Role of tyramine in calcium dynamics of GABAergic neurons and escape behavior in Caenorhabditis elegans

Zoological Letters - Tập 4 - Trang 1-14 - 2018
Yuko Kagawa-Nagamura1,2, Keiko Gengyo-Ando1,2,3, Masamichi Ohkura1,2, Junichi Nakai1,2,3
1Brain and Body System Science Institute, Saitama University, Saitama, Japan
2Graduate School of Science and Engineering, Saitama University, Saitama, Japan
3RIKEN Center for Brain Science, Saitama, Japan

Tóm tắt

Tyramine, known as a “trace amine” in mammals, modulates a wide range of behavior in invertebrates; however, the underlying cellular and circuit mechanisms are not well understood. In the nematode Caenorhabditis elegans (C. elegans), tyramine affects key behaviors, including foraging, feeding, and escape responses. The touch-evoked backward escape response is often coupled with a sharp omega turn that allows the animal to navigate away in the opposite direction. Previous studies have showed that a metabotropic tyramine receptor, SER-2, in GABAergic body motor neurons controls deep body bending in omega turns. In this study, we focused on the role of tyramine in GABAergic head motor neurons. Our goal is to understand the mechanism by which tyraminergic signaling alters neural circuit activity to control escape behavior. Using calcium imaging in freely moving C. elegans, we found that GABAergic RME motor neurons in the head had high calcium levels during forward locomotion but low calcium levels during spontaneous and evoked backward locomotion. This calcium decrease was also observed during the omega turn. Mutant analyses showed that tbh-1 mutants lacking only octopamine had normal calcium responses, whereas tdc-1 mutants lacking both tyramine and octopamine did not exhibit the calcium decrease in RME. This neuromodulation was mediated by SER-2. Moreover, tyraminergic RIM neuron activity was negatively correlated with RME activity in the directional switch from forward to backward locomotion. These results indicate that tyramine released from RIM inhibits RME via SER-2 signaling. The omega turn is initiated by a sharp head bend when the animal reinitiates forward movement. Interestingly, ser-2 mutants exhibited shallow head bends and often failed to execute deep-angle omega turns. The behavioral defect and the abnormal calcium response in ser-2 mutants could be rescued by SER-2 expression in RME. These results suggest that tyraminergic inhibition of RME is involved in the control of omega turns. We demonstrate that endogenous tyramine downregulates calcium levels in GABAergic RME motor neurons in the head via the tyramine receptor SER-2 during backward locomotion and omega turns. Our data suggest that this neuromodulation allows deep head bending during omega turns and plays a role in the escape behavior in C. elegans.

Tài liệu tham khảo

Harris-Warrick RM. Neuromodulation and flexibility in central pattern generator networks. Curr Opin Neurobiol. 2011;21:685–92. https://doi.org/10.1016/j.conb.2011.05.011.

Bargmann CI. Beyond the connectome: how neuromodulators shape neural circuits. BioEssays. 2012;34:458–65. https://doi.org/10.1002/bies.201100185.

Roeder T. Tyramine and Octopamine : ruling behavior and metabolism. Rev Lit Arts Am. 2005;50:447–77. https://doi.org/10.1146/annurev.ento.50.071803.130404.

Selcho M, Pauls D, el Jundi B, et al. The role of octopamine and tyramine in Drosophila larval locomotion. J Comp Neurol. 2012;520:3764–85. https://doi.org/10.1002/cne.23152.

Bacon JP, Thompson KS, Stern M. Identified octopaminergic neurons provide an arousal mechanism in the locust brain. J Neurophysiol. 1995;74:2739–43.

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

Suo S, Kimura Y, Van Tol HHM. Starvation induces cAMP response element-binding protein-dependent gene expression through octopamine-Gq signaling in Caenorhabditis elegans. J Neurosci. 2006;26:10082–90. https://doi.org/10.1523/JNEUROSCI.0819-06.2006.

Horvitz H, Chalfie M, Trent C, et al. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science (80- ). 1982;216:1012–4. https://doi.org/10.1126/science.6805073.

Hammer M, Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem. 1998;5:146–56. https://doi.org/10.1101/lm.5.1.146.

Jin X, Pokala N, Bargmann CI. Distinct circuits for the formation and retrieval of an imprinted olfactory memory. Cell. 2016;164:632–43. https://doi.org/10.1016/j.cell.2016.01.007.

Bendesky A, Tsunozaki M, Rockman MV, et al. Catecholamine receptor polymorphisms affect decision-making in C. Elegans. Nature. 2011;472:313–8. https://doi.org/10.1038/nature09821.

Adamo SA, Linn CE, Hoy RR (1995) The role of neurohormonal octopamine during “fight or flight” behaviour in the field cricket Gryllus bimaculatus. J Exp Biol 198:1691–1700. doi:10.1.1.300.1325

Burchett SA, Hicks TP. The mysterious trace amines: protean neuromodulators of synaptic transmission in mammalian brain. Prog Neurobiol. 2006;79:223–46. https://doi.org/10.1016/j.pneurobio.2006.07.003.

