Heterologous expression of the invertebrate FMRFamide-gated sodium channel as a mechanism to selectively activate mammalian neurons

Neuroscience

Volumn 155, Issue 2, 2008, Pages 374-386

  Schanuel, S M ^a   Bell, K A ^a   Henderson, S C ^a   McQuiston, A R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

activation; heterologous expression; invertebrate ion channel; mammalian neuron; single cell electroporation

Indexed keywords

ACID SENSING ION CHANNEL; AMILORIDE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; NALPHA (DIPHENYLACETYL) N (4 HYDROXYBENZYL) DEXTRO ARGININAMIDE; NEUROPEPTIDE FF; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; RED FLUORESCENT PROTEIN; SODIUM CHANNEL;

ACTION POTENTIAL; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHANNEL GATING; CONTROLLED STUDY; DEPOLARIZATION; DOSE RESPONSE; ELECTROPORATION; HELIX ASPERSA; HIPPOCAMPUS; INVERTEBRATE; MAMMAL; MUTATION; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; TISSUE CULTURE;

ACTION POTENTIALS; ANIMALS; DNA, COMPLEMENTARY; ELECTROPORATION; FMRFAMIDE; GENE EXPRESSION; HELIX (SNAILS); HIPPOCAMPUS; ION CHANNEL GATING; MAMMALS; ORGAN CULTURE TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS; SPECIES SPECIFICITY;

EID: 49349115955     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.05.052     Document Type: Article

References (95)

