Temperature regulates synaptic subcellular specificity mediated by inhibitory glutamate signaling
Autoři:
Mengqing Wang aff001; Daniel Witvliet aff002; Mengting Wu aff001; Lijun Kang aff004; Zhiyong Shao aff001
Působiště autorů:
Department of Neurosurgery, State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Institutes of Brain Science, Zhongshan Hospital, Fudan University, Shanghai, China
aff001; Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada
aff002; Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada
aff003; Department of Neurobiology and Department of Neurosurgery of the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China
aff004
Vyšlo v časopise:
Temperature regulates synaptic subcellular specificity mediated by inhibitory glutamate signaling. PLoS Genet 17(1): e1009295. doi:10.1371/journal.pgen.1009295
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009295
Souhrn
Environmental factors such as temperature affect neuronal activity and development. However, it remains unknown whether and how they affect synaptic subcellular specificity. Here, using the nematode Caenorhabditis elegans AIY interneurons as a model, we found that high cultivation temperature robustly induces defects in synaptic subcellular specificity through glutamatergic neurotransmission. Furthermore, we determined that the functional glutamate is mainly released by the ASH sensory neurons and sensed by two conserved inhibitory glutamate-gated chloride channels GLC-3 and GLC-4 in AIY. Our work not only presents a novel neurotransmission-dependent mechanism underlying the synaptic subcellular specificity, but also provides a potential mechanistic insight into high-temperature-induced neurological defects.
Klíčová slova:
Neurotransmission – Genetically modified animals – Glutamate – Chlorides – Interneurons – Neurons – Synapses – Test statistics
Zdroje
1. Sanes JR, Yamagata M. Many paths to synaptic specificity. Annu Rev Cell Dev Biol. 2009;25:161–195. doi: 10.1146/annurev.cellbio.24.110707.175402 19575668
2. Shen K, Scheiffele P. Genetics and cell biology of building specific synaptic connectivity. Annu Rev Neurosci. 2010;33:473–507. doi: 10.1146/annurev.neuro.051508.135302 20367446
3. Yogev S, Shen K. Cellular and molecular mechanisms of synaptic specificity. Annu Rev Cell Dev Biol. 2014;30:417–437. doi: 10.1146/annurev-cellbio-100913-012953 25150010
4. Ango F, Cristo Gd, Higashiyama H, Bennett V, Wu P, Huang ZJ. Ankyrin-Based Subcellular Gradient of Neurofascin, an Immunoglobulin Family Protein, Directs GABAergic Innervation at Purkinje Axon Initial Segment. Cell. 2004;119(2):257–272. doi: 10.1016/j.cell.2004.10.004 15479642
5. White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 1986;314(1165):1–340. doi: 10.1098/rstb.1986.0056 22462104
6. Colón-Ramos DA, Margeta MA, Kang S. Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science. 2007;318(5847):103–106. doi: 10.1126/science.1143762 17916735
7. Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, et al. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci. 2004;7(11):1184–1186. doi: 10.1038/nn1334 15475951
8. Huang ZJ. Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules. Nat Neurosci. 2006;9(2):163–166. doi: 10.1038/nn1638 16439983
9. Klassen MP, Shen K. Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans. Cell. 2007;130(4):704–716. doi: 10.1016/j.cell.2007.06.046 17719547
10. Betley JN, Wright CV, Kawaguchi Y, Erdelyi F, Szabo G, Jessell TM, et al. Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell. 2009;139(1):161–174. doi: 10.1016/j.cell.2009.08.027 19804761
