A knockout mutation of a constitutive GPCR in Tetrahymena decreases both G-protein activity and chemoattraction

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Lampert, Thomas J ^a   Coleman, Kevin D ^a   Hennessey, Todd M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM ION; CHEMOATTRACTANT; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); LYSOPHOSPHATIDIC ACID; PEPTONE; PERTUSSIS TOXIN; POTASSIUM ION; PROTEOSEPEPTONE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMOTAXIS; CONTROLLED STUDY; DNA SEQUENCE; G PROTEIN COUPLED RECEPTOR 6 GENE; GENE INACTIVATION; GENE MUTATION; GENOME ANALYSIS; KNOCKOUT GENE; MICROSOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAMECIUM; PHENOTYPE; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTOZOAL GENETICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TETRAHYMENA THERMOPHILA; WILD TYPE;

AMINO ACID SEQUENCE; CELL LINE; CHEMOTAXIS; ELECTROPHYSIOLOGICAL PHENOMENA; GENE KNOCKOUT TECHNIQUES; GENOME; GTP-BINDING PROTEINS; MICROSOMES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PERTUSSIS TOXIN; PROTOZOAN PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION; TETRAHYMENA;

EID: 82255195437     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028022     Document Type: Article

References (80)

1. Francis JT, Hennessey TM, (1995) Chemorepellents in Paramecium and Tetrahymena. J Eukaryot Microbiol 42: 78-83.
2. Kuruvilla H, Kim M, Hennessey T, (1997) Chemosensory Adaptation to Lysozyme and GTP Involves Independently Regulated Receptors in Tetrahymena thermophila. Euk Microbiol 44 (3): 263-268.
3. Hennessey TM, (2005) Responses of the ciliates Tetrahymena and Paramecium to external ATP and GTP. Purinergic Signal 1: 101-110.
4. Rodgers LF, Markle KL, Hennessey TM, (2008) Responses of the ciliates Tetrahymena and Paramecium to vertebrate odorants and tastants. J Eukaryot Microbiol 55: 27-33.
5. Hellung-Larsen P, Leick V, Tommerup N, (1986) Chemoattraction in Tetrahymena: On the Role of Chemokinesis. Biological Bulletin 170: 357-367.
6. Lampert TJ, Coleman KD, Hennessey TM, (2011) Chemoattraction to lysophosphatidic acid does not require a change in membrane potential in Tetrahymena thermophila. Cell Biol Int 35: 519-528.
7. Leick V, Koppelhus U, Rosenberg J, (1994) Cilia-mediated oriented chemokinesis in Tetrahymena thermophila. J Eukaryot Microbiol 41: 546-553.
8. Koppelhus U, Hellung-Larsen P, Leick V, (2001) A quantitative assay for measurement of chemokinesis in Tetrahymena. Methods Mol Biol 161: 101-106.
9. Bell WE, Preston RR, Yano J, Van Houten JL, (2007) Genetic dissection of attractant-induced conductances in Paramecium. J Exp Biol 210: 357-365.
10. Eckert R, (1972) Bioelectric control of ciliary activity. Science 176: 473-481.
11. Machemer H, (1977) Motor activity and bioelectric control of cilia. Fortschr Zool 24: 195-210.
12. Onimaru H, Ohki K, Nozawa Y, Naitoh Y, (1980) Electrical properties of Tetrahymena, a suitable tool for studies on membrane excitation. Proc Jpn Acad 56: 538-533.
13. Hennessey TM, Kuruvilla HG, (2000) Electrophysiology of Tetrahymena. Methods Cell Biol 62: 363-377.
14. Suwa M, Sugihara M, Ono Y, (2011) Functional and structural overview of G-protein-coupled receptors comprehensively obtained from genome sequences. Pharmaceuticals 4: 652-664.
15. Xue C, Hsueh YP, Heitman J, (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32: 1010-1032.
16. Pierce KL, Premont RT, Lefkowitz RJ, (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3: 639-650.
17. Fredriksson R, Schioth HB, (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67: 1414-1425.
18. Touhara K, Vosshall LB, (2009) Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 71: 307-332.
19. Lemaire K, Van de Velde S, Van Dijck P, Thevelein JM, (2004) Glucose and sucrose act as agonist and mannose as antagonist ligands of the G protein-coupled receptor Gpr1 in the yeast Saccharomyces cerevisiae. Mol Cell 16: 293-299.
20. Welton RM, Hoffman CS, (2000) Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. Genetics 156: 513-521.
21. Johnson RL, Saxe CL 3rd, Gollop R, Kimmel AR, Devreotes PN, (1993) Identification and targeted gene disruption of cAR3, a cAMP receptor subtype expressed during multicellular stages of Dictyostelium development. Genes Dev 7: 273-282.
22. Renaud FL, Colon I, Lebron J, Ortiz N, Rodriguez F, et al. (1995) A novel opioid mechanism seems to modulate phagocytosis in Tetrahymena. J Eukaryot Microbiol 42: 205-207.
