Isolation and functional characterization of an allatotropin receptor from manduca sexta

Insect Biochemistry and Molecular Biology

Volumn 41, Issue 10, 2011, Pages 804-814

  Horodyski, Frank M ^a   Verlinden, Heleen ^b   Filkin, Nanda ^a   Vandersmissen, Hans Peter ^b   Fleury, Christophe ^c   Reynolds, Stuart E ^c   Kai, Zhen peng ^a   Broeck, Jozef Vanden ^b  

^a OHIO UNIVERSITY   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c University of Bath   (United Kingdom)

Author keywords

Allatotropin; G protein coupled receptors; Juvenile hormone; Manduca sexta; Neuropeptides

Indexed keywords

ALLATOTROPIN; CALCIUM; COMPLEMENTARY DNA; CYCLIC AMP; INSECT HORMONE; INSECT PROTEIN; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CALCIUM SIGNALING; CHEMISTRY; CHO CELL; CRICETULUS; FEMALE; HAMSTER; ISOLATION AND PURIFICATION; LEPIDOPTERA; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CALCIUM; CALCIUM SIGNALING; CHO CELLS; CRICETINAE; CRICETULUS; CYCLIC AMP; DNA, COMPLEMENTARY; FEMALE; INSECT HORMONES; INSECT PROTEINS; MALE; MANDUCA; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; RECEPTORS, NEUROPEPTIDE;

BOMBYX MORI; HEXAPODA; INVERTEBRATA; MAMMALIA; MANDUCA SEXTA; VERTEBRATA;

EID: 80051826381     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2011.06.002     Document Type: Article

References (67)

1. Abdel-latief M., Hoffmann K.H. Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae). Arch. Insect Biochem. Physiol. 2010, 74:135-146.
2. Abdel-latief M., Meyering-Vos M., Hoffmann K.H. Molecular characterization of cDNAs from the fall armyworm Spodoptera frugiperda encoding Manduca sexta allatotropin and allatostatin preprohormone peptides. Insect Biochem. Mol. Biol. 2003, 33:467-476.
3. Allen C.U., Herman B., Granger N.A. Fura-2 measurement of cytosolic free Ca2+ concentration in corpus allatum cells of larval Manduca sexta. J. Exp. Biol. 1992, 166:253-266.
4. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.L. Gapped BLAST and PHI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 29:3389-3402.
5. Amare A., Sweedler J.V. Neuropeptide precursors in Tribolium castaneum. Peptides 2007, 28:1282-1291.
6. Audsley N., Weaver R.J., Edwards J.P. Juvenile hormone biosynthesis by corpora allata of larval tomato moth, Lacanobia oleracea, and regulation by Manduca sexta allatostatin and allatotropin. Insect Biochem. Mol. Biol. 2000, 30:681-689.
7. Bell R.A., Joachim F.A. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann. Entomol. Soc. Am. 1976, 69:365-373.
8. Don R.H., Cox P.T., Wainwright B.J., Baker K., Mattick J.S. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 1991, 19:4008.
9. Duve H., Audsley N., Weaver R.J., Thorpe A. Triple co-localization of two types of allatostatin and an allatotropin in the frontal ganglion of the lepidopteran Lacanobia oleracea (Noctuidae): innervation and action on the foregut. Cell Tissue Res. 2000, 300:153-163.
10. Duve H., East P.D., Thorpe A. Regulation of lepidopteran foregut movement by allatostatins and allatotropin from the frontal ganglion. J. Comp. Neurol. 1999, 413:405-416.
11. Elekonich M.M., Horodyski F.M. Insect allatotropins belong to a family of structurally-related myoactive peptides present in several invertebrate phyla. Peptides 2003, 24:1623-1632.
12. Glasscock J.M., Mizoguchi A., Rachinsky A. Immunocytochemical localization of an allatotropin in developmental stages of Heliothis virescens and Apis mellifera. J. Insect Physiol. 2005, 51:345-355.
13. Harada A., Yoshida M., Minakata H., Nomoto K., Muneoka Y., Kobayashi M. Structure and function of the molluscan myoactive tetradecapeptides. Zool. Sci. 1993, 10:257-265.
14. Hauser F., Neupert S., Williamson M., Predel R., Tanaka Y., Grimmelikhuijzen C.J.P. Genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp Nasonia vitripennis. J. Proteome Res. 2010, 9:5296-5310.
15. Hewes R.S., Taghert P.H. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 2001, 11:1126-1142.
16. Horodyski F.M., Bhatt S.R., Lee K.-Y. Alternative splicing of transcripts expressed by the Manduca sexta allatotropin (Mas-AT) gene is regulated in a tissue-specific manner. Peptides 2001, 22:263-269.
17. Hummon A.B., Richmond T.A., Verleyen P., Baggerman G., Huybrechts J., Ewing M.A., Vierstraete E., Rodriguez-Zas S.L., Schoofs L., Robinson G.E., Sweedler J.V. From the genome to the proteome: uncovering peptides in the Apis brain. Science 2006, 314:647-649.
18. Jiang H., Wang Y., Kanost M.R. Primary structure of ribosomal proteins S3 and S7 from Manduca sexta. Insect Mol. Biol. 1996, 5:31-38.
19. Kataoka H., Toschi A., Li J.P., Carney R.L., Schooley D.A., Kramer S.J. Identification of an allatotropin from adult Manduca sexta. Science 1989, 243:1481-1483.
20. Kingan T.G., Shabanowitz J., Hunt D.F., Witten J.L. Characterization of two myotropic neuropeptides in the FMRFamide family from segmental ganglia of the moth Manduca sexta: candidate neurohormones and neuromodulators. J. Exp. Biol. 1996, 199:1095-1104.
21. Koladich P.M., Tobe S.S., McNeil J.N. Enhanced haemolymph circulation by insect ventral nerve cord: hormonal control by Pseudaletia unipuncta allatotropin and serotonin. J. Exp. Biol. 2002, 205:3123-3131.
22. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
23. Kumar S., Dudley J., Nei M., Tamura K. Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