11. Williams ME, Wilke SA, Daggett A, Davis E, Otto S, Ravi D, et al. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron. 2011;71(4):640–655. doi: 10.1016/j.neuron.2011.06.019 21867881
12. Ashrafi S, Betley JN, Comer JD, Brenner-Morton S, Bar V, Shimoda Y, et al. Neuronal Ig/Caspr recognition promotes the formation of axoaxonic synapses in mouse spinal cord. Neuron. 2014;81(1):120–129. doi: 10.1016/j.neuron.2013.10.060 24411736
13. Poon VY, Klassen MP, Shen K. UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature. 2008;455(7213):669–673. doi: 10.1038/nature07291 18776887
14. Mizumoto K, Shen K. Interaxonal interaction defines tiled presynaptic innervation in C. elegans. Neuron. 2013;77(4):655–666. doi: 10.1016/j.neuron.2012.12.031 23439119
15. Shen K, Bargmann CI. The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell. 2003;112(5):619–630. doi: 10.1016/s0092-8674(03)00113-2 12628183
16. Shen K, Fetter RD, Bargmann CI. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell. 2004;116(6):869–881. doi: 10.1016/s0092-8674(04)00251-x 15035988
17. West AE, Greenberg ME. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb Perspect Biol. 2011;3(6). doi: 10.1101/cshperspect.a005744 21555405
18. Penn AA. Early brain wiring: activity-dependent processes. Schizophr Bull. 2001;27(3):337–347. doi: 10.1093/oxfordjournals.schbul.a006880 11596840
19. Luhmann HJ, Khazipov R. Neuronal activity patterns in the developing barrel cortex. Neuroscience. 2018;368:256–267. doi: 10.1016/j.neuroscience.2017.05.025 28528963
20. Frohlich A, Meinertzhagen IA. Cell recognition during synaptogenesis is revealed after temperature-shock-induced perturbations in the developing fly's optic lamina. Journal of neurobiology. 1993;24(12):1642–1654. doi: 10.1002/neu.480241208 8301271
21. Sigrist SJ, Reiff DF, Thiel PR, Steinert JR, Schuster CM. Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci. 2003;23(16):6546–6556. doi: 10.1523/JNEUROSCI.23-16-06546.2003 12878696
22. Peng IF, Berke BA, Zhu Y, Lee WH, Chen W, Wu CF. Temperature-dependent developmental plasticity of Drosophila neurons: cell-autonomous roles of membrane excitability, Ca2+ influx, and cAMP signaling. J Neurosci. 2007;27(46):12611–12622. doi: 10.1523/JNEUROSCI.2179-07.2007 18003840
23. Zhong Y, Wu CF. Neuronal activity and adenylyl cyclase in environment-dependent plasticity of axonal outgrowth in Drosophila. J Neurosci. 2004;24(6):1439–1445. doi: 10.1523/JNEUROSCI.0740-02.2004 14960616
24. Black B, Vishwakarma V, Dhakal K, Bhattarai S, Pradhan P, Jain A, et al. Spatial temperature gradients guide axonal outgrowth. Sci Rep. 2016;6:29876. doi: 10.1038/srep29876 27460512
25. Chopra M, Singh S. Developmental temperature selectively regulates a voltage-activated potassium current in Drosophila. Journal of neurobiology. 1994;25(2):119–126. doi: 10.1002/neu.480250204 8021644
26. Galli L, Maffei L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science. 1988;242(4875):90–91. doi: 10.1126/science.3175637 3175637
27. Wiesel TN, Hubel DH. SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. J Neurophysiol. 1963;26:1003–1017. doi: 10.1152/jn.1963.26.6.1003 14084161
28. Katz LC, Shatz CJ. Synaptic activity and the construction of cortical circuits. Science. 1996;274(5290):1133–1138. doi: 10.1126/science.274.5290.1133 8895456
29. Oland LA, Pott WM, Bukhman G, Sun XJ, Tolbert LP. Activity blockade does not prevent the construction of olfactory glomeruli in the moth Manduca sexta. International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience. 1996;14(7–8):983–996.