1. Adamantidis A.R., Zhang F., Aravanis A.M., Deisseroth K., and de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450 (2007) 420-424
2. Apicella P. Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur J Neurosci 16 (2002) 2017-2026
3. Aravanis A.M., Wang L.P., Zhang F., Meltzer L.A., Mogri M.Z., Schneider M.B., and Deisseroth K. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng 4 (2007) S143-S156
4. Arenkiel B.R., Klein M.E., Davison I.G., Katz L.C., and Ehlers M.D. Genetic control of neuronal activity in mice conditionally expressing TRPV1. Nat Methods 5 (2008) 299-302
5. Arenkiel B.R., Peca J., Davison I.G., Feliciano C., Deisseroth K., Augustine G.J., Ehlers M.D., and Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54 (2007) 205-218
6. Arnold D.B. Polarized targeting of ion channels in neurons. Pflugers Arch 453 (2007) 763-769
7. Askwith C.C., Cheng C., Ikuma M., Benson C., Price M.P., and Welsh M.J. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 26 (2000) 133-141
8. Banghart M., Borges K., Isacoff E., Trauner D., and Kramer R.H. Light-activated ion channels for remote control of neuronal firing. Nat Neurosci 7 (2004) 1381-1386
9. Bi A., Cui J., Ma Y.P., Olshevskaya E., Pu M., Dizhoor A.M., and Pan Z.H. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50 (2006) 23-33
10. Bonini J.A., Jones K.A., Adham N., Forray C., Artymyshyn R., Durkin M.M., Smith K.E., Tamm J.A., Boteju L.W., Lakhlani P.P., Raddatz R., Yao W.J., Ogozalek K.L., Boyle N., Kouranova E.V., Quan Y., Vaysse P.J., Wetzel J.M., Branchek T.A., Gerald C., and Borowsky B. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J Biol Chem 275 (2000) 39324-39331
11. Boyden E.S., Zhang F., Bamberg E., Nagel G., and Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8 (2005) 1263-1268
12. Brussaard A.B., Kits K.S., ter Maat A., Mulder A.H., and Schoffelmeer A.N. Peripheral injection of DNS-RFa, a FMRFa agonist, suppresses morphine-induced analgesia in rats. Peptides 10 (1989) 735-739
13. Burlet-Schiltz O., Mazarguil H., Sol J.C., Chaynes P., Monsarrat B., Zajac J.M., and Roussin A. Identification of neuropeptide FF-related peptides in human cerebrospinal fluid by mass spectrometry. FEBS Lett 532 (2002) 313-318
14. Chambers J.J., Banghart M.R., Trauner D., and Kramer R.H. Light-induced depolarization of neurons using a modified shaker K(+) channel and a molecular photoswitch. J Neurophysiol 96 (2006) 2792-2796
15. Chung H.J., Jan Y.N., and Jan L.Y. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc Natl Acad Sci U S A 103 (2006) 8870-8875
16. Cottrell G.A. The first peptide-gated ion channel. J Exp Biol 200 (1997) 2377-2386
17. + channels. Pflugers Arch 450 (2005) 168-177
18. Dampney R.A., Horiuchi J., Tagawa T., Fontes M.A., Potts P.D., and Polson J.W. Medullary and supramedullary mechanisms regulating sympathetic vasomotor tone. Acta Physiol Scand 177 (2003) 209-218
19. + channels in Helisoma trivolvis and Helix aspersa neurones. J Neurocytol 30 (2001) 877-884
20. Detari L., Rasmusson D.D., and Semba K. The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog Neurobiol 58 (1999) 249-277
21. Dreher J.C., and Burnod Y. An integrative theory of the phasic and tonic modes of dopamine modulation in the prefrontal cortex. Neural Netw 15 (2002) 583-602
22. Ellis-Davies G.C. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat Methods 4 (2007) 619-628
23. Engstrom M., Brandt A., Wurster S., Savola J.M., and Panula P. Prolactin releasing peptide has high affinity and efficacy at neuropeptide FF2 receptors. J Pharmacol Exp Ther 305 (2003) 825-832
24. Fetter M. Vestibulo-ocular reflex. Dev Ophthalmol 40 (2007) 35-51
25. Fukusumi S., Fujii R., and Hinuma S. Recent advances in mammalian RFamide peptides: the discovery and functional analyses of PrRP, RFRPs and QRFP. Peptides 27 (2006) 1073-1086
26. Fukusumi S., Yoshida H., Fujii R., Maruyama M., Komatsu H., Habata Y., Shintani Y., Hinuma S., and Fujino M. A new peptidic ligand and its receptor regulating adrenal function in rats. J Biol Chem 278 (2003) 46387-46395
27. Furukawa Y., Miyawaki Y., and Abe G. Molecular cloning and functional characterization of the Aplysia FMRFamide-gated Na(+) channel. Pflugers Arch 451 (2006) 646-656
28. Garcia-Rill E., Homma Y., and Skinner R.D. Arousal mechanisms related to posture and locomotion: 1. Descending modulation. Prog Brain Res 143 (2004) 283-290
29. Garrido J.J., Fernandes F., Giraud P., Mouret I., Pasqualini E., Fache M.P., Jullien F., and Dargent B. Identification of an axonal determinant in the C-terminus of the sodium channel Na. (v) 1.2. EMBO J 20 (2001) 5950-5961
30. Garrido J.J., Giraud P., Carlier E., Fernandes F., Moussif A., Fache M.P., Debanne D., and Dargent B. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300 (2003) 2091-2094
31. Grace A.A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41 (1991) 1-24
32. + channel by FMRFamide and its analogues. J Physiol 519 Pt 1 (1999) 47-56
33. Green K.A., and Cottrell G.A. Activity modes and modulation of the peptide-gated Na(+) channel of Helix neurones. Pflugers Arch 443 (2002) 813-821