Borowsky B, Adham N, K a J, et al. Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci U S A. 2001;98:8966–71. https://doi.org/10.1073/pnas.151105198.

Pei Y, Asif-Malik A, Canales JJ. Trace amines and the trace amine-associated receptor 1: pharmacology, neurochemistry, and clinical implications. Front Neurosci. 2016;10:1–17. https://doi.org/10.3389/fnins.2016.00148.

Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR. Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron. 2005;46:247–60. https://doi.org/10.1016/j.neuron.2005.02.024.

Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983;100:64–119. https://doi.org/10.1016/0012-1606(83)90201-4.

White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc B Biol Sci. 1986;314:1–340. https://doi.org/10.1098/rstb.1986.0056.

Rex E, Molitor SC, Hapiak V, et al. Tyramine receptor (SER-2) isoforms are involved in the regulation of pharyngeal pumping and foraging behavior in Caenorhabditis elegans. J Neurochem. 2004;91:1104–15. https://doi.org/10.1111/j.1471-4159.2004.02787.x.

Donnelly JL, Clark CM, Leifer AM, et al. Monoaminergic orchestration of motor programs in a Complex C. Elegans behavior. PLoS Biol. 2013; https://doi.org/10.1371/journal.pbio.1001529.

Miyawaki A, Llopis J, Heim R, et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature. 1997;388:882–7. https://doi.org/10.1038/42264.

Nakai J, Ohkura M, Imoto K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat Biotechnol. 2001;19:137–41. https://doi.org/10.1038/84397.

Nagel G, Szellas T, Huhn W, et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A. 2003;100:13940–5. https://doi.org/10.1073/pnas.1936192100.

Kerr R, Lev-Ram V, Baird G, et al. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. Elegans. Neuron. 2000;26:583–94. https://doi.org/10.1016/S0896-6273(00)81196-4.

Kerr R. Imaging the activity of neurons and muscles. WormBook. 2006:1–13. https://doi.org/10.1895/wormbook.1.113.1.

Bargmann CI. Neurobiology of the Caenorhabditis elegans genome. Science (80- ). 1998;282:2028–33.

Gengyo-Ando K, Kagawa-Nagamura Y, Ohkura M, et al. A new platform for long-term tracking and recording of neural activity and simultaneous optogenetic control in freely behaving Caenorhabditis elegans. J Neurosci Methods. 2017;286:56–68. https://doi.org/10.1016/j.jneumeth.2017.05.017.

Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77:71–94. https://doi.org/10.1002/cbic.200300625.

Mello CC, Kramer JM, Stinchcomb D, Ambros V. Efficient gene transfer in C.Elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991;10:3959–70. https://doi.org/10.1016/0168-9525(92)90342-2.

Mitani S. Genetic regulation of mec-3 gene expression implicated in the specification of the mechanosensory neuron cell types in Caenorhabditis elegans. Develop Growth Differ. 1995;37:551–7. https://doi.org/10.1046/j.1440-169X.1995.t01-4-00010.x.

Ohkura M, Sasaki T, Sadakari J, et al. Genetically encoded green fluorescent Ca2+ indicators with improved detectability for neuronal Ca2+ signals. PLoS One. 2012;7:1–10. https://doi.org/10.1371/journal.pone.0051286.

Inoue M, Takeuchi A, Horigane S, et al. Rational design of a high-affinity, fast, red calcium indicator R-CaMP2. Nat Methods. 2015;12:64–70. https://doi.org/10.1038/nmeth.3185.

Fire A, Harrison SW, Dixon D. A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene. 1990;93:189–98. https://doi.org/10.1016/0378-1119(90)90224-F.

Gengyo-Ando K, Yoshina S, Inoue H, Mitani S. An efficient transgenic system by TA cloning vectors and RNAi for C. Elegans. Biochem Biophys Res Commun. 2006;349:1345–50. https://doi.org/10.1016/j.bbrc.2006.08.183.

Jin Y, Jorgensen E, Hartwieg E, Horvitz HR. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J Neurosci. 1999;19:539–48.

McIntire SL, Reimer RJ, Schuske K, et al. Identification and characterization of the vesicular GABA transporter. Nature. 1997;389:870–6. https://doi.org/10.1038/39908.

McMullan R, Hiley E, Morrison P, Nurrish SJ. Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. Elegans. Genes Dev. 2006;20:65–76. https://doi.org/10.1101/gad.359706.

Westmoreland JJ, McEwen J, B a M, et al. Conserved function of Caenorhabditis elegans UNC-30 and mouse Pitx2 in controlling GABAergic neuron differentiation. J Neurosci. 2001;21:6810–9. https://doi.org/10.1016/j.expneurol.2004.05.018.

Tsalik EL, Niacaris T, Wenick AS, et al. LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. Elegans nervous system. Dev Biol. 2003;263:81–102. https://doi.org/10.1016/S0012-1606(03)00447-0.

