/1567205013666160502122933 27137221.

26. Stigler KA, McDougle CJ. Pharmacotherapy of irritability in pervasive developmental disorders. Child Adolesc Psychiatr Clin N Am. 2008;17(4):739–52, vii-viii. Epub 2008/09/09. doi: 10.1016/j.chc.2008.06.002 18775367.

27. Kim S, Boylan K. Effectiveness of Antidepressant Medications for Symptoms of Irritability and Disruptive Behaviors in Children and Adolescents. J Child Adolesc Psychopharmacol. 2016;26(8):694–704. Epub 2016/08/03. doi: 10.1089/cap.2015.0127 27482998.

28. Moret C, Briley M. The importance of norepinephrine in depression. Neuropsychiatr Dis Treat. 2011;7(Suppl 1):9–13. Epub 2011/07/14. doi: 10.2147/NDT.S19619 21750623; PubMed Central PMCID: PMC3131098.

29. Sharma T, Guski LS, Freund N, Gotzsche PC. Suicidality and aggression during antidepressant treatment: systematic review and meta-analyses based on clinical study reports. BMJ. 2016;352:i65. Epub 2016/01/29. doi: 10.1136/bmj.i65 26819231; PubMed Central PMCID: PMC4729837.

30. Agnati LF, Guidolin D, Guescini M, Genedani S, Fuxe K. Understanding wiring and volume transmission. Brain Res Rev. 2010;64(1):137–59. Epub 2010/03/30. doi: 10.1016/j.brainresrev.2010.03.003 20347870.

31. Beaudet A, Descarries L. The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience. 1978;3(10):851–60. Epub 1978/01/01. doi: 10.1016/0306-4522(78)90115-x 215936.

32. Descarries L, Berube-Carriere N, Riad M, Bo GD, Mendez JA, Trudeau LE. Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res Rev. 2008;58(2):290–302. Epub 2007/11/29. doi: 10.1016/j.brainresrev.2007.10.005 18042492.

33. Descarries L, Watkins KC, Lapierre Y. Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Res. 1977;133(2):197–222. Epub 1977/09/16. doi: 10.1016/0006-8993(77)90759-4 902092.

34. De-Miguel FF, Trueta C. Synaptic and extrasynaptic secretion of serotonin. Cell Mol Neurobiol. 2005;25(2):297–312. doi: 10.1007/s10571-005-3061-z 16047543.

35. Fuxe K, Agnati LF, Marcoli M, Borroto-Escuela DO. Volume Transmission in Central Dopamine and Noradrenaline Neurons and Its Astroglial Targets. Neurochem Res. 2015;40(12):2600–14. Epub 2015/04/22. doi: 10.1007/s11064-015-1574-5 25894681.

36. Marder E, Thirumalai V. Cellular, synaptic and network effects of neuromodulation. Neural Netw. 2002;15(4–6):479–93. doi: 10.1016/s0893-6080(02)00043-6 12371506.

37. Takahashi A, Quadros IM, de Almeida RM, Miczek KA. Behavioral and pharmacogenetics of aggressive behavior. Curr Top Behav Neurosci. 2012;12:73–138. doi: 10.1007/7854_2011_191 22297576; PubMed Central PMCID: PMC3864145.

38. Moutsimilli L, Farley S, El Khoury MA, Chamot C, Sibarita JB, Racine V, et al. Antipsychotics increase vesicular glutamate transporter 2 (VGLUT2) expression in thalamolimbic pathways. Neuropharmacology. 2008;54(3):497–508. Epub 2007/12/25. doi: 10.1016/j.neuropharm.2007.10.022 18155072.

39. Uezato A, Meador-Woodruff JH, McCullumsmith RE. Vesicular glutamate transporter mRNA expression in the medial temporal lobe in major depressive disorder, bipolar disorder, and schizophrenia. Bipolar Disord. 2009;11(7):711–25. Epub 2009/10/21. doi: 10.1111/j.1399-5618.2009.00752.x 19839996.

40. Tordera RM, Pei Q, Sharp T. Evidence for increased expression of the vesicular glutamate transporter, VGLUT1, by a course of antidepressant treatment. J Neurochem. 2005;94(4):875–83. Epub 2005/07/05. doi: 10.1111/j.1471-4159.2005.03192.x 15992385.

41. Shan D, Lucas EK, Drummond JB, Haroutunian V, Meador-Woodruff JH, McCullumsmith RE. Abnormal expression of glutamate transporters in temporal lobe areas in elderly patients with schizophrenia. Schizophr Res. 2013;144(1–3):1–8. Epub 2013/01/30. doi: 10.1016/j.schres.2012.12.019 23356950; PubMed Central PMCID: PMC3572263.

42. Mingote S, Chuhma N, Kalmbach A, Thomsen GM, Wang Y, Mihali A, et al. Dopamine neuron dependent behaviors mediated by glutamate cotransmission. Elife. 2017;6. Epub 2017/07/14. doi: 10.7554/eLife.27566 28703706; PubMed Central PMCID: PMC5599237.

43. Andrews JC, Fernandez MP, Yu Q, Leary GP, Leung AK, Kavanaugh MP, et al. Octopamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males. PLoS Genet. 2014;10(5):e1004356. Epub 2014/05/24. doi: 10.1371/journal.pgen.1004356 24852170; PubMed Central PMCID: PMC4031044.

44. Baier A, Wittek B, Brembs B. Drosophila as a new model organism for the neurobiology of aggression? J Exp Biol. 2002;205(Pt 9):1233–40. 11948200.

45. Certel SJ, Savella MG, Schlegel DC, Kravitz EA. Modulation of Drosophila male behavioral choice. Proc Natl Acad Sci U S A. 2007;104(11):4706–11. doi: 10.1073/pnas.0700328104 17360588.

46. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL, et al. Octopamine in male aggression of Drosophila. Curr Biol. 2008;18(3):159–67. doi: 10.1016/j.cub.2007.12.052 18249112.

47. Zhou C, Rao Y, Rao Y. A subset of octopaminergic neurons are important for Drosophila aggression. Nat Neurosci. 2008;11(9):1059–67. doi: 10.1038/nn.2164 19160504.

48. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, et al. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci. 1998;18(23):9733–50. Epub 1998/11/21. doi: 10.1523/JNEUROSCI.18-23-09733.1998 9822734.

49. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, et al. Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron. 2010;65(5):643–56. Epub 2010/03/13. doi: 10.1016/j.neuron.2010.02.012 20223200; PubMed Central PMCID: PMC2846457.

50. Jonas P, Bischofberger J, Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse. Science. 1998;281(5375):419–24. Epub 1998/07/17. doi: 10.1126/science.281.5375.419 9665886.

51. Ren J, Qin C, Hu F, Tan J, Qiu L, Zhao S, et al. Habenula "cholinergic" neurons co-release glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron. 2011;69(3):445–52. Epub 2011/02/15. doi: 10.1016/j.neuron.2010.12.038 21315256.

52. Tritsch NX, Ding JB, Sabatini BL. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature. 2012;490(7419):262–6. Epub 2012/10/05. doi: 10.1038/nature11466 23034651; PubMed Central PMCID: PMC3944587.

53. Rodriguez-Valentin R, Lopez-Gonzalez I, Jorquera R, Labarca P, Zurita M, Reynaud E. Oviduct contraction in Drosophila is modulated by a neural network that is both, octopaminergic and glutamatergic. J Cell Physiol. 2006;209(1):183–98. doi: 10.1002/jcp.20722 16826564.

54. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci. 2010;30(24):8229–33. Epub 2010/06/18. doi: 10.1523/JNEUROSCI.1754-10.2010 20554874; PubMed Central PMCID: PMC2918390.

55. Certel SJ, Leung A, Lin CY, Perez P, Chiang AS, Kravitz EA. Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLoS One. 2010;5(10):e13248. Epub 2010/10/23. doi: 10.1371/journal.pone.0013248 20967276; PubMed Central PMCID: PMC2953509.

56. Watanabe K, Chiu H, Pfeiffer BD, Wong AM, Hoopfer ED, Rubin GM, et al. A Circuit Node that Integrates Convergent Input from Neuromodulatory and Social Behavior-Promoting Neurons to Control Aggression in Drosophila. Neuron. 2017;95(5):1112–28 e7. Epub 2017/09/01. doi: 10.1016/j.neuron.2017.08.017 28858617; PubMed Central PMCID: PMC5588916.

57. Chen S, Lee AY, Bowens NM, Huber R, Kravitz EA. Fighting fruit flies: a model system for the study of aggression. Proc Natl Acad Sci U S A. 2002;99(8):5664–8. doi: 10.1073/pnas.082102599 11960020.

58. Dierick HA. A method for quantifying aggression in male Drosophila melanogaster. Nat Protoc. 2007;2(11):2712–8. doi: 10.1038/nprot.2007.404 18007606.

59. Baek M, Mann RS. Lineage and birth date specify motor neuron targeting and dendritic architecture in adult Drosophila. J Neurosci. 2009;29(21):6904–16. Epub 2009/05/29. doi: 10.1523/JNEUROSCI.1585-09.2009 19474317.

60. Nern A, Pfeiffer BD, Svoboda K, Rubin GM. Multiple new site-specific recombinases for use in manipulating animal genomes. Proc Natl Acad Sci U S A. 2011;108(34):14198–203. Epub 2011/08/13. doi: 10.1073/pnas.1111704108 21831835; PubMed Central PMCID: PMC3161616.

61. Jensen AA, Fahlke C, Bjorn-Yoshimoto WE, Bunch L. Excitatory amino acid transporters: recent insights into molecular mechanisms, novel modes of modulation and new therapeutic possibilities. Curr Opin Pharmacol. 2015;20:116–23. Epub 2014/12/04. doi: 10.1016/j.coph.2014.10.008 25466154.

62. Martin CA, Krantz DE. Drosophila melanogaster as a genetic model system to study neurotransmitter transporters. Neurochem Int. 2014;73:71–88. Epub 2014/04/08. doi: 10.1016/j.neuint.2014.03.015 24704795; PubMed Central PMCID: PMC4264877.

63. Seal RP, Daniels GM, Wolfgang WJ, Forte MA, Amara SG. Identification and characterization of a cDNA encoding a neuronal glutamate transporter from Drosophila melanogaster. Receptors Channels. 1998;6(1):51–64. Epub 1998/07/17. 9664622.

64. Soustelle L, Besson MT, Rival T, Birman S. Terminal glial differentiation involves regulated expression of the excitatory amino acid transporters in the Drosophila embryonic CNS. Dev Biol. 2002;248(2):294–306. Epub 2002/08/09. doi: 10.1006/dbio.2002.0742 12167405.

65. Stacey SM, Muraro NI, Peco E, Labbe A, Thomas GB, Baines RA, et al. Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated notch signaling and is essential for larval locomotion. J Neurosci. 2010;30(43):14446–57. Epub 2010/10/29. doi: 10.1523/JNEUROSCI.1021-10.2010 20980602.

66. Matsuno M, Horiuchi J, Ofusa K, Masuda T, Saitoe M. Inhibiting Glutamate Activity during Consolidation Suppresses Age-Related Long-Term Memory Impairment in Drosophila. iScience. 2019;15:55–65. Epub 2019/04/29. doi: 10.1016/j.isci.2019.04.014 31030182; PubMed Central PMCID: PMC6487374.

67. Monastirioti M, Linn CE Jr., White K. Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci. 1996;16(12):3900–11. doi: 10.1523/JNEUROSCI.16-12-03900.1996 8656284.

68. Tison KV, McKinney HM, Stowers RS. Demonstration of a Simple Epitope Tag Multimerization Strategy for Enhancing the Sensitivity of Protein Detection Using Drosophila vAChT. G3 (Bethesda). 2019. Epub 2019/11/27. doi: 10.1534/g3.119.400750 31767639.

69. Atwood HL, Govind CK, Wu CF. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol. 1993;24(8):1008–24. Epub 1993/08/01. doi: 10.1002/neu.480240803 8409966.

70. Grygoruk A, Chen A, Martin CA, Lawal HO, Fei H, Gutierrez G, et al. The redistribution of Drosophila vesicular monoamine transporter mutants from synaptic vesicles to large dense-core vesicles impairs amine-dependent behaviors. J Neurosci. 2014;34(20):6924–37. Epub 2014/05/16. doi: 10.1523/JNEUROSCI.0694-14.2014 24828646; PubMed Central PMCID: PMC4019805.

71. Sujkowski A, Ramesh D, Brockmann A, Wessells R. Octopamine Drives Endurance Exercise Adaptations in Drosophila. Cell Rep. 2017;21(7):1809–23. Epub 2017/11/16. doi: 10.1016/j.celrep.2017.10.065 29141215; PubMed Central PMCID: PMC5693351.

72. Brewer JC, Olson AC, Collins KM, Koelle MR. Serotonin and neuropeptides are both released by the HSN command neuron to initiate Caenorhabditis elegans egg laying. PLoS Genet. 2019;15(1):e1007896. Epub 2019/01/25. doi: 10.1371/journal.pgen.1007896 30677018; PubMed Central PMCID: PMC6363226.

73. Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O, et al. VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci. 2010;30(6):2198–210. Epub 2010/02/12. doi: 10.1523/JNEUROSCI.5196-09.2010 20147547.

74. Ciranna L. Serotonin as a modulator of glutamate- and GABA-mediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol. 2006;4(2):101–14. Epub 2008/07/11. doi: 10.2174/157015906776359540 18615128; PubMed Central PMCID: PMC2430669.

75. Pittaluga A. Presynaptic Release-Regulating mGlu1 Receptors in Central Nervous System. Front Pharmacol. 2016;7:295. Epub 2016/09/16. doi: 10.3389/fphar.2016.00295 27630571; PubMed Central PMCID: PMC5006178.

76. Birgner C, Nordenankar K, Lundblad M, Mendez JA, Smith C, le Greves M, et al. VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation. Proc Natl Acad Sci U S A. 2010;107(1):389–94. Epub 2009/12/19. doi: 10.1073/pnas.0910986107 20018672; PubMed Central PMCID: PMC2806710.

77. Fortin GM, Ducrot C, Giguere N, Kouwenhoven WM, Bourque MJ, Pacelli C, et al. Segregation of dopamine and glutamate release sites in dopamine neuron axons: regulation by striatal target cells. FASEB J. 2019;33(1):400–17. Epub 2018/07/17. doi: 10.1096/fj.201800713RR 30011230.

78. Zhang S, Qi J, Li X, Wang HL, Britt JP, Hoffman AF, et al. Dopaminergic and glutamatergic microdomains in a subset of rodent mesoaccumbens axons. Nat Neurosci. 2015;18(3):386–92. Epub 2015/02/11. doi: 10.1038/nn.3945 25664911; PubMed Central PMCID: PMC4340758.

79. Koganezawa M, Kimura K, Yamamoto D. The Neural Circuitry that Functions as a Switch for Courtship versus Aggression in Drosophila Males. Curr Biol. 2016;26(11):1395–403. Epub 2016/05/18. doi: 10.1016/j.cub.2016.04.017 27185554.

80. Crocker A, Sehgal A. Octopamine regulates sleep in Drosophila through protein kinase A-dependent mechanisms. J Neurosci. 2008;28(38):9377–85. doi: 10.1523/JNEUROSCI.3072-08a.2008 18799671.

81. Scheiner R, Steinbach A, Classen G, Strudthoff N, Scholz H. Octopamine indirectly affects proboscis extension response habituation in Drosophila melanogaster by controlling sucrose responsiveness. J Insect Physiol. 2014;69:107–17. Epub 2014/05/14. doi: 10.1016/j.jinsphys.2014.03.011 24819202.

82. Stevenson PA, Dyakonova V, Rillich J, Schildberger K. Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci. 2005;25(6):1431–41. doi: 10.1523/JNEUROSCI.4258-04.2005 15703397.

83. Youn H, Kirkhart C, Chia J, Scott K. A subset of octopaminergic neurons that promotes feeding initiation in Drosophila melanogaster. PLoS One. 2018;13(6):e0198362. Epub 2018/06/28. doi: 10.1371/journal.pone.0198362 29949586; PubMed Central PMCID: PMC6021039.