34. Gu C., Jan Y.N., and Jan L.Y. A conserved domain in axonal targeting of Kv1 (shaker) voltage-gated potassium channels. Science 301 (2003) 646-649
35. + channel axonal targeting. Neuron 52 (2006) 803-816
36. Guan C., Zhang S., Sun Y., and Zheng X. Assess the effect of ciliary neurotrophic factor on extracellular level of neuropeptide Y in paraventricular nucleus using microdialysis. Conf Proc IEEE Eng Med Biol Soc 4 (2005) 3608-3611
37. Haas K., Sin W.C., Javaherian A., Li Z., and Cline H.T. Single-cell electroporation for gene transfer in vivo. Neuron 29 (2001) 583-591
38. Han X., and Boyden E.S. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2 (2007) e299
39. Heien M.L., and Wightman R.M. Phasic dopamine signaling during behavior, reward, and disease states. CNS Neurol Disord Drug Targets 5 (2006) 99-108
40. Herlitze S., and Landmesser L.T. New optical tools for controlling neuronal activity. Curr Opin Neurobiol 17 (2007) 87-94
41. Hikosaka O. GABAergic output of the basal ganglia. Prog Brain Res 160 (2007) 209-226
42. Hilke S., Theodorsson A., Fetissov S., Aman K., Holm L., Hokfelt T., and Theodorsson E. Estrogen induces a rapid increase in galanin levels in female rat hippocampal formation-possibly a nongenomic/indirect effect. Eur J Neurosci 21 (2005) 2089-2099
43. Hinuma S., Shintani Y., Fukusumi S., Iijima N., Matsumoto Y., Hosoya M., Fujii R., Watanabe T., Kikuchi K., Terao Y., Yano T., Yamamoto T., Kawamata Y., Habata Y., Asada M., Kitada C., Kurokawa T., Onda H., Nishimura O., Tanaka M., Ibata Y., and Fujino M. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2 (2000) 703-708
44. Ishizuka T., Kakuda M., Araki R., and Yawo H. Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci Res 54 (2006) 85-94
45. Jeziorski M.C., Green K.A., Sommerville J., and Cottrell G.A. Cloning and expression of a FMRFamide-gated Na(+) channel from Helisoma trivolvis and comparison with the native neuronal channel. J Physiol 526 Pt 1 (2000) 13-25
46. Kellenberger S., and Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82 (2002) 735-767
47. Kiyashchenko L.I., Mileykovskiy B.Y., Maidment N., Lam H.A., Wu M.F., John J., Peever J., and Siegel J.M. Release of hypocretin (orexin) during waking and sleep states. J Neurosci 22 (2002) 5282-5286
48. Kiyatkin E.A. Functional significance of mesolimbic dopamine. Neurosci Biobehav Rev 19 (1995) 573-598
49. Kozak M. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15 (1987) 8125-8148
50. Kramer R.H., Chambers J.J., and Trauner D. Photochemical tools for remote control of ion channels in excitable cells. Nat Chem Biol 1 (2005) 360-365
51. Li X., Gutierrez D.V., Hanson M.G., Han J., Mark M.D., Chiel H., Hegemann P., Landmesser L.T., and Herlitze S. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A 102 (2005) 17816-17821
52. Lima S.Q., and Miesenbock G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121 (2005) 141-152
53. Lingueglia E., Champigny G., Lazdunski M., and Barbry P. Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature 378 (1995) 730-733
54. Lingueglia E., Deval E., and Lazdunski M. FMRFamide-gated sodium channel and ASIC channels: a new class of ionotropic receptors for FMRFamide and related peptides. Peptides 27 (2006) 1138-1152
55. Liu Q., Guan X.M., Martin W.J., McDonald T.P., Clements M.K., Jiang Q., Zeng Z., Jacobson M., Williams Jr. D.L., Yu H., Bomford D., Figueroa D., Mallee J., Wang R., Evans J., Gould R., and Austin C.P. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276 (2001) 36961-36969
56. Malin D.H., Lake J.R., Hammond M.V., Fowler D.E., Rogillio R.B., Brown S.L., Sims J.L., Leecraft B.M., and Yang H.Y. FMRF-NH2-like mammalian octapeptide: possible role in opiate dependence and abstinence. Peptides 11 (1990) 969-972
57. Mollereau C., Gouarderes C., Dumont Y., Kotani M., Detheux M., Doods H., Parmentier M., Quirion R., and Zajac J.M. Agonist and antagonist activities on human NPFF(2) receptors of the NPY ligands GR231118 and BIBP3226. Br J Pharmacol 133 (2001) 1-4
58. Mollereau C., Mazarguil H., Marcus D., Quelven I., Kotani M., Lannoy V., Dumont Y., Quirion R., Detheux M., Parmentier M., and Zajac J.M. Pharmacological characterization of human NPFF(1) and NPFF(2) receptors expressed in CHO cells by using NPY Y(1) receptor antagonists. Eur J Pharmacol 451 (2002) 245-256
59. Muir A.I., Chamberlain L., Elshourbagy N.A., Michalovich D., Moore D.J., Calamari A., Szekeres P.G., Sarau H.M., Chambers J.K., Murdock P., Steplewski K., Shabon U., Miller J.E., Middleton S.E., Darker J.G., Larminie C.G., Wilson S., Bergsma D.J., Emson P., Faull R., Philpott K.L., and Harrison D.C. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276 (2001) 28969-28975
60. Nagel G., Brauner M., Liewald J.F., Adeishvili N., Bamberg E., and Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15 (2005) 2279-2284
61. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100 (2003) 13940-13945