Gray JM, Hill JJ, Bargmann CI. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2005;102:3184–91. https://doi.org/10.1073/pnas.0409009101.

Kato S, Kaplan HS, Yemini E, et al. (2015) Global brain dynamics embed the motor command sequence of Caenorhabditis elegans article global brain dynamics embed the motor command sequence of Caenorhabditis elegans. 1–14. doi: https://doi.org/10.1016/j.cell.2015.09.034.

Venkatachalam V, Ji N, Wang X, et al. Pan-neuronal imaging in roaming Caenorhabditis elegans. Proc Natl Acad Sci. 2015;201507109 https://doi.org/10.1073/pnas.1507109113.

Guo ZV, Hart AC, Ramanathan S. Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods. 2009;6:891–6. https://doi.org/10.1038/nmeth.1397.

Weinshenker D, Garriga G, Thomas JH. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. Elegans. J Neurosci. 1995;15:6975–85.

Kawano T, Po MD, Gao S, et al. An imbalancing act: gap junctions reduce the backward motor circuit activity to bias C. Elegans for forward locomotion. Neuron. 2011;72:572–86. https://doi.org/10.1016/j.neuron.2011.09.005.

Piggott BJ, Liu J, Feng Z, et al. The neural circuits and synaptic mechanisms underlying motor initiation in C. Elegans. Cell. 2011;147:922–33. https://doi.org/10.1016/j.cell.2011.08.053.

Pirri JK, McPherson AD, Donnelly JL, et al. A tyramine-gated Chloride Channel coordinates distinct motor programs of a Caenorhabditis elegans escape response. Neuron. 2009;62:526–38. https://doi.org/10.1016/j.neuron.2009.04.013.

Rex E, Komuniecki RW. Characterization of a tyramine receptor from Caenorhabditis elegans. J Neurochem. 2002;82:1352–9. https://doi.org/10.1046/j.1471-4159.2002.01065.x.

Rex E, Hapiak V, Hobson R, et al. TYRA-2 (F01E11.5): a Caenorhabditis elegans tyramine receptor expressed in the MC and NSM pharyngeal neurons. J Neurochem. 2005;94:181–91. https://doi.org/10.1111/j.1471-4159.2005.03180.x.

Wragg RT, Hapiak V, Miller SB, et al. Tyramine and Octopamine independently inhibit serotonin-stimulated aversive behaviors in Caenorhabditis elegans through two novel amine receptors. J Neurosci. 2007;27:13402–12. https://doi.org/10.1523/JNEUROSCI.3495-07.2007.

Jin Y, Hoskins R, Horvitz HR. Control of type-D GABAergic neuron differentiation by C. Elegans UNC-30 homeodomain protein. Nature. 1994;372:780–3. https://doi.org/10.1038/372780a0.

Chronis N, Zimmer M, Bargmann CI. Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods. 2007;4:727–31. https://doi.org/10.1038/nmeth1075.

Jorgensen EM. Gaba. WormBook. 2005;1:1–13. https://doi.org/10.1895/wormbook.1.14.1.

Shen Y, Wen Q, Liu H, et al. An extrasynaptic GABAergic signal modulates a pattern of forward movement in Caenorhabditis elegans. Elife. 2016;5:1–25. https://doi.org/10.7554/eLife.14197.

McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. The GABAergic nervous system of Caenorhabditis elegans. Nature. 1993;364:337–41. https://doi.org/10.1038/364337a0.

Ségalat L, D a E, Kaplan JM. Modulation of serotonin-controlled behaviors by go in Caenorhabditis elegans. Science. 1995;267:1648–51. https://doi.org/10.1126/science.7886454.

Mendel JE, Korswagen HC, Liu KS, et al. Participation of the protein go in multiple aspects of behavior in C. Elegans. Science (80- ). 1995;267:1652–5. https://doi.org/10.1126/science.7886455.

Nurrish S, Ségalat L, Kaplan JM. Serotonin inhibition of synaptic transmission: gα(o) decreases the abundance of unc-13 at release sites. Neuron. 1999;24:231–42. https://doi.org/10.1016/S0896-6273(00)80835-1.

Miller KG, Emerson MD, Rand JB. Go alpha and diacylglycerol kinase negatively regulate the Gq alpha pathway in C elegans. Neuron. 1999;24:323–33.

Emtage L, Aziz-Zaman S, Padovan-Merhar O, et al. IRK-1 potassium channels mediate peptidergic inhibition of Caenorhabditis elegans serotonin neurons via a G(o) signaling pathway. J Neurosci. 2012;32:16285–95. https://doi.org/10.1523/JNEUROSCI.2667-12.2012.

Herlitze S, Garcia DE, Mackie K, et al. Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature. 1996;380:258–62. https://doi.org/10.1038/380258a0.

Reuveny E, Slesinger PA, Inglese J, et al. Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature. 1994;370:143–6. https://doi.org/10.1038/370143a0.

Thông tin
Thông tin xuất bản

Zoological Letters

Tập 4

1-14

Thông tin tác giả