An internally modulated, thermostable, pH-sensitive cys loop receptor from the hydrothermal vent worm Alvinella pompejana

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 15130-15140

  Juneja, Puneet ^a   Horlacher, Reinhold ^b   Bertrand, Daniel ^c   Krause, Ryoko ^c   Marger, Fabrice ^c   Welte, Wolfram ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b Trenzyme GmbH   (Germany)

^c HiQScreen Sàrl ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CLONING; DROPS;

EXPRESSED SEQUENCE TAG DATABASE; FUNCTIONAL CHANNELS; FUNCTIONAL RECEPTORS; HYDROTHERMAL VENT; INTRACELLULAR LOOP; MEMBRANE POTENTIALS; NICOTINIC ACETYLCHOLINE RECEPTORS; SEQUENCE COMPARISONS;

HOT SPRINGS;

CYSTEINE LOOP LIGAND GATED ION CHANNEL RECEPTOR; IVERMECTIN; NICOTINIC RECEPTOR;

ALVINELLA POMPEJANA; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANNELID; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; ELECTRODE; EXPRESSED SEQUENCE TAG; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PH; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PURIFICATION; SEQUENCE ANALYSIS; TEMPERATURE; THERMOSTABILITY; TORPEDO CALIFORNICA; VOLTAGE CLAMP TECHNIQUE; XENOPUS;

ALVINELLA POMPEJANA; CYS LOOP RECEPTOR; IVERMECTIN; MEMBRANE PROTEINS; NEUROTRANSMITTER RECEPTORS; NICOTINIC ACETYLCHOLINE RECEPTORS; PATCH CLAMP ELECTROPHYSIOLOGY; PH SENSITIVITY; PROTEIN CONFORMATION; RECOMBINANT PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; ANTIPARASITIC AGENTS; BASE SEQUENCE; CYSTEINE LOOP LIGAND-GATED ION CHANNEL RECEPTORS; FEMALE; HYDROGEN-ION CONCENTRATION; HYDROTHERMAL VENTS; IVERMECTIN; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; OOCYTES; PHYLOGENY; PICROTOXIN; POLYCHAETA; PROTEIN STABILITY; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SF9 CELLS; TEMPERATURE; XENOPUS;

EID: 84901391215     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.525576     Document Type: Article

References (47)