84. Classen G, Scholz H. Octopamine Shifts the Behavioral Response From Indecision to Approach or Aversion in Drosophila melanogaster. Front Behav Neurosci. 2018;12:131. Epub 2018/07/19. doi: 10.3389/fnbeh.2018.00131 30018540; PubMed Central PMCID: PMC6037846.

85. Mingote S, Amsellem A, Kempf A, Rayport S, Chuhma N. Dopamine-glutamate neuron projections to the nucleus accumbens medial shell and behavioral switching. Neurochem Int. 2019;129:104482. Epub 2019/06/07. doi: 10.1016/j.neuint.2019.104482 31170424.

86. Manchia M, Carpiniello B, Valtorta F, Comai S. Serotonin Dysfunction, Aggressive Behavior, and Mental Illness: Exploring the Link Using a Dimensional Approach. ACS Chem Neurosci. 2017;8(5):961–72. Epub 2017/04/06. doi: 10.1021/acschemneuro.6b00427 28378993.

87. Vermeiren Y, Van Dam D, Aerts T, Engelborghs S, De Deyn PP. Monoaminergic neurotransmitter alterations in postmortem brain regions of depressed and aggressive patients with Alzheimer's disease. Neurobiol Aging. 2014;35(12):2691–700. Epub 2014/07/07. doi: 10.1016/j.neurobiolaging.2014.05.031 24997673.

88. Certel SJ, Kravitz EA. Scoring and analyzing aggression in Drosophila. Cold Spring Harb Protoc. 2012;2012(3):319–25. Epub 2012/03/03. doi: 10.1101/pdb.prot068130 22383642.

89. Koon AC, Ashley J, Barria R, DasGupta S, Brain R, Waddell S, et al. Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat Neurosci. 2011;14(2):190–9. Epub 2010/12/28. nn.2716 [pii] doi: 10.1038/nn.2716 21186359.

90. Petersen LK, Stowers RS. A Gateway MultiSite recombination cloning toolkit. PLoS One. 2011;6(9):e24531. Epub 2011/09/21. doi: 10.1371/journal.pone.0024531 21931740; PubMed Central PMCID: PMC3170369.

91. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A. 2008;105(28):9715–20. doi: 10.1073/pnas.0803697105 18621688.

92. Williams JL, Shearin HK, Stowers RS. Conditional Synaptic Vesicle Markers for Drosophila. G3 (Bethesda). 2019. Epub 2019/01/13. doi: 10.1534/g3.118.200975 30635441.

93. Shearin HK, Dvarishkis AR, Kozeluh CD, Stowers RS. Expansion of the gateway multisite recombination cloning toolkit. PLoS One. 2013;8(10):e77724. Epub 2013/11/10. doi: 10.1371/journal.pone.0077724 24204935; PubMed Central PMCID: PMC3799639.

94. Pfeiffer BD, Truman JW, Rubin GM. Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci U S A. 2012;109(17):6626–31. Epub 2012/04/12. doi: 10.1073/pnas.1204520109 22493255; PubMed Central PMCID: PMC3340069.

95. Wang JW, Beck ES, McCabe BD. A modular toolset for recombination transgenesis and neurogenetic analysis of Drosophila. PLoS One. 2012;7(7):e42102. Epub 2012/08/01. doi: 10.1371/journal.pone.0042102 22848718; PubMed Central PMCID: PMC3405054.

96. Port F, Chen HM, Lee T, Bullock SL. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc Natl Acad Sci U S A. 2014;111(29):E2967–76. Epub 2014/07/09. doi: 10.1073/pnas.1405500111 25002478; PubMed Central PMCID: PMC4115528.

97. Daniels RW, Collins CA, Chen K, Gelfand MV, Featherstone DE, DiAntonio A. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron. 2006;49(1):11–6. Epub 2006/01/03. doi: 10.1016/j.neuron.2005.11.032 16387635; PubMed Central PMCID: PMC2248602.

98. Ren X, Sun J, Housden BE, Hu Y, Roesel C, Lin S, et al. Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9. Proc Natl Acad Sci U S A. 2013;110(47):19012–7. Epub 2013/11/06. doi: 10.1073/pnas.1318481110 24191015; PubMed Central PMCID: PMC3839733.

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Svět praktické medicíny 1/2024 (znalostní test z časopisu)

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se