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. 1994 Jul 5;91(14):6506–6510. doi: 10.1073/pnas.91.14.6506

Structural organization of the Helicoverpa zea gene encoding the precursor protein for pheromone biosynthesis-activating neuropeptide and other neuropeptides.

P W Ma 1, D C Knipple 1, W L Roelofs 1
PMCID: PMC44231  PMID: 8022813

Abstract

Sex pheromone biosynthesis in a number of moth species is induced by a conserved 33-amino acid amidated neuropeptide PBAN (pheromone biosynthesis-activating neuropeptide). We have isolated and characterized the Helicoverpa zea PBAN cDNA corresponding to a 766-nucleotide mRNA that is expressed in the subesophageal ganglion of adult moths. This mRNA is encoded on a transcription unit comprising 6 exons. The longest open reading frame of the cDNA encodes a 194-amino acid precursor protein that contains the PBAN peptide sequence. Proteolytic processing of this protein, which has structural features consistent with its being a preprohormone, is predicted to generate Hez-PBAN and four additional neuropeptides having a common C-terminal pentapeptide motif, Phe-Xaa-Pro-(Arg or Lys)-Leu (Xaa = Gly, Ser, or Thr), which is also found in insect pyrokinin and myotropin peptide families.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bradfield J. Y., Keeley L. L. Adipokinetic hormone gene sequence from Manduca sexta. J Biol Chem. 1989 Aug 5;264(22):12791–12793. [PubMed] [Google Scholar]
  2. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  4. Darby N. J., Smyth D. G. Endopeptidases and prohormone processing. Biosci Rep. 1990 Feb;10(1):1–13. doi: 10.1007/BF01116845. [DOI] [PubMed] [Google Scholar]
  5. Davis M. T., Vakharia V. N., Henry J., Kempe T. G., Raina A. K. Molecular cloning of the pheromone biosynthesis-activating neuropeptide in Helicoverpa zea. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):142–146. doi: 10.1073/pnas.89.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Edwards J. B., Delort J., Mallet J. Oligodeoxyribonucleotide ligation to single-stranded cDNAs: a new tool for cloning 5' ends of mRNAs and for constructing cDNA libraries by in vitro amplification. Nucleic Acids Res. 1991 Oct 11;19(19):5227–5232. doi: 10.1093/nar/19.19.5227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engler-Blum G., Meier M., Frank J., Müller G. A. Reduction of background problems in nonradioactive northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations. Anal Biochem. 1993 May 1;210(2):235–244. doi: 10.1006/abio.1993.1189. [DOI] [PubMed] [Google Scholar]
  8. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Harvey R. J., Vreugdenhil E., Zaman S. H., Bhandal N. S., Usherwood P. N., Barnard E. A., Darlison M. G. Sequence of a functional invertebrate GABAA receptor subunit which can form a chimeric receptor with a vertebrate alpha subunit. EMBO J. 1991 Nov;10(11):3239–3245. doi: 10.1002/j.1460-2075.1991.tb04887.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kawakami A., Kataoka H., Oka T., Mizoguchi A., Kimura-Kawakami M., Adachi T., Iwami M., Nagasawa H., Suzuki A., Ishizaki H. Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science. 1990 Mar 16;247(4948):1333–1335. doi: 10.1126/science.2315701. [DOI] [PubMed] [Google Scholar]
  11. Kawano T., Kataoka H., Nagasawa H., Isogai A., Suzuki A. cDNA cloning and sequence determination of the pheromone biosynthesis activating neuropeptide of the silkworm, Bombyx mori. Biochem Biophys Res Commun. 1992 Nov 30;189(1):221–226. doi: 10.1016/0006-291x(92)91547-4. [DOI] [PubMed] [Google Scholar]
  12. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res. 1985 Jul 11;13(13):4971–4981. doi: 10.1093/nar/13.13.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kitamura A., Nagasawa H., Kataoka H., Ando T., Suzuki A. Amino acid sequence of pheromone biosynthesis activating neuropeptide-II (PBAN-II) of the silkmoth, Bombyx mori. Agric Biol Chem. 1990 Sep;54(9):2495–2497. [PubMed] [Google Scholar]