1. Smart, T. G., and Paoletti, P. (2012) Synaptic neurotransmitter-gated receptors. Cold Spring Harb. Perspect. Biol. 4, 1-26
2. Corringer, P.-J., Poitevin, F., Prevost, M. S., Sauguet, L., Delarue, M., and Changeux, J.-P. (2012) Structure and pharmacology of pentameric receptor channels: from bacteria to brain. Structure 20, 941-956
3. Sine, S. M., and Engel, A. G. (2006) Recent advances in Cys-loop receptor structure and function. Nature 440, 448-455
4. Miyazawa, A., Fujiyoshi, Y., and Unwin, N. (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423, 949-955 (Pubitemid 36806903)
5. Karlin, A. (2002) Emerging structure of the nicotinic acetylcholine receptors. Nat. Rev. Neurosci. 3, 102-114 (Pubitemid 135706579)
6. Tasneem, A., Iyer, L. M., Jakobsson, E., and Aravind, L. (2005) Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels. Genome Biol. 6, R4
7. Bocquet, N., Prado de Carvalho, L., Cartaud, J., Neyton, J., Le Poupon, C., Taly, A., Grutter, T., Changeux, J.-P., and Corringer, P.-J. (2007) A prokaryotic proton-gated ion channel from the nicotinic acetylcholine receptor family. Nature 445, 116-119 (Pubitemid 46067312)
8. Bocquet, N., Nury, H., Baaden, M., Le Poupon, C., Changeux, J.-P., Delarue, M., and Corringer, P.-J. (2009) X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation. Nature 457, 111-114
9. Desbruyères, D., and Laubier, L. (1980) Alvinella pompejana gen. sp. nov., aberrant Ampharetidae from the East Pacific Rise hydrothermal vents. Oceanologica Acta 3, 267-274
10. Stein, S. T., and Cary, S. C. (1998) Worm bask in extreme temperatures. Nature 391, 545-546
11. Le Bris, N., and Gaill, F. (2006) How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment? Rev. Environ. Sci. Biotechnol. 6, 197-221 (Pubitemid 46130088)
12. Gagnière, N., Jollivet, D., Boutet, I., Brélivet, Y., Busso, D., Da Silva, C., Gaill, F., Higuet, D., Hourdez, S., Knoops, B., Lallier, F., Leize-Wagner, E., Mary, J., Moras, D., Perrodou, E., Rees, J.-F., Segurens, B., Shillito, B., Tanguy, A., Thierry, J.-C., Weissenbach, J., Wincker, P., Zal, F., Poch, O., and Lecompte, O. (2010) Insights into metazoan evolution from Alvinella pompejana cDNAs. BMC Genomics 11, 634
13. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M., Claverie, J.-M., and Gascuel, O. (2008) Phylogeny.fr: robust phylogenetic analysis for the nonspecialist. Nucleic Acids Res. 36, W465-469
14. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H., and Poolman, B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. J. Mol. Biol. 317, 591-600 (Pubitemid 34722171)
15. Hoda, J.-C., Gu, W., Friedli, M., Phillips, H. A., Bertrand, S., Antonarakis, S. E., Goudie, D., Roberts, R., Scheffer, I. E., Marini, C., Patel, J., Berkovic, S. F., Mulley, J. C., Steinlein, O. K., and Bertrand, D. (2008) Human nocturnal frontal lobe epilepsy: pharmocogenomic profiles of pathogenic nicotinic acetylcholine receptor β-subunit mutations outside the ion channel pore. Mol. Pharmacol. 74, 379-391
16. Hogg, R. C., Bandelier, F., Benoit, A., Dosch, R., and Bertrand, D. (2008) An automated system for intracellular and intranuclear injection. J. Neurosci. Methods 169, 65-75
17. Silberberg, S. D., Li, M., and Swartz, K. J. (2007) Ivermectin interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels. Neuron 54, 263-274 (Pubitemid 46561201)
18. Krause, R. M., Buisson, B., Bertrand, S., Corringer, P. J., Galzi, J. L., Changeux, J. P., and Bertrand, D. (1998) Ivermectin: a positive allosteric effector of the α7 neuronal nicotinic acetylcholine receptor. Mol. Pharmacol. 53, 283-294 (Pubitemid 28099739)
19. Hurst, R. S., Hajós, M., Raggenbass, M., Wall, T. M., Higdon, N. R., Lawson, J. A., Rutherford-Root, K. L., Berkenpas, M. B., Hoffmann, W. E., Piotrowski, D. W., Groppi, V. E., Allaman, G., Ogier, R., Bertrand, S., Bertrand, D., and Arneric, S. P. (2005) A novel positive allosteric modulator of the α7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. J. Neurosci. 25, 4396-4405 (Pubitemid 40628784)
20. Hibbs, R. E., and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60
21. Jensen, M. L., Schousboe, A., and Ahring, P. K. (2005) Charge selectivity of the Cys-loop family of ligand-gated ion channels. J. Neurochem. 92, 217-225 (Pubitemid 40194013)
22. Thompson, A. J., Alqazzaz, M., Ulens, C., and Lummis, S. C. (2012) The pharmacological profile of ELIC, a prokaryotic GABA-gated receptor. Neuropharmacology 63, 761-767
23. Velisetty, P., and Chakrapani, S. (2012) Desensitization mechanism in prokaryotic ligand-gated ion channel. J. Biol. Chem. 287, 18467-18477
24. Duret, G., Van Renterghem, C., Weng, Y., Prevost, M., Moraga-Cid, G., Huon, C., Sonner, J. M., and Corringer, P.-J. (2011) Functional prokaryotic-eukaryotic chimera from the pentameric ligand-gated ion channel family. Proc. Natl. Acad. Sci. U.S.A. 108, 12143-12148