62. Pallis E.G., Spyraki C., and Thermos K. Chronic antidepressant treatment modulates the release of somatostatin in the rat nucleus accumbens. Neurosci Lett 395 (2006) 76-81
63. Pan Z., Kao T., Horvath Z., Lemos J., Sul J.Y., Cranstoun S.D., Bennett V., Scherer S.S., and Cooper E.C. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26 (2006) 2599-2613
64. Parrish A.R., Wang W., and Wang L. Manipulating proteins for neuroscience. Curr Opin Neurobiol 16 (2006) 585-592
65. + channel and its modulation by acid pH. J Neurosci 21 (2001) 5559-5567
66. Perry S.J., Yi-Kung H.E., Cronk D., Bagust J., Sharma R., Walker R.J., Wilson S., and Burke J.F. A human gene encoding morphine modulating peptides related to NPFF and FMRFamide. FEBS Lett 409 (1997) 426-430
67. Petreanu L., Huber D., Sobczyk A., and Svoboda K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10 (2007) 663-668
68. Price D.A., and Greenberg M.J. Structure of a molluscan cardioexcitatory neuropeptide. Science 197 (1977) 670-671
69. Rae J.L., and Levis R.A. Single-cell electroporation. Pflugers Arch 443 (2002) 664-670
70. 2) and related peptides on mammals. Peptides 9 (1988) 915-922
71. Raffa R.B. Supraspinal FMRFamide antagonizes morphine-induced horizontal, but not vertical, locomotor activity. Peptides 10 (1989) 403-406
72. Rathenberg J., Nevian T., and Witzemann V. High-efficiency transfection of individual neurons using modified electrophysiology techniques. J Neurosci Methods 126 (2003) 91-98
73. Richard P., Moos F., Dayanithi G., Gouzenes L., and Sabatier N. Rhythmic activities of hypothalamic magnocellular neurons: autocontrol mechanisms. Biol Cell 89 (1997) 555-560
74. Rivera J.F., Chu P.J., and Arnold D.B. The T1 domain of Kv1.3 mediates intracellular targeting to axons. Eur J Neurosci 22 (2005) 1853-1862
75. Roumy M., and Zajac J.M. Neuropeptide FF, pain and analgesia. Eur J Pharmacol 345 (1998) 1-11
76. Salio C., Lossi L., Ferrini F., and Merighi A. Neuropeptides as synaptic transmitters. Cell Tissue Res 326 (2006) 583-598
77. Sampo B., Kaech S., Kunz S., and Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37 (2003) 611-624
78. Schroll C., Riemensperger T., Bucher D., Ehmer J., Voller T., Erbguth K., Gerber B., Hendel T., Nagel G., Buchner E., and Fiala A. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16 (2006) 1741-1747
79. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., and Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22 (2004) 1567-1572
80. Shaner N.C., Steinbach P.A., and Tsien R.Y. A guide to choosing fluorescent proteins. Nat Methods 2 (2005) 905-909
81. Silverman M.A., Kaech S., Jareb M., Burack M.A., Vogt L., Sonderegger P., and Banker G. Sorting and directed transport of membrane proteins during development of hippocampal neurons in culture. Proc Natl Acad Sci U S A 98 (2001) 7051-7057
82. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37 (1991) 173-182
83. Sundblom D.M., Kalso E., Tigerstedt I., Wahlbeck K., Panula P., and Fyhrquist F. Neuropeptide FF-like immunoreactivity in human cerebrospinal fluid of chronic pain patients and healthy controls. Peptides 18 (1997) 923-927
84. Tang J., Yang H.Y., and Costa E. Inhibition of spontaneous and opiate-modified nociception by an endogenous neuropeptide with Phe-Met-Arg-Phe-NH2-like immunoreactivity. Proc Natl Acad Sci U S A 81 (1984) 5002-5005
85. Vilim F.S., Aarnisalo A.A., Nieminen M.L., Lintunen M., Karlstedt K., Kontinen V.K., Kalso E., States B., Panula P., and Ziff E. Gene for pain modulatory neuropeptide NPFF: induction in spinal cord by noxious stimuli. Mol Pharmacol 55 (1999) 804-811
86. Volgraf M., Gorostiza P., Numano R., Kramer R.H., Isacoff E.Y., and Trauner D. Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat Chem Biol 2 (2006) 47-52
87. Wightman R.M., and Robinson D.L. Transient changes in mesolimbic dopamine and their association with 'reward'. J Neurochem 82 (2002) 721-735
88. +-gated currents in cultured dorsal root ganglion neurons. J Neurophysiol 89 (2003) 2459-2465
89. Yang H.Y., Fratta W., Majane E.A., and Costa E. Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci U S A 82 (1985) 7757-7761
90. Zangen A., Nakash R., and Yadid G. Serotonin-mediated increases in the extracellular levels of beta-endorphin in the arcuate nucleus and nucleus accumbens: a microdialysis study. J Neurochem 73 (1999) 2569-2574
91. Zemelman B.V., Lee G.A., Ng M., and Miesenbock G. Selective photostimulation of genetically chARGed neurons. Neuron 33 (2002) 15-22
92. Zemelman B.V., Nesnas N., Lee G.A., and Miesenbock G. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc Natl Acad Sci U S A 100 (2003) 1352-1357
93. Zhang W., Ge W., and Wang Z. A toolbox for light control of Drosophila behaviors through channelrhodopsin 2-mediated photoactivation of targeted neurons. Eur J Neurosci 26 (2007) 2405-2416
94. Zhang Y.P., and Oertner T.G. Optical induction of synaptic plasticity using a light-sensitive channel. Nat Methods 4 (2007) 139-141
95. Zhou F.M., Wilson C.J., and Dani J.A. Cholinergic interneuron characteristics and nicotinic properties in the striatum. J Neurobiol 53 (2002) 590-605