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PBAN/pyrokinin peptides in the central nervous system of the fire ant, Solenopsis invicta

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Abstract

The pyrokinin/pheromone-biosynthesis-activating neuropeptide (PBAN) family of peptides found in insects is characterized by a 5-amino-acid C-terminal sequence, FXPRLamide. The pentapeptide is the active core required for diverse physiological functions, including the stimulation of pheromone biosynthesis in female moths, muscle contraction, induction of embryonic diapause, melanization, acceleration of puparium formation, and termination of pupal diapause. We have used immunocytochemical techniques to demonstrate the presence of pyrokinin/PBAN-like peptides in the central nervous system of the fire ant, Solenopsis invicta. Polyclonal antisera against the C-terminal end of PBAN have revealed the location of the peptide-producing cell bodies and axons in the central nervous system. Immunoreactive material is detectable in at least three groups of neurons in the subesophageal ganglion and corpora cardiaca of all adult sexual forms. The ventral nerve cord of adults consists of two segmented thoracic ganglia and four segmented abdominal ganglia. Two immunoreactive pairs of neurons are present in the thoracic ganglia, and three neuron pairs in each of the first three abdominal ganglia. The terminal abdominal ganglion has no immunoreactive neurons. PBAN immunoreactive material found in abdominal neurons appears to be projected to perisympathetic organs connected to the abdominal ganglia. These results indicate that the fire ant nervous system contains pyrokinin/PBAN-like peptides, and that these peptides are released into the hemolymph. In support of our immunocytochemical results, significant pheromonotropic activity is found in fire ant brain-subesophageal ganglion extracts from all adult fire ant forms (queens, female and male alates, and workers) when extracts are injected into decapitated females of Helicoverpa zea. This is the first demonstration of the presence of pyrokinin/PBAN-like peptides and pheromonotropic activity in an ant species.

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References

  • Banks WA, Lofgren CS, Jouvenaz DP, Stringer CE, Bishop PM, Williams DF, Wojcik DP, Glancey BM (1981) Techniques for collecting, rearing, and handling imported fire ants. USDA, SEA AATS-S-21:9

    Google Scholar 

  • Blackburn MB, Kingan TG, Raina AK, Ma MC (1992) Colocalization and differential expression of PBAN- and FMRFamide-like immunoreactivity in the subesophageal ganglion of Helicoverpa zea (Lepidoptera: Noctuidae) during development. Arch Insect Biochem Physiol 21:225–238

    Article  CAS  Google Scholar 

  • Choi M-Y, Tatsuki S, Boo KS (1998) Regulation of sex pheromone biosynthesis in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). J Insect Physiol 44:653–658

    Article  CAS  Google Scholar 

  • Choi M-Y, