Gα encoding gene family of the malaria vector mosquito Anopheles gambiae: Expression analysis and immunolocalization of AG αq and AGαo in female antennae

Journal of Comparative Neurology

Volumn 499, Issue 4, 2006, Pages 533-545

  Rützler, Michael ^a   Lu, Tan ^a   Zwiebel, Laurence J ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

G protein; Insect; Olfaction; RT PCR

Indexed keywords

G PROTEIN ALPHA O; G PROTEIN ALPHA Q; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; ISOPROTEIN; PROTEIN SUBUNIT; RECEPTOR; UNCLASSIFIED DRUG;

AGA GENE; ANIMAL TISSUE; ANOPHELES GAMBIAE; ANTENNA; ARTICLE; DEVELOPMENTAL STAGE; DISEASE CARRIER; FEMALE; GENE; GENE EXPRESSION; GENOME; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; MALARIA; MOSQUITO; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; ODOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; BRAIN; COMPARATIVE STUDY; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MECHANOTRANSDUCTION; METABOLISM; MOLECULAR GENETICS; OLFACTORY RECEPTOR; PHYLOGENY; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIBRISSA; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; BLOTTING, WESTERN; BRAIN; DROSOPHILA MELANOGASTER; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GTP-BINDING PROTEIN ALPHA SUBUNITS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MECHANOTRANSDUCTION, CELLULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN ISOFORMS; RECEPTORS, ODORANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIBRISSAE;

EID: 33750220493     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21083     Document Type: Article

References (63)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410.
2. Boekhoff I, Raming K, Breer H. 1990. Pheromone-induced stimulation of inositol-trisphosphate formation in insect antennae is mediated by G-proteins. J Comp Physiol B 160:99-103.
3. Boo KS. 1980. Fine structure of the antennal sensory hairs in female Anopheles stephensi. Zeit Parasitenkunde (Parasitology Research) 61:161-171.
4. Breer H, Boekhoff I, Tareilus E. 1990. Rapid kinetics of second messenger formation in olfactory transduction. Nature 345:65-68.
5. Chyb S, Dahanukar A, Wickens A, Carlson JR. 2003. Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci U S A 100(Suppl 2):14526-14530.
6. Clements AN. 1999. The biology of mosquitoes. New York: CABI Publishing.
7. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-338.
8. Conklin BR, Bourne HR. 1993. Structural elements of G-alpha subunits that interact with G-beta-gamma, receptors, and effectors. Cell 73:631-641.
9. Conklin BR, Farfel Z, Lustig KD, Julius D, Bourne HR. 1993. Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha. Nature 363:274-276.
10. Dahanukar A, Hallem EA, Carlson JR. 2005. Insect chemoreception. Curr Opin Neurobiol 15:423-430.
11. de Sousa SM, Hoveland LL, Yarfitz S, Hurley JB. 1989. The Drosophila Go alpha-like G protein gene produces multiple transcripts and is expressed in the nervous system and in ovaries. J Biol Chem 264:18544-18551.
12. Dobritsa AA, van der Goes van Naters W, Warr CG, Steinbrecht RA, Carlson JR. 2003. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37:827-841.
13. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ. 2001. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc Natl Acad Sci U S A 98:14693-14697.
14. Gao Q, Chess A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31-39.
15. Goldman AL, Van der Goes van Naters W, Lessing D, Warr CG, Carlson JR. 2005. Coexpression of two functional odor receptors in one neuron. Neuron 45:661-666.
16. Hallem E, Ho MG, Carlson JR. 2004a. The molecular basis of odor coding in the Drosophila antenna. Cell 117:965-979.
17. Hallem EA, Nicole Fox A, Zwiebel LJ, Carlson JR. 2004b. Olfaction: mosquito receptor for human-sweat odorant. Nature 427:212-213.
18. Hamm HE, Deretic D, Arendt A, Hargrave PA, Koenig B, Hofmann KP. 1988. Site of G protein binding to rhodopsin mapped with synthetic peptides from the alpha subunit. Science 241:832-835.
19. Hart MJ, Jiang X, Kozasa T, Roscoe W, Singer WD, Gilman AG, Sternweis PC, Bollag G. 1998. Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science 280:2112-2114.
20. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ. 2002. G protein-coupled receptors in Anopheles gambiae. Science 298:176-178.
21. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chatuverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL. 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129-149.
22. Jacquin-Joly E, Francois MC, Burnet M, Lucas P, Bourrat F, Maida R. 2002. Expression pattern in the antennae of a newly isolated lepidopteran Gq protein alpha subunit cDNA. Eur J Biochem 269:2133-2142.
23. Jones DT, Reed RR. 1989. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244:790-795.
24. Kenakin T. 1995. Agonist-receptor efficacy. I. Mechanisms of efficacy and receptor promiscuity. Trends Pharmacol Sci 16:188-192.
25. Kenakin T. 2003. Ligand-selective receptor conformations revisited: the promise and the problem. Trends Pharmacol Sci 24:346-354.
26. Kreher SA, Kwon JY, Carlson JR. 2005. The molecular basis of odor coding in the Drosophila larva. Neuron 46:445-456.
27. Krieger J, Breer H. 1999. Olfactory reception in invertebrates. Science 286:720-723.
28. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Laue M, Maida R, Redkozubov A. 1997. G-protein activation, identification and immunolocalization in pheromone-sensitive sensilla trichodea of moths. Cell Tissue Res 288:149-158.
30. Lee YJ, Dobbs MB, Verardi ML, Hyde DR. 1990. dgq: a Drosophila gene encoding a visual system-specific G alpha molecule. Neuron 5:889-898.
31. Lopez I, Mak EC, Ding J, Hamm HE, Lomasney JW. 2001. A novel bifunctional phospholipase c that is regulated by Galpha 12 and stimulates the Ras/mitogen-activated protein kinase pathway. J Biol Chem 276:2758-2765.
32. Markby DW, Onrust R, Bourne HR. 1993. Separate GTP binding and GTPase activating domains of a G alpha subunit. Science 262:1895-1901.
33. McIver SB. 1972. Fine structure of pegs on the palps of female culicine mosquitoes. Can J Zool 50:571-576.
34. McIver SB. 1982. Sensilla mosquitoes (Diptera: Culicidae). J Med Entomol 19:489-535.
35. Miura N, Atsumi S, Tabunoki H, Sato R. 2005. Expression and localization of three G protein alpha subunits, Go, Gq, and Gs, in adult antennae of the silkmoth (Bombyx mori). J Comp Neurol 485:143-152.
36. Nakagawa T, Sakurai T, Nishioka T, Touhara K. 2005. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638-1642.
37. Neuhaus EM, Gisselmann G, Zhang W, Dooley R, Stortkuhl K, Hatt H. 2005. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 8:15-17.
38. Neves SR, Ram PT, Iyengar R. 2002. G protein pathways. Science 296:1636-1639.
39. Niu J, Vaiskunaite R, Suzuki N, Kozasa T, Carr DW, Dulin N, Voyno-Yasenetskaya TA. 2001. Interaction of heterotrimeric G13 protein with an A-kinase-anchoring protein 110 (AKAP110) mediates cAMP-independent PKA activation. Curr Biol 11:1686-1690.
40. Parks S, Wieschaus E. 1991. The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell 64:447-458.
41. Quan F, Forte MA. 1990. Two forms of Drosophila melanogaster Gs alpha are produced by alternate splicing involving an unusual splice site. Mol Cell Biol 10:910-917.
42. Quan F, Wolfgang WJ, Forte M. 1993. A Drosophila G-protein alpha subunit, Gf alpha, expressed in a spatially and temporally restricted pattern during Drosophila development. Proc Natl Acad Sci U S A 90:4236-4240.
43. Ratnaparkhi A, Banerjee S, Hasan G. 2002. Altered levels of Gq activity modulate axonal pathfinding in Drosophila. J Neurosci 22:4499-4508.
44. Riesgo-Escovar J, Raha D, Carlson JR. 1995. Requirement for a phospholipase C in odor response: overlap between olfaction and vision in Drosophila. Proc Natl Acad Sci U S A 92:2864-2868.
45. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
46. Rutzler M, Zwiebel L. 2005. Molecular biology of insect olfaction: recent progress and conceptual models. J Comp Physiol A Neuroethol Sens Neural Behav Physiol:1-14.
47. Sakurai T, Nakagawa T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T. 2004. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci U S A 101:16653-16658.
48. Salazar CE, Mills-Hamm D, Kumar V, Collins FH. 1993. Sequence of a cDNA from the mosquito Anopheles gambiae encoding a homolog of human ribosomal protein S7. Nucleic Acids Res 21:4147.
49. Schaefer M, Petronczki M, Dorner D, Forte M, Knoblich JA. 2001. Heterotrimeric G proteins direct two modes of asymmetric cell division in the Drosophila nervous system. Cell 107:183-194.
50. Scott K, Becker A, Sun Y, Hardy R, Zuker C. 1995. Gq alpha protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 15:919-927.
51. Shirokova E, Schmiedeberg K, Bedner P, Niessen H, Willecke K, Raguse JD, Meyerhof W, Krautwurst D. 2005. Identification of specific ligands for orphan olfactory receptors. G protein-dependent agonism and antagonism of odorants. J Biol Chem 280(12):11807-11815.
52. Strathmann MP, Simon MI. 1991. G alpha 12 and G alpha 13 subunits define a fourth class of G protein alpha subunits. Proc Natl Acad Sci U S A 88:5582-5586.
53. Sun B, Salvaterra PM. 1995. Characterization of Nervana, a Drosophila melanogaster neuron-specific glycoprotein antigen recognized by anti-horseradish peroxidase antibodies. J Neurochem 65:434-443.
54. Suzuki N, Nakamura S, Mano H, Kozasa T. 2003. Galpha 12 activates Rho GTPase through tyrosine-phosphorylated leukemia-associated Rho-GEF. Proc Natl Acad Sci U S A 100:733-738.
55. Swofford DL. 1998. PAUP*. Phylogenetic analysis using parsimony (*and other methods), v. 4. New York: Sinauer Press.
56. Talluri S, Bhatt A, Smith DP. 1995. Identification of a Drosophila G protein alpha subunit (dGq alpha-3) expressed in chemosensory cells and central neurons. Proc Natl Acad Sci U S A 92:11475-11479.
57. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
58. Wolfgang WJ, Quan F, Goldsmith P, Unson C, Spiegel A, Forte M. 1990. Immunolocalization of G protein alpha-subunits in the Drosophila CNS. J Neurosci 10:1014-1024.
59. Yamaguchi Y, Katoh H, Mori K, Negishi M. 2002. Galpha(12) and Galpha(13) interact with Ser/Thr protein phosphatase type 5 and stimulate its phosphatase activity. Curr Biol 12:1353-1358.
60. Yoon J, Shortridge RD, Bloomquist BT, Schneuwly S, Perdew MH, Pak WL. 1989. Molecular characterization of Drosophila gene encoding G0 alpha subunit homolog. J Biol Chem 264:18536-18543.
61. Zhu D, Kosik KS, Meigs TE, Yanamadala V, Denker BM. 2004. Galpha12 directly interacts with PP2A: evidence FOR Galpha12-stimulated PP2A phosphatase activity and dephosphorylation of microtubule-associated protein, tau. J Biol Chem 279:54983-54986.
62. Zwaal RR, Mendel JE, Sternberg PW, Plasterk RH. 1997. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics 145:715-727.
63. Zwiebel LJ, Takken W. 2004. Olfactory regulation of mosquito-host interactions. Insect Biochem Mol Biol 34:645-652.