24. Lee K.-Y., Chamberlin M.E., Horodyski F.M. Biological activity of Manduca sexta allatotropin-like peptides, predicted products of tissue-specific and developmentally-regulated alternatively spliced mRNAs. Peptides 2002, 23:1933-1941.
25. Lee K.-Y., Horodyski F.M., Chamberlin M.E. Inhibition of midgut ion transport by allatotropin (Mas-AT) and Manduca FLRFamide peptides in the tobacco hornworm, Manduca sexta. J. Exp. Biol. 1998, 201:3067-3074.
26. Li B., Predel R., Neupert S., Hauser F., Tanaka Y., Cazzamali G., Williamson M., Arakane Y., Verleyen P., Schoofs L., Schachtner J., Grimmelikhuijzen C.J.P., Park Y. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res. 2008, 18:113-122.
27. Li K.W., Holling T., de With N.D., Geraerts W.P.M. Purification and characterization of a novel tetradecapeptide that modulates oesophagus motility in Lymnaea stagnalis. Biochem. Biophys. Res. Commun. 1993, 197:1056-1061.
28. Li S., Jiang R.-J., Cao M.-X. Allatotropic and allatostatic activities in extracts of brain and the effects of Manduca sexta allatotropin and Manduca sexta allatostatin on juvenile hormone synthesis in vitro by corpora allata from the Eri silkworm, Samia cynthia ricini. Physiol. Entomol. 2002, 27:322-329.
29. Li Y., Unnithan G.C., Veenstra J.A., Feyereisen R., Noriega F.G. Stimulation of JH biosynthesis by the corpora allata of adult female Aedes aegypti in vitro: effect of farnesoic acid and Aedes allatotropin. J. Exp. Biol. 2003, 206:1825-1832.
30. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 2001, 25:402-408.
31. Paemen L., Tips A., Schoofs L., Proost P., VanDamme J., DeLoof A. Lom-AG-myotropin: a novel myotropic peptide from the male accessory glands of Locusta migratoria. Peptides 1991, 12:7-10.
32. Petri B., Homberg U., Loesel R., Stengl M. Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J. Exp. Biol. 2002, 205:1459-1469.
33. Price D.A., Greenberg M.J. Structure of a molluscan cardioexcitatory neuropeptide. Science 1977, 197:670-671.
34. Rachinsky A., Feldlaufer M.F. Responsiveness of honey bee (Apis mellifera L.) corpora allata to allatoregulatory peptides from four insect species. J. Insect Physiol. 2000, 46:41-46.
35. Rachinsky A., Srinivasan A., Ramaswamy S.B. Regulation of juvenile hormone biosynthesis in Heliothis virescens by Manduca sexta allatotropin. Arch. Insect Biochem. Physiol. 2003, 54:121-133.
36. Rachinsky A., Tobe S.S. Role of second messengers in the regulation of juvenile hormone production in insects, with particular emphasis on calcium and phosphoinositide signaling. Arch. Insect Biochem. Physiol. 1996, 33:259-282.
37. Rankin S.M., Kwok R., Seymour M.L., Rahman U.S., Tobe S.S. Effects of Manduca allatotropin and localization of Manduca allatotropin-immunoreactive cells in earwigs. Comp. Biochem. Physiol. 2005, 142B:113-122.
38. Reagan J.D., Miller W.H., Kramer S.J. Allatotropin-induced formation of inositol phosphates in the corpora allata of the moth, Manduca sexta. Arch. Insect Biochem. Physiol. 1992, 20:145-155.
39. Reese M.G., Eeckman F.H., Kulp D., Haussler D. Improved splice site detection in genie. J. Comput. Biol. 1997, 4:311-323.
40. Riddiford L.M. Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv. In Insect Phys. 1994, 24:213-274.
41. Riddiford L.M., Curtis A.T., Kiguchi K. Culture of the epidermis of the tobacco hornworm, Manduca sexta. Tissue Cult. Assoc. Man. 1979, 5:975-985.
42. Riehle M.A., Garczynski S.F., Crim J.W., Hill C.A., Brown M.R. Neuropeptides and peptide hormones in Anopheles gambiae. Science 2002, 298:172-175.
43. Rudwall A.J., Sliwowska J., Nässel D.R. Allatotropin-like neuropeptide in the cockroach abdominal nervous system: myotropic actions, sexually dimorphic distribution and colocalization with serotonin. J. Comp. Neurol. 2000, 428:159-173.
44. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richardson J.A., Kozlowski G.P., Wilson S., Arch J.R.S., Buckingham R.E., Haynes A.C., Carr S.A., Annan R.S., McNulty D.E., Liu W.-S., Terrett J.A., Elshourbagy N.A., Bergsma D.J., Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
45. Santini M.S., Ronderos J.R. Allatotropin-like peptide released by Malpighian tubules induces hindgut activity associated with diuresis in the Chagas disease vector Triatoma infestans (Klug). J. Exp. Biol. 2007, 210:1986-1991.