  14. Kitamura A., Nagasawa H., Kataoka H., Inoue T., Matsumoto S., Ando T., Suzuki A. Amino acid sequence of pheromone-biosynthesis-activating neuropeptide (PBAN) of the silkworm, Bombyx mori. Biochem Biophys Res Commun. 1989 Aug 30;163(1):520–526. doi: 10.1016/0006-291x(89)92168-2. [DOI] [PubMed] [Google Scholar]
  15. Matsumoto S., Fónagy A., Kurihara M., Uchiumi K., Nagamine T., Chijimatsu M., Mitsui T. Isolation and primary structure of a novel pheromonotropic neuropeptide structurally related to leucopyrokinin from the armyworm larvae, Pseudaletia separata. Biochem Biophys Res Commun. 1992 Jan 31;182(2):534–539. doi: 10.1016/0006-291x(92)91765-i. [DOI] [PubMed] [Google Scholar]
  16. Nambu J. R., Murphy-Erdosh C., Andrews P. C., Feistner G. J., Scheller R. H. Isolation and characterization of a Drosophila neuropeptide gene. Neuron. 1988 Mar;1(1):55–61. doi: 10.1016/0896-6273(88)90209-7. [DOI] [PubMed] [Google Scholar]
  17. Nichols R., Schneuwly S. A., Dixon J. E. Identification and characterization of a Drosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem. 1988 Sep 5;263(25):12167–12170. [PubMed] [Google Scholar]
  18. Noyes B. E., Schaffer M. H. The structurally similar neuropeptides adipokinetic hormone I and II are derived from similar, very small mRNAs. J Biol Chem. 1990 Jan 5;265(1):483–489. [PubMed] [Google Scholar]
  19. Padgett R. A., Grabowski P. J., Konarska M. M., Seiler S., Sharp P. A. Splicing of messenger RNA precursors. Annu Rev Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  20. Raina A. K., Jaffe H., Kempe T. G., Keim P., Blacher R. W., Fales H. M., Riley C. T., Klun J. A., Ridgway R. L., Hayes D. K. Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science. 1989 May 19;244(4906):796–798. doi: 10.1126/science.244.4906.796. [DOI] [PubMed] [Google Scholar]
  21. Raina A. K. Neuroendocrine control of sex pheromone biosynthesis in Lepidoptera. Annu Rev Entomol. 1993;38:329–349. doi: 10.1146/annurev.en.38.010193.001553. [DOI] [PubMed] [Google Scholar]
  22. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  23. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sato Y., Oguchi M., Menjo N., Imai K., Saito H., Ikeda M., Isobe M., Yamashita O. Precursor polyprotein for multiple neuropeptides secreted from the suboesophageal ganglion of the silkworm Bombyx mori: characterization of the cDNA encoding the diapause hormone precursor and identification of additional peptides. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3251–3255. doi: 10.1073/pnas.90.8.3251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schneider L. E., Taghert P. H. Isolation and characterization of a Drosophila gene that encodes multiple neuropeptides related to Phe-Met-Arg-Phe-NH2 (FMRFamide). Proc Natl Acad Sci U S A. 1988 Mar;85(6):1993–1997. doi: 10.1073/pnas.85.6.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schoofs L., Vanden Broeck J., De Loof A. The myotropic peptides of Locusta migratoria: structures, distribution, functions and receptors. Insect Biochem Mol Biol. 1993 Dec;23(8):859–881. doi: 10.1016/0965-1748(93)90104-z. [DOI] [PubMed] [Google Scholar]
  27. Schulz-Aellen M. F., Roulet E., Fischer-Lougheed J., O'Shea M. Synthesis of a homodimer neurohormone precursor of locust adipokinetic hormone studied by in vitro translation and cDNA cloning. Neuron. 1989 Apr;2(4):1369–1373. doi: 10.1016/0896-6273(89)90075-5. [DOI] [PubMed] [Google Scholar]
  28. Tessier D. C., Brousseau R., Vernet T. Ligation of single-stranded oligodeoxyribonucleotides by T4 RNA ligase. Anal Biochem. 1986 Oct;158(1):171–178. doi: 10.1016/0003-2697(86)90606-8. [DOI] [PubMed] [Google Scholar]
  29. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wahle E., Keller W. The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev Biochem. 1992;61:419–440. doi: 10.1146/annurev.bi.61.070192.002223. [DOI] [PubMed] [Google Scholar]
  31. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]
  32. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

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