30. Jefferis GS, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, Tanaka NK, et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development. 2004;131(1):117–130. doi: 10.1242/dev.00896 14645123
31. Hiesinger PR, Zhai RG, Zhou Y, Koh TW, Mehta SQ, Schulze KL, et al. Activity-independent prespecification of synaptic partners in the visual map of Drosophila. Curr Biol. 2006;16(18):1835–1843. doi: 10.1016/j.cub.2006.07.047 16979562
32. Kratsios P, Pinan-Lucarré B, Kerk SY, Weinreb A, Bessereau JL, Hobert O. Transcriptional coordination of synaptogenesis and neurotransmitter signaling. Curr Biol. 2015;25(10):1282–1295. doi: 10.1016/j.cub.2015.03.028 25913400
33. Gally C, Bessereau JL. GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J Neurosci. 2003;23(7):2591–2599. doi: 10.1523/JNEUROSCI.23-07-02591.2003 12684444
34. 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(2):539–548. doi: 10.1523/JNEUROSCI.19-02-00539.1999 9880574
35. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, et al. Activity-dependent plasticity in an olfactory circuit. Neuron. 2007;56(5):838–850. doi: 10.1016/j.neuron.2007.10.035 18054860
36. Tessier CR, Broadie K. Activity-dependent modulation of neural circuit synaptic connectivity. Front Mol Neurosci. 2009;2:8. doi: 10.3389/neuro.02.008.2009 19668708
37. Golovin RM, Broadie K. Developmental experience-dependent plasticity in the first synapse of the Drosophila olfactory circuit. J Neurophysiol. 2016;116(6):2730–2738. doi: 10.1152/jn.00616.2016 27683892
38. Grunwald Kadow IC. State-dependent plasticity of innate behavior in fruit flies. Curr Opin Neurobiol. 2019;54:60–65. doi: 10.1016/j.conb.2018.08.014 30219668
39. Peckol EL, Zallen JA, Yarrow JC, Bargmann CI. Sensory activity affects sensory axon development in C. elegans. Development. 1999;126(9):1891–1902. 10101123
40. Zhao H, Nonet ML. A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction. Development. 2000;127(6):1253–1266. 10683178
41. Cohn JA, Cebul ER, Valperga G, Brose L, de Bono M, Heiman MG, et al. Long-term activity drives dendritic branch elaboration of a C. elegans sensory neuron. Dev Biol. 2020;461(1):66–74. doi: 10.1016/j.ydbio.2020.01.005 31945343
42. Hart MP, Hobert O. Neurexin controls plasticity of a mature, sexually dimorphic neuron. Nature. 2018;553(7687):165–170. doi: 10.1038/nature25192 29323291
43. Horowitz LB, Brandt JP, Ringstad N. Repression of an activity-dependent autocrine insulin signal is required for sensory neuron development in C. elegans. Development. 2019;146(22). doi: 10.1242/dev.182873 31628111
44. Thompson-Peer KL, Bai J, Hu Z, Kaplan JM. HBL-1 patterns synaptic remodeling in C. elegans. Neuron. 2012;73(3):453–465. doi: 10.1016/j.neuron.2011.11.025 22325199
45. Cuentas-Condori A, Mulcahy B, He S, Palumbos S, Zhen M, Miller DM 3rd. C. elegans neurons have functional dendritic spines. Elife. 2019;8. doi: 10.7554/eLife.47918 31584430
46. Mori I, Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature. 1995;376(6538):344–348. doi: 10.1038/376344a0 7630402
47. Ryu WS, Samuel AD. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined Thermal stimuli. J Neurosci. 2002;22(13):5727–5733. doi: 20026542 12097525
48. Gray JM, Hill JJ, Bargmann CI. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2005;102(9):3184–3191. doi: 10.1073/pnas.0409009101 15689400
49. Ikeda M, Nakano S, Giles AC, Xu L, Costa WS, Gottschalk A, et al. Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2020;117(11):6178–6188. doi: 10.1073/pnas.1918528117 32123108
50. Luo L, Cook N, Venkatachalam V, Martinez-Velazquez LA, Zhang X, Calvo AC, et al. Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proc Natl Acad Sci U S A. 2014;111(7):2776–2781. doi: 10.1073/pnas.1315205111 24550307
51. Ohnishi N, Kuhara A, Nakamura F, Okochi Y, Mori I. Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. Embo j. 2011;30(7):1376–1388. doi: 10.1038/emboj.2011.13 21304490
52. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol. 1986;117(2):456–487. doi: 10.1016/0012-1606(86)90314-3 2428682
53. Biron D, Wasserman S, Thomas JH, Samuel AD, Sengupta P. An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proc Natl Acad Sci U S A. 2008;105(31):11002–11007. doi: 10.1073/pnas.0805004105 18667708
54. Kuhara A, Okumura M, Kimata T, Tanizawa Y, Takano R, Kimura KD, et al. Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science. 2008;320(5877):803–807. doi: 10.1126/science.1148922 18403676
55. Shao Z, Watanabe S, Christensen R, Jorgensen EM, Colon-Ramos DA. Synapse location during growth depends on glia location. Cell. 2013;154(2):337–350. doi: 10.1016/j.cell.2013.06.028 23870123
56. Fan J, Ji T, Wang K, Huang J, Wang M, Manning L, et al. A muscle-epidermis-glia signaling axis sustains synaptic specificity during allometric growth in Caenorhabditis elegans. Elife. 2020;9. doi: 10.7554/eLife.55890 32255430
57. Maruyama IN, Brenner S. A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1991;88(13):5729–5733. doi: 10.1073/pnas.88.13.5729 2062851
58. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in caenorhabditis elegans. J Neurosci. 1999;19(1):159–167. doi: 10.1523/JNEUROSCI.19-01-00159.1999 9870947
59. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. Identification and characterization of the vesicular GABA transporter. Nature. 1997;389(6653):870–876. doi: 10.1038/39908 9349821
60. Alfonso A, Grundahl K, Duerr JS, Han HP, Rand JB. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science. 1993;261(5121):617–619. doi: 10.1126/science.8342028 8342028
61. Lints R, Emmons SW. Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene. Development. 1999;126(24):5819–5831. 10572056
62. Thompson O, Edgley M, Strasbourger P, Flibotte S, Ewing B, Adair R, et al. The million mutation project: a new approach to genetics in Caenorhabditis elegans. Genome Res. 2013;23(10):1749–1762. doi: 10.1101/gr.157651.113 23800452
63. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, Horvitz HR, et al. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J Neurosci. 1997;17(21):8061–8073. doi: 10.1523/JNEUROSCI.17-21-08061.1997 9334382
64. Serrano-Saiz E, Poole RJ, Felton T, Zhang F, De La Cruz ED, Hobert O. Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell. 2013;155(3):659–673. doi: 10.1016/j.cell.2013.09.052 24243022
65. Egan CR, Chung MA, Allen FL, Heschl MF, Van Buskirk CL, McGhee JD. A gut-to-pharynx/tail switch in embryonic expression of the Caenorhabditis elegans ges-1 gene centers on two GATA sequences. Dev Biol. 1995;170(2):397–419. doi: 10.1006/dbio.1995.1225 7649372
66. Fox RM, Watson JD, Stetina SEV, Mcdermott J, Brodigan TM, Fukushige T, et al. The embryonic muscle transcriptome of Caenorhabditis elegans. Genome Biology. 2007;8(9):R188. doi: 10.1186/gb-2007-8-9-r188 17848203
67. McMahon L, Muriel JM, Roberts B, Quinn M, Johnstone IL. Two sets of interacting collagens form functionally distinct substructures within a Caenorhabditis elegans extracellular matrix. Mol Biol Cell. 2003;14(4):1366–1378. doi: 10.1091/mbc.e02-08-0479 12686594
68. McMiller TL, Johnson CM. Molecular characterization of HLH-17, a C. elegans bHLH protein required for normal larval development. Gene. 2005;356:1–10. doi: 10.1016/j.gene.2005.05.003 16014321
69. Wenick AS, Hobert O. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev Cell. 2004;6(6):757–770. doi: 10.1016/j.devcel.2004.05.004 15177025
70. Kim K, Li C. Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. J Comp Neurol. 2004;475(4):540–550. doi: 10.1002/cne.20189 15236235
71. Yu S, Avery L, Baude E, Garbers DL. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci U S A. 1997;94(7):3384–3387. doi: 10.1073/pnas.94.7.3384 9096403
72. Troemel ER, Sagasti A, Bargmann CI. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell. 1999;99(4):387–398. doi: 10.1016/s0092-8674(00)81525-1 10571181
73. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV. Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci. 2001;21(5):1510–1522. doi: 10.1523/JNEUROSCI.21-05-01510.2001 11222641
74. Dwyer ND, Troemel ER, Sengupta P, Bargmann CI. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell. 1998;93(3):455–466. doi: 10.1016/s0092-8674(00)81173-3 9590179
75. Lee BH, Liu J, Wong D, Srinivasan S, Ashrafi K. Hyperactive neuroendocrine secretion causes size, feeding, and metabolic defects of C. elegans Bardet-Biedl syndrome mutants. PLoS Biol. 2011;9(12):e1001219. doi: 10.1371/journal.pbio.1001219 22180729
76. Macosko EZ, Navin P, Feinberg EH, Chalasani SH, Butcher RA, Jon C, et al. A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature. 2009;458(7242):1171–1175. doi: 10.1038/nature07886 19349961
77. Miyabayashi T, Palfreyman MT, Sluder AE, Slack F, Sengupta P. Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Developmental Biology. 1999;215(2):314. doi: 10.1006/dbio.1999.9470 10545240
78. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 1995;83(2):207–218. doi: 10.1016/0092-8674(95)90162-0 7585938
79. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, et al. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci. 2004;24(46):10466–10474. doi: 10.1523/JNEUROSCI.3001-04.2004 15548661
80. Daniels RW, Miller BR, DiAntonio A. Increased vesicular glutamate transporter expression causes excitotoxic neurodegeneration. Neurobiol Dis. 2011;41(2):415–420. doi: 10.1016/j.nbd.2010.10.009 20951206
81. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, et al. Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci. 2005;25(26):6221–6234. doi: 10.1523/JNEUROSCI.3003-04.2005 15987952
82. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, et al. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A. 2004;101(18):7158–7163. doi: 10.1073/pnas.0401764101 15103023
83. Chelur DS, Martin C. Targeted cell killing by reconstituted caspases. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(7):2283–2288. doi: 10.1073/pnas.0610877104 17283333
84. Brockie PJ, Maricq AV. Ionotropic glutamate receptors in Caenorhabditis elegans. Neuro-Signals. 2003;12(3):108–125. doi: 10.1159/000072159 12904685
85. Brockie PJ, Maricq AV. Ionotropic glutamate receptors: genetics, behavior and electrophysiology. WormBook. 2006:1–16.