46. Schwartz L.M., Truman J.W. Hormonal control of rates of metamorphic development in the tobacco hornworm Manduca sexta. Dev. Biol. 1983, 99:103-114.
47. Sheng Z., Ma L., Cao M.-X., Li S., Jiang R.-J. Biochemical and molecular characterization of allatotropin and allatostatin from the Eri silkworm, Samia cynthia ricini. Insect Biochem. Mol. Biol. 2007, 37:90-96.
48. Spittaels K., Vankeerberghen A., Schoofs L., Proost P., Van Damme J., DeLoof A. Isolation and characterization of Locusta migratoria accessory gland myotropin I (Lom-AG-MT-1) from the brain of the Colorado potato beetle. Arch. Insect Biochem. Physiol. 1996, 31:149-155.
49. Stables J., Green A., Marshall F., Fraser N., Knight E., Sautel M., Milligan G., Lee M., Rees S. A bioluminescent assay for agonist activity at potentially any G-protein-coupled receptor. Anal. Biochem. 1997, 252:115-126.
50. Stangier J., Hilbich C., Beyreuther K., Keller R. Unusual cardioactive peptide (CCAP) from pericardial organs of the shore crab Carcinus maenas. Proc. Nat. Acad. Sci. U. S. A. 1987, 84:575-579.
51. Taylor P.A., Bhatt T.R., Horodyski F.M. Molecular characterization and expression analysis of Manduca sexta allatotropin. Eur. J. Biochem. 1996, 239:588-596.
52. Tu M.-P., Kou R., Wang Z.-S., Stoffolano J.G., Yin C.-M. Immunolocalization and possible effect of a moth allatotropin-like substance in a fly, Phormia regina (Diptera: Calliphoridae). J. Insect Physiol. 2001, 47:233-244.
53. Ukena K., Oumi T., Matsushima O., Ikeda T., Fujita T., Minakata H., Nomoto K. A novel gut tetradecapeptide isolated from the earthworm, Eisenia foetida. Peptides 1995, 16:995-999.
54. Vanden Broeck J. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 2001, 22:241-254.
55. Veenstra J.A. Isolation and structure of corazonin, a cardioactive peptide from the American cockroach. FEBS Lett. 1989, 250:231-234.
56. Veenstra J.A., Costes L. Isolation and identification of a peptide and its cDNA from the mosquito Aedes aegypti related to Manduca sexta allatotropin. Peptides 1999, 20:1145-1151.
57. Veenstra J.A., Lehman H.K., Davis N.T. Allatotropin is a cardioacceleratory peptide in Manduca sexta. J. Exp. Biol. 1994, 188:347-354.
58. Voisin T., Rouet-Benzineb P., Reuter N., Laburthe M. Orexins and their receptors: structural aspects and role in peripheral tissues. Cell. Mol. Life Sci. 2003, 60:72-87.
59. Weaver R.J., Audsley N. Neuropeptides of the beetle, Tenebrio molitor identified using MALDI-TOF mass spectrometry and deduced sequences from the Tribolium castaneum genome. Peptides 2008, 29:168-178.
60. Weaver R.J., Audsley N. Neuropeptide regulators of juvenile hormone synthesis. Ann. N. Y. Acad. Sci. 2009, 1163:316-329.
61. Wyatt G.R., Davey K.G. Cell and molecular actions of juvenile hormone II. Roles of juvenile hormone in adult insects. Adv. In Insect Phys. 1996, 26:1-155.
62. Yamanaka N., Hua Y.-J., Mizoguchi A., Watanabe K., Niwa R., Tanaka Y., Kataoka H. Identification of a novel prothoracicostatic hormone and its receptor in the silkworm, Bombyx mori. J. Biol. Chem. 2005, 280:14684-14690.
63. Yamanaka N., Yamamoto S., Zitnan D., Watanabe K., Kawada T., Satake H., Hiruma K., Tanaka Y., Shinoda T., Kataoka H. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE 2008, 3:e3048.
64. Yi S.-X., Adams T.S. Age- and diapause-related acid and alkaline phosphatase activities in the intestine and Malpighian tubules of the Colorado potato beetle Leptinotarsa decemlineata (Say). Arch. Insect Biochem. Physiol. 2001, 46:152-163.
65. Yin H., Zhang T.-Y., Xu W.-H. Structural organization and expression analysis of the cDNA encoding allatotropin in the cotton bollworm, Helicoverpa armigera. Arch. Insect Biochem. Physiol. 2005, 60:71-83.
66. Ziegler R., Eckert K., Schwarz H., Keller R. Amino acid sequence of Manduca sexta adipokinetic hormone elucidated by combined fast atom bombardment/tandem mass spectrometry. Biochem. Biophys. Res. Commun. 1985, 133:337-342.
67. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.