25. Celie, P. H., van Rossum-Fikkert, S. E., van Dijk, W. J., Brejc, K., Smit, A. B., and Sixma, T. K. (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41, 907-914 (Pubitemid 38429734)
26. Schnizler, K., Saeger, B., Pfeffer, C., Gerbaulet, A., Ebbinghaus-Kintscher, U., Methfessel, C., Franken, E.-M., Raming, K., Wetzel, C. H., Saras, A., Pusch, H., Hatt, H., and Gisselmann, G. (2005)Anovel chloride channel in Drosophila melanogaster is inhibited by protons. J. Biol. Chem. 280, 16254-16262 (Pubitemid 40616752)
27. Beg, A. A., Ernstrom, G. G., Nix, P., Davis, M. W., and Jorgensen, E. M. (2008) Protons act as a transmitter for muscle contraction in C. elegans. Cell 132, 149-160
28. Wooltorton, J. R., Moss, S. J., and Smart, T. G. (1997) Pharmacological and physiological characterization of murine homomeric β3 GABA(A) receptors. Eur. J. Neurosci. 9, 2225-2235
29. Papke, R. L., Kem, W. R., Soti, F., López-Hernández, G. Y., and Horenstein, N. A. (2009) Activation and desensitization of nicotinic α7-type acetylcholine receptors by benzylidene anabaseines and nicotine. J. Pharmacol. Exp. Ther. 329, 791-807
30. Gondhalekar, A. D., and Scharf, M. E. (2012) Mechanisms underlying fipronil resistance in a multiresistant field strain of the German cockroach (Blattodea: Blattellidae). J. Med. Entomol. 49, 122-131
31. Shan, Q., Haddrill, J. L., and Lynch, J. W. (2001) Ivermectin, an unconventional agonist of the glycine receptor chloride channel. J. Biol. Chem. 276, 12556-12564
32. McCavera, S., Rogers, A. T., Yates, D. M., Woods, D. J., and Wolstenholme, A. J. (2009) An ivermectin-sensitive glutamate-gated chloride channel from the parasitic nematode Haemonchus contortus. Mol. Pharmacol. 75, 1347-1355
33. Mounsey, K. E., Dent, J. A., Holt, D. C., McCarthy, J., Currie, B. J., and Walton, S. F. (2007) Molecular characterisation of a pH-gated chloride channel from Sarcoptes scabiei. Invert. Neurosci. 7, 149-156 (Pubitemid 47339786)
34. Brownlee, D. J., Holden-Dye, L., and Walker, R. J. (1997) Actions of the anthelmintic ivermectin on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology 115, 553-561 (Pubitemid 27469661)
35. Wolstenholme, A. J., and Rogers, A. T. (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131, S85-95
36. Bar-Lev, D. D., Degani-Katzav, N., Perelman, A., and Paas, Y. (2011) Molecular dissection of Cl-selective Cys-loop receptor points to components that are dispensable or essential for channel activity. J. Biol. Chem. 286, 43830-43841
37. McKinnon, N. K., Bali, M., and Akabas, M. H. (2012) Length and amino acid sequence of peptides substituted for the 5-HT3A receptor M3M4 loop may affect channel expression and desensitization. PloS ONE 7, e35563
38. Hu, X.-Q., Sun, H., Peoples, R. W., Hong, R., and Zhang, L. (2006) An interaction involving an arginine residue in the cytoplasmic domain of the 5-HT3A receptor contributes to receptor desensitization mechanism. J. Biol. Chem. 281, 21781-21788 (Pubitemid 44181882)
39. O'Toole, K. K., and Jenkins, A. (2011) Discrete M3-M4 intracellular loop subdomains control specific aspects of β-aminobutyric acid type A receptor function. J. Biol. Chem. 286, 37990-37999
40. Millar, N. S. (2008) RIC-3: a nicotinic acetylcholine receptor chaperone: RIC-3: a nicotinic receptor chaperone. Br. J. Pharmacol. 153, S177-S183 (Pubitemid 351341014)
41. Kelley, S. P., Dunlop, J. I., Kirkness, E. F., Lambert, J. J., and Peters, J. A. (2003) A cytoplasmic region determines single-channel conductance in 5-HT3 receptors. Nature 424, 321-324 (Pubitemid 36899374)
42. Kashiwagi, S., Kuraoka, I., Fujiwara, Y., Hitomi, K., Cheng, Q. J., Fuss, J. O., Shin, D. S., Masutani, C., Tainer, J. A., Hanaoka, F., and Iwai, S. (2010) Characterization of a Y-family DNA polymerase eta from the eukaryotic thermophile Alvinella pompejana. J. Nucleic Acids 10.4061/2010/701472
43. Gaill, F., Mann, K., Wiedemann, H., Engel, J., and Timpl, R. (1995) Structural comparison of cuticle and interstitial collagens from annelids living in shallow sea-water and at deep-sea hydrothermal vents. J. Mol. Biol. 246, 284-294
44. Holder, T., Basquin, C., Ebert, J., Randel, N., Jollivet, D., Conti, E., Jékely, G., and Bono, F. (2013) Deep transcriptome-sequencing and proteome analysis of the hydrothermal vent annelid Alvinella pompejana identifies the CvP-bias as a robust measure of eukaryotic thermostability. Biol. Direct 8, 2
45. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010) New algorithms and methods to estimate maximumlikelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321
46. Anisimova, M., and Gascuel, O. (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55, 539-552 (Pubitemid 43922340)
47. Edgar, R. C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 19, 1792-1797 (Pubitemid 38832724)