86. Dillon J, Hopper NA, Holden-Dye L, O'Connor V. Molecular characterization of the metabotropic glutamate receptor family in Caenorhabditis elegans. Biochem Soc Trans. 2006;34(Pt 5):942–948. doi: 10.1042/BST0340942 17052233
87. Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br J Pharmacol. 2001;132(6):1247–1254. doi: 10.1038/sj.bjp.0703937 11250875
88. Dent JA, Davis MW, Avery L. avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. Embo j. 1997;16(19):5867–5879. doi: 10.1093/emboj/16.19.5867 9312045
89. Petersen CI, McFarland TR, Stepanovic SZ, Yang P, Reiner DJ, Hayashi K, et al. In vivo identification of genes that modify ether-a-go-go-related gene activity in Caenorhabditis elegans may also affect human cardiac arrhythmia. Proc Natl Acad Sci U S A. 2004;101(32):11773–11778. doi: 10.1073/pnas.0306005101 15280551
90. Collins KM, Koelle MR. Postsynaptic ERG potassium channels limit muscle excitability to allow distinct egg-laying behavior states in Caenorhabditis elegans. J Neurosci. 2013;33(2):761–775. doi: 10.1523/JNEUROSCI.3896-12.2013 23303953
91. Jin X, Pokala N, Bargmann Cornelia I. Distinct Circuits for the Formation and Retrieval of an Imprinted Olfactory Memory. Cell. 2016;164(4):632–643. doi: 10.1016/j.cell.2016.01.007 26871629
92. Bai X, Li K, Yao L, Kang XL, Cai SQ. A forward genetic screen identifies chaperone CNX-1 as a conserved biogenesis regulator of ERG K(+) channels. The Journal of general physiology. 2018;150(8):1189–1201. doi: 10.1085/jgp.201812025 29941431
93. Hawk JD, Calvo AC, Liu P, Almoril-Porras A, Aljobeh A, Torruella-Suárez ML, et al. Integration of Plasticity Mechanisms within a Single Sensory Neuron of C. elegans Actuates a Memory. Neuron. 2018;97(2):356–367.e354. doi: 10.1016/j.neuron.2017.12.027 29307713
94. Cook SJ, Jarrell TA, Brittin CA, Wang Y, Bloniarz AE, Yakovlev MA, et al. Whole-animal connectomes of both Caenorhabditis elegans sexes. Nature. 2019;571(7763):63–71. doi: 10.1038/s41586-019-1352-7 31270481
95. Witvliet D, Mulcahy B, Mitchell JK, Meirovitch Y, Berger DR, Wu Y, et al. Connectomes across development reveal principles of brain maturation in C. elegans. 2020:2020.2004.2030.066209.
