A neuronal signaling pathway of CaMKII and Gqα regulates experience-dependent transcription of tph-1

Journal of Neuroscience

Volumn 33, Issue 3, 2013, Pages 925-935

  Qin, Yuqi ^a   Zhang, Xiaodong ^a   Zhang, Yun ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; G PROTEIN COUPLED RECEPTOR; PHOSPHOPROTEIN; PROTEIN EGL 30; SEROTONIN; TRANSCRIPTION FACTOR; TRYPTOPHAN HYDROXYLASE; TRYPTOPHAN HYDROXYLASE 1; UNC 43 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AVERSION; CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO; FLUORESCENCE MICROSCOPY; GENOTYPE; LEARNING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSATION; SIGNAL TRANSDUCTION; TRAINING; TRANSCRIPTION REGULATION; TRANSGENIC ANIMAL; UPREGULATION;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; NEURONS; PHOSPHORYLATION; SEROTONIN; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRYPTOPHAN HYDROXYLASE;

EID: 84872283713     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2355-12.2013     Document Type: Article

References (65)

1. Azmitia EC (2007) Serotonin and brain: evolution, neuroplasticity, and homeostasis. Int Rev Neurobiol 77:31-56. CrossRef Medline
2. Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-527. CrossRef Medline
3. Bastiani CA, Gharib S, Simon MI, Sternberg PW (2003) Caenorhabditis elegans Galphaq regulates egg-laying behavior via a PLCbeta-independent and serotonin-dependent signaling pathway and likely functions both in the nervous system and in muscle. Genetics 165:1805-1822. Medline
4. Baylis HA, Furuichi T, Yoshikawa F, Mikoshiba K, Sattelle DB (1999) Inositol 1,4,5-trisphosphate receptors are strongly expressed in the nervous system, pharynx, intestine, gonad and excretory cell of Caenorhabditis elegans and are encoded by a single gene (itr-1). J Mol Biol 294:467-476. CrossRef Medline
5. Berman NE, Puri V, Chandrala S, Puri S, Macgregor R, Liverman CS, Klein RM (2006) Serotonin in trigeminal ganglia of female rodents: relevance to menstrual migraine. Headache 46:1230-1245. CrossRef Medline
6. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94. Medline
7. Brocke L, Srinivasan M, Schulman H (1995) Developmental and regional expression of multifunctional Ca2+/calmodulin-dependent protein kinase isoforms in rat brain. J Neurosci 15:6797-6808. Medline
8. Brundage L, Avery L, Katz A, Kim UJ, Mendel JE, Sternberg PW, Simon MI (1996) Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability. Neuron 16:999-1009. CrossRef Medline
9. Busch KE, Laurent P, Soltesz Z, Murphy RJ, Faivre O, Hedwig B, Thomas M, Smith HL, de Bono M (2012) Tonic signaling from O(2) sensors sets neural circuit activity and behavioral state. Nat Neurosci 15:581-591. CrossRef Medline
10. Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman MB, Bargmann CI (2007) Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450:63-70. CrossRef Medline
11. Chamas F, Serova L, Sabban EL (1999) Tryptophan hydroxylase mRNA levels are elevated by repeated immobilization stress in rat raphe nuclei but not in pineal gland. Neurosci Lett 267:157-160. CrossRef Medline
12. Chase DL, Koelle MR (2007) Biogenic amine neurotransmitters in C. elegans. WormBook 1-15.
13. Chronis N, Zimmer M, Bargmann CI (2007) Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4:727-731. CrossRef Medline
14. Clandinin TR, DeModena JA, Sternberg PW (1998) Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92:523-533. CrossRef Medline
15. Dal Santo P, Logan MA, Chisholm AD, Jorgensen EM (1999) The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98:757-767.CrossRef Medline
16. Doi M, Iwasaki K (2002) Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33:249-259. CrossRef Medline
17. Ehret M, Cash CD, Hamon M, Maitre M (1989) Formal demonstration of the phosphorylation of rat brain tryptophan hydroxylase by Ca2+/calmodulin-dependent protein kinase. J Neurochem 52:1886-1891. CrossRef Medline
18. Elks ML, Youngblood WW, Kizer JS (1979) Serotonin synthesis and release in brain slices: independence of tryptophan. Brain Res 172:471-486. CrossRef Medline
19. Estevez AO, Cowie RH, Gardner KL, Estevez M (2006) Both insulin and calcium channel signaling are required for developmental regulation of serotonin synthesis in the chemosensory ADF neurons of Caenorhabditis elegans. Dev Biol 298:32-44. CrossRef Medline
20. Estevez M, Estevez AO, Cowie RH, Gardner KL (2004) The voltage-gated calcium channel UNC-2 is involved in stress-mediated regulation of tryptophan hydroxylase. J Neurochem 88:102-113. CrossRef Medline
21. Flavell SW, Greenberg ME (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31:563-590. CrossRef Medline
22. Frøkjaer-Jensen C, Kindt KS, Kerr RA, Suzuki H, Melnik-Martinez K, Gerstbreih B, Driscol M, Schafer WR (2006) Effects of voltage-gated calcium channel subunit genes on calcium influx in cultured C. elegans mechanosensory neurons. J Neurobiol 66:1125-1139. CrossRef Medline
23. Ha HI, Hendricks M, Shen Y, Gabel CV, Fang-Yen C, Qin Y, Colón-Ramos D, Shen K, Samuel AD, Zhang Y (2010) Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 68:1173-1186. CrossRef Medline
24. Hamon M, Bourgoin S, Artaud F, Glowinski J (1979) The role of intraneuronal 5-HT and of tryptophan hydroxylase activation in the control of 5-HT synthesis in rat brain slices incubated in K-enriched medium. J Neurochem 33:1031-1042. CrossRef Medline
25. Hendricks M, Ha H, Maffey N, Zhang Y (2012) Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement. Nature 487:99-103. CrossRef Medline
26. Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, Schafer WR (2005) In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J 24:63-72. CrossRef Medline
27. Jansen G, Thijssen KL, Werner P, van der Horst M, Hazendonk E, Plasterk RH (1999) The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat Genet 21:414-419. CrossRef Medline
28. Jensen P, Farago AF, Awatramani RB, Scott MM, Deneris ES, Dymecki SM (2008) Redefining the serotonergic system by genetic lineage. Nat Neurosci 11:417-419. CrossRef Medline
29. Kawli T, Wu C, Tan MW (2010) Systemic and cell intrinsic roles of Gqalpha signaling in the regulation of innate immunity, oxidative stress, and longevity in Caenorhabditis elegans. Proc Natl Acad Sci U S A 107:13788-13793. CrossRef Medline
30. Kelsch W, Lin CW, Mosley CP, Lois C (2009) A critical period for activitydependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 29:11852-11858. CrossRef Medline
31. Kunkel MT, Johnstone DB, Thomas JH, Salkoff L (2000) Mutants of a temperature-sensitive two-P domain potassium channel. J Neurosci 20: 7517-7524. Medline
32. Lackner MR, Nurrish SJ, Kaplan JM (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24:335-346. CrossRef Medline
33. Lee J, Jee C, Song HO, Bandyopadhyay J, Lee JI, Yu JR, Lee J, Park BJ, Ahnn J (2004) Opposing functions of calcineurin and CaMKII regulate G-protein signaling in egg-laying behavior of C. elegans. J Mol Biol 344: 585-595. CrossRef Medline
34. Lee RY, Lobel L, Hengartner M, Horvitz HR, Avery L (1997) Mutations in the alpha1 subunit of an L-type voltage-activated Ca2 channel cause myotonia in Caenorhabditis elegans. EMBO J 16:6066-6076. CrossRef Medline
35. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190. CrossRef Medline
36. Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169-182. CrossRef Medline
37. Malek ZS, Dardente H, Pevet P, Raison S (2005) Tissue-specific expression of tryptophan hydroxylase mRNAs in the rat midbrain: anatomical evidence and daily profiles. Eur J Neurosci 22:895-901. CrossRef Medline
38. Maryon EB, Coronado R, Anderson P (1996) unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J Cell Biol 134:885-893. CrossRef Medline
39. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959-3970. Medline
40. Mendel JE, Korswagen HC, Liu KS, Hajdu-Cronin YM, Simon MI, Plasterk RH, Sternberg PW (1995) Participation of the protein Go in multiple aspects of behavior in C. elegans. Science 267:1652-1655. CrossRef Medline
41. Miller KG, Emerson MD, Rand JB (1999) Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24:323-333. CrossRef Medline
42. Miyabayashi T, Palfreyman MT, Sluder AE, Slack F, Sengupta P (1999) Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Dev Biol 215:314-331. CrossRef Medline
43. Moussaif M, Sze JY (2009) Intraflagellar transport/Hedgehog-related signaling components couple sensory cilium morphology and serotonin biosynthesis in Caenorhabditis elegans. J Neurosci 29:4065-4075. CrossRef Medline
44. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101: 10554-10559. CrossRef Medline
45. Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19:137-141. CrossRef Medline
46. Nitabach MN, Wu Y, Sheeba V, Lemon WC, Strumbos J, Zelensky PK, White BH, Holmes TC (2006) Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J Neurosci 26:479-489. CrossRef Medline
47. Nurrish S, Ségalat L, Kaplan JM (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24:231-242. CrossRef Medline
48. Reiner DJ, Newton EM, Tian H, Thomas JH (1999) Diverse behavioural defects caused by mutations in Caenorhabditis elegans unc-43 CaM kinase II. Nature 402:199-203. CrossRef Medline
49. Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294:2372-2375. CrossRef Medline
50. Roayaie K, Crump JG, Sagasti A, Bargmann CI (1998) The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20:55-67. CrossRef Medline
51. Robatzek M, Thomas JH (2000) Calcium/calmodulin-dependent protein kinase II regulates Caenorhabditis elegans locomotion in concert with a G(o)/G(q) signaling network. Genetics 156:1069-1082. Medline
52. Rongo C, Kaplan JM (1999) CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402:195-199. CrossRef Medline
53. Sakube Y, Ando H, Kagawa H (1997) An abnormal ketamine response in mutants defective in the ryanodine receptor gene ryr-1 (unc-68) of Caenorhabditis elegans. J Mol Biol 267:849-864. CrossRef Medline
54. Schafer WR, Kenyon CJ (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375:73-78. CrossRef Medline
55. Ségalat L, Elkes DA, Kaplan JM (1995) Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267:1648-1651. CrossRef Medline
56. Shishkina GT, Kalinina TS, Dygalo NN (2008) Serotonergic changes produced by repeated exposure to forced swimming: correlation with behavior. Ann N Y Acad Sci 1148:148-153. CrossRef Medline
57. Suzuki H, Kerr R, Bianchi L, Frøkjaer-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M, Schafer WR (2003) In vivo imaging of C. elegans mechano sensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39:1005-1017. CrossRef Medline
58. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403:560-564. CrossRef Medline
59. Tallini YN, Ohkura M, Choi BR, Ji G, Imoto K, Doran R, Lee J, Plan P, Wilson J, Xin HB, Sanbe A, Gulick J, Mathai J, Robbins J, Salama G, Nakai J, Kotlikoff MI (2006) Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2 indicator GCaMP2. Proc Natl Acad Sci U S A 103:4753-4758. CrossRef Medline
60. Troemel ER, Kimmel BE, Bargmann CI (1997) Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91:161-169. CrossRef Medline
61. Umemura T, Rapp P, Rongo C (2005) The role of regulatory domain inter-actions in UNC-43 CaMKII localization and trafficking. J Cell Sci 118: 3327-3338. CrossRef Medline
62. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340. CrossRef Medline
63. Williams SL, Lutz S, Charlie NK, Vettel C, Ailion M, Coco C, Tesmer JJ, Jorgensen EM, Wieland T, Miller KG (2007) Trio's Rho-specific GEF domain is the missing Galpha q effector in C. elegans. Genes Dev 21:2731-2746. CrossRef Medline
64. Zhang S, Sokolchik I, Blanco G, Sze JY (2004) Caenorhabditis elegans TRPV ion channel regulates 5HT biosynthesis in chemosensory neurons. Development 131:1629-1638. CrossRef Medline
65. Zhang Y, Lu H, Bargmann CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438:179-184. CrossRef Medline