23. de Ondarza J, Symington SB, Van Houten JL, Clark JM, (2003) G-protein modulators alter the swimming behavior and calcium influx of Paramecium tetraurelia. J Eukaryot Microbiol 50: 349-355.
24. Marino MJ, Sherman TG, Wood DC, (2001) Partial cloning of putative G-proteins modulating mechanotransduction in the ciliate stentor. J Eukaryot Microbiol 48: 527-536.
25. Fabczak H, Fabczak S, Song PS, Checcucci G, Ghetti F, et al. (1993) Photosensory transduction in ciliates. Role of intracellular pH and comparison between Stentor coeruleus and Blepharisma japonicum. J Photochem Photobiol B 21: 47-52.
26. Dyer M, Day K, (2000) Expression of Plasmodium falciparum trimeric G proteins and their involvement in switching to sexual development. Mol Biochem Parasitol 110: 437-448.
27. Bernal J, Kelsey AM, Ehrlich BE, (1991) GTP-gamma-S increases the duration of backward swimming behavior and the calcium action potential in marine Paramecium. J Exp Biol 155: 505-518.
28. Levoye A, Dam J, Ayoub MA, Guillaume JL, Jockers R, (2006) Do orphan G-protein-coupled receptors have ligand-independent functions? New insights from receptor heterodimers. EMBO Rep 7: 1094-1098.
29. Leurs R, Bakker RB, Casarosa P, Verzijl D, Timmerman H, et al. (2003) Modulation of constitutive GPCR activity: a way of life? International Congress Series 1249: 131-138.
30. Smit MJ, Vischer HF, Bakker RA, Jongejan A, Timmerman H, et al. (2007) Pharmacogenomic and structural analysis of constitutive g protein-coupled receptor activity. Annu Rev Pharmacol Toxicol 47: 53-87.
31. Couty JP, Lupu-Meiri M, Oron Y, Gershengorn MC, (2009) Kaposi's sarcoma-associated herpesvirus-G protein-coupled receptor-expressing endothelial cells exhibit reduced migration and stimulated chemotaxis by chemokine inverse agonists. J Pharmacol Exp Ther 329: 1142-1147.
32. Lunn CA, Reich EP, Fine JS, Lavey B, Kozlowski JA, et al. (2008) Biology and therapeutic potential of cannabinoid CB2 receptor inverse agonists. Br J Pharmacol 153: 226-239.
33. Pandey S, Assmann SM, (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16: 1616-1632.
34. Rohrer DK, Kobilka BK, (1998) G protein-coupled receptors: functional and mechanistic insights through altered gene expression. Physiol Rev 78: 35-52.
35. Cassidy-Hanley D, Bowen J, Lee JH, Cole E, VerPlank LA, et al. (1997) Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146: 135-147.
36. Gaertig J, Gu L, Hai B, Gorovsky MA, (1994) High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res 22: 5391-5398.
37. Terakita A, (2005) The opsins. Genome Biol 6: 213.
38. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, et al. (2007) Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2: e790.
39. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, et al. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455: 497-502.
40. Ji TH, Grossmann M, Ji I, (1998) G protein-coupled receptors. I. Diversity of receptor-ligand interactions. J Biol Chem 273: 17299-17302.
41. Lin WZ, Xiao X, Chou KC, (2009) GPCR-GIA: a web-server for identifying G-protein coupled receptors and their families with grey incidence analysis. Protein Eng Des Sel 22: 699-705.
42. Papasaikas PK, Bagos PG, Litou ZI, Promponas VJ, Hamodrakas SJ, (2004) PRED-GPCR: GPCR recognition and family classification server. Nucleic Acids Res 32: W380-382.
43. Noda K, Saad Y, Graham RM, Karnik SS, (1994) The high affinity state of the beta 2-adrenergic receptor requires unique interaction between conserved and non-conserved extracellular loop cysteines. J Biol Chem 269: 6743-6752.
44. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, et al. (2002) A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci U S A 99: 3734-3739.
45. Saimi Y, Kung C, (1987) Behavioral genetics of Paramecium. Annu Rev Genet 21: 47-65.
46. Schein SJ, (1976) Nonbehavioral selection for pawns, mutants of Paramecium aurelia with decreased excitability. Genetics 84: 453-468.
47. Van Houten J, (1978) Two mechanisms of chemoattraction in Paramecium. J Comp Physiol 127: 167-174.
48. Gronlien HK, Ronnevig AK, Hagen B, Sand O, (2010) Chemo-accumulation without changes in membrane potential in the microstome form of the ciliate Tetrahymena vorax. J Exp Biol 213: 3980-3987.
49. Asano T, Pedersen SE, Scott CW, Ross EM, (1984) Reconstitution of catecholamine-stimulated binding of guanosine 5′-O-(3-thiotriphosphate) to the stimulatory GTP-binding protein of adenylate cyclase. Biochemistry 23: 5460-5467.
50. Ui M, (1990) Pertussis toxin as a valuable probe for G-protein involvement in signal transduction, in ADP-Ribosylating Toxins and G Proteins. American Society for Microbiology, Washington DC 45.
51. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, et al. (2006) Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4: e286.
52. Marinissen MJ, Chiariello M, Gutkind JS, (2001) Regulation of gene expression by the small GTPase Rho through the ERK6 (p38 gamma) MAP kinase pathway. Genes Dev 15: 535-553.
53. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, et al. (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52: 399-451.
54. Risk JM, Day CL, Macknight RC, (2009) Reevaluation of abscisic acid-binding assays shows that G-Protein-Coupled Receptor2 does not bind abscisic Acid. Plant Physiol 150: 6-11.
55. Nilson SE, Assmann SM, (2010) The alpha-subunit of the Arabidopsis heterotrimeric G protein, GPA1, is a regulator of transpiration efficiency. Plant Physiol 152: 2067-2077.
56. Zhang W, Jeon BW, Assmann SM, (2011) Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells. J Exp Bot 62: 2371-2379.
57. Miao W, Xiong J, Bowen J, Wang W, Liu Y, et al. (2009) Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS One 4: e4429.
58. Maidan MM, Thevelein JM, Van Dijck P, (2005) Carbon source induced yeast-to-hypha transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem Soc Trans 33: 291-293.
59. Schenk PW, Epskamp SJ, Knetsch ML, Harten V, Lagendijk EL, et al. (2001) Lysophosphatidic acid- and Gbeta-dependent activation of Dictyostelium MAP kinase ERK2. Biochem Biophys Res Commun 282: 765-772.
60. van Es S, Devreotes PN, (1999) Molecular basis of localized responses during chemotaxis in amoebae and leukocytes. Cell Mol Life Sci 55: 1341-1351.
61. Gudi S, Nolan JP, Frangos JA, (1998) Modulation of GTPase activity of G proteins by fluid shear stress and phospholipid composition. Proc Natl Acad Sci U S A 95: 2515-2519.
62. Seifert R, Wenzel-Seifert K, (2002) Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch Pharmacol 366: 381-416.
63. Tiberi M, Caron MG, (1994) High agonist-independent activity is a distinguishing feature of the dopamine D1B receptor subtype. J Biol Chem 269: 27925-27931.
64. Jones JC, Duffy JW, Machius M, Temple BR, Dohlman HG, et al. (2011) The crystal structure of a self-activating G protein alpha subunit reveals its distinct mechanism of signal initiation. Sci Signal 4: ra8.
65. Hille B, (2001) Ion Channels of Excitable Membranes Sunderland, Massachusetts Sinauer Associates.
66. Takahashi M, (1992) Locus-dependent profiles of the rescue of nonexcitable behavioral mutants during conjugation in Tetrahymena thermophila. Dev Genet 13: 174-179.
67. Sato K, Pellegrino M, Nakagawa T, Vosshall LB, Touhara K, (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452: 1002-1006.
68. Deng Y, Zhang W, Farhat K, Oberland S, Gisselmann G, et al. (2011) The stimulatory Galpha(s) protein is involved in olfactory signal transduction in Drosophila. PLoS One 6: e18605.
69. Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, et al. (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452: 1007-1011.
70. Nakagawa T, Vosshall LB, (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19: 284-292.
71. Adler J, (1987) How motile bacteria sense and respond to chemicals. Ann N Y Acad Sci 510: 95-97.
72. Hanyu N, Kuchino Y, Nishimura S, Beier H, (1986) Dramatic events in ciliate evolution: alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in two Tetrahymena tRNAs. EMBO J 5: 1307-1311.
73. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
74. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2010) Geneious v5.3. wwwgeneiouscom.
75. Hofmann K, Stoffel W, (1993) Tmbase - A database of membrane spanning proteins segments. Biol Chem 347: 166.
76. Claros MG, von Heijne G, (1994) TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10: 685-686.
77. Krogh A, Larsson B, von Heijne G, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
78. Deber CM, Wang C, Liu LP, Prior AS, Agrawal S, et al. (2001) TM Finder: a prediction program for transmembrane protein segments using a combination of hydrophobicity and nonpolar phase helicity scales. Protein Sci 10: 212-219.
79. Hai B, Gorovsky MA, (1997) Germ-line knockout heterokaryons of an essential alpha-tubulin gene enable high-frequency gene replacement and a test of gene transfer from somatic to germ-line nuclei in Tetrahymena thermophila. Proc Natl Acad Sci U S A 94: 1310-1315.
80. Snaar-Jagalska BE, De Wit RJ, Van Haastert PJ, (1988) Pertussis toxin inhibits cAMP surface receptor-stimulated binding of [35S]GTP gamma S to Dictyostelium discoideum membranes. FEBS Lett 232: 148-152.