96. Fatt HV, Dougherty EC. Genetic Control of Differential Heat Tolerance in Two Strains of the Nematode Caenorhabditis elegans. Science. 1963;141(3577):266–267. doi: 10.1126/science.141.3577.266 17841565
97. Miesenböck G, De Angelis DA, Rothman JE. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature. 1998;394(6689):192–195. doi: 10.1038/28190 9671304
98. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science. 1999;284(5421):1811–1816. doi: 10.1126/science.284.5421.1811 10364548
99. Wong WT, Wong RO. Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nat Neurosci. 2001;4(4):351–352. doi: 10.1038/85987 11276221
100. Zheng JQ, Felder M, Connor JA, Poo MM. Turning of nerve growth cones induced by neurotransmitters. Nature. 1994;368(6467):140–144. doi: 10.1038/368140a0 8139655
101. Huang ZJ. Activity-dependent development of inhibitory synapses and innervation pattern: role of GABA signalling and beyond. J Physiol. 2009;587(Pt 9):1881–1888. doi: 10.1113/jphysiol.2008.168211 19188247
102. Oh WC, Smith KR. Activity-dependent development of GABAergic synapses. Brain Res. 2019;1707:18–26. doi: 10.1016/j.brainres.2018.11.014 30439352
103. Oh WC, Lutzu S, Castillo PE, Kwon HB. De novo synaptogenesis induced by GABA in the developing mouse cortex. Science. 2016;353(6303):1037–1040. doi: 10.1126/science.aaf5206 27516412
104. Gibson CL, Balbona JT, Niedzwiecki A, Rodriguez P, Nguyen KCQ, Hall DH, et al. Glial loss of the metallo β-lactamase domain containing protein, SWIP-10, induces age- and glutamate-signaling dependent, dopamine neuron degeneration. PLoS Genet. 2018;14(3):e1007269. doi: 10.1371/journal.pgen.1007269 29590100
105. Kalivas PW. The glutamate homeostasis hypothesis of addiction. Nat Rev Neurosci. 2009;10(8):561–572. doi: 10.1038/nrn2515 19571793
106. Mitchell SJ, Silver RA. Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature. 2000;404(6777):498–502. doi: 10.1038/35006649 10761918
107. Katz M, Corson F, Keil W, Singhal A, Bae A, Lu Y, et al. Glutamate spillover in C. elegans triggers repetitive behavior through presynaptic activation of MGL-2/mGluR5. Nat Commun. 2019;10(1):1882. doi: 10.1038/s41467-019-09581-4 31015396
108. Hardaway JA, Sturgeon SM, Snarrenberg CL, Li Z, Xu XZ, Bermingham DP, et al. Glial Expression of the Caenorhabditis elegans Gene swip-10 Supports Glutamate Dependent Control of Extrasynaptic Dopamine Signaling. J Neurosci. 2015;35(25):9409–9423. doi: 10.1523/JNEUROSCI.0800-15.2015 26109664
109. Isaacson JS, Solís JM, Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron. 1993;10(2):165–175. doi: 10.1016/0896-6273(93)90308-e 7679913
110. Isaacson JS. Spillover in the spotlight. Curr Biol. 2000;10(13):R475–477. doi: 10.1016/s0960-9822(00)00551-0 10898970
111. Manz KM, Baxley AG, Zurawski Z, Hamm HE, Grueter BA. Heterosynaptic GABA(B) Receptor Function within Feedforward Microcircuits Gates Glutamatergic Transmission in the Nucleus Accumbens Core. J Neurosci. 2019;39(47):9277–9293. doi: 10.1523/JNEUROSCI.1395-19.2019 31578230
112. Sanchez-Vives MV, Barbero-Castillo A, Perez-Zabalza M, Reig R. GABA(B) receptors: modulation of thalamocortical dynamics and synaptic plasticity. Neuroscience. 2020. doi: 10.1016/j.neuroscience.2020.03.011 32194227
113. Vassilatis DK, Arena JP, Plasterk RH, Wilkinson HA, Schaeffer JM, Cully DF, et al. Genetic and biochemical evidence for a novel avermectin-sensitive chloride channel in Caenorhabditis elegans. Isolation and characterization. J Biol Chem. 1997;272(52):33167–33174. doi: 10.1074/jbc.272.52.33167 9407104
114. Wolstenholme AJ. Glutamate-gated chloride channels. J Biol Chem. 2012;287(48):40232–40238. doi: 10.1074/jbc.R112.406280 23038250
115. Vassilatis DK, Elliston KO, Paress PS, Hamelin M, Arena JP, Schaeffer JM, et al. Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate-gated chloride channels. Journal of molecular evolution. 1997;44(5):501–508. doi: 10.1007/pl00006174 9115174
116. Avila A, Vidal PM, Dear TN, Harvey RJ, Rigo JM, Nguyen L. Glycine receptor alpha2 subunit activation promotes cortical interneuron migration. Cell Rep. 2013;4(4):738–750. doi: 10.1016/j.celrep.2013.07.016 23954789
117. Kirsch J, Betz H. Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature. 1998;392(6677):717–720. doi: 10.1038/33694 9565032
118. Lynch JW, Zhang Y, Talwar S, Estrada-Mondragon A. Glycine Receptor Drug Discovery. Adv Pharmacol. 2017;79:225–253. doi: 10.1016/bs.apha.2017.01.003 28528670
119. Beverly M, Anbil S, Sengupta P. Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans. J Neurosci. 2011;31(32):11718–11727. doi: 10.1523/JNEUROSCI.1098-11.2011 21832201
120. Edwards MJ. Review: Hyperthermia and fever during pregnancy. Birth defects research Part A, Clinical and molecular teratology. 2006;76(7):507–516. doi: 10.1002/bdra.20277 16933304
121. Wang X, Amei A, de Belle JS, Roberts SP. Environmental effects on Drosophila brain development and learning. The Journal of experimental biology. 2018;221(Pt 1). doi: 10.1242/jeb.169375 29061687
122. Mellert DJ, Williamson WR, Shirangi TR, Card GM, Truman JW. Genetic and Environmental Control of Neurodevelopmental Robustness in Drosophila. PLoS One. 2016;11(5):e0155957. doi: 10.1371/journal.pone.0155957 27223118
123. Zhang B, Gong J, Zhang W, Xiao R, Liu J, Xu XZS. Brain-gut communications via distinct neuroendocrine signals bidirectionally regulate longevity in C. elegans. Genes Dev. 2018;32(3–4):258–270. doi: 10.1101/gad.309625.117 29491136
124. Kotera I, Tran NA, Fu D, Kim JH, Byrne Rodgers J, Ryu WS. Pan-neuronal screening in Caenorhabditis elegans reveals asymmetric dynamics of AWC neurons is critical for thermal avoidance behavior. Elife. 2016;5. doi: 10.7554/eLife.19021 27849153
125. Samuel AD, Silva RA, Murthy VN. Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J Neurosci. 2003;23(2):373–376. doi: 10.1523/JNEUROSCI.23-02-00373.2003 12533596
126. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94. 4366476
127. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, 3rd, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6(5):343–345. doi: 10.1038/nmeth.1318 19363495
128. Mello C, Fire A. DNA transformation. Methods Cell Biol. 1995;48:451–482. 8531738
129. Ventimiglia D, Bargmann CI. Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons. Elife. 2017;6. doi: 10.7554/eLife.31234 29160768
130. Saalfeld S, Cardona A, Hartenstein V, Tomancak P. CATMAID: collaborative annotation toolkit for massive amounts of image data. Bioinformatics (Oxford, England). 2009;25(15):1984–1986. doi: 10.1093/bioinformatics/btp266 19376822
131. Chandler-Brown D, Choi H, Park S, Ocampo BR, Chen S, Le A, et al. Sorbitol treatment extends lifespan and induces the osmotic stress response in Caenorhabditis elegans. Frontiers in genetics. 2015;6:316. doi: 10.3389/fgene.2015.00316 26579191
132. Lee SS, Lee RY, Fraser AG, Kamath RS, Ahringer J, Ruvkun G. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat Genet. 2003;33(1):40–48. doi: 10.1038/ng1056 12447374
133. Shao J, Zhang X, Cheng H, Yue X, Zou W, Kang L. Serotonergic neuron ADF modulates avoidance behaviors by inhibiting sensory neurons in C. elegans. Pflugers Archiv: European journal of physiology. 2019;471(2):357–363. doi: 10.1007/s00424-018-2202-4 30206705
Článek vyšel v časopise
PLOS Genetics
2021 Číslo 1
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- MED19 alters AR occupancy and gene expression in prostate cancer cells, driving MAOA expression and growth under low androgen
- A rare coding mutation in the MAST2 gene causes venous thrombosis in a French family with unexplained thrombophilia: The Breizh MAST2 Arg89Gln variant
- Population structure of indigenous inhabitants of Arabia
- Epithelial cell-turnover ensures robust coordination of tissue growth in Drosophila ribosomal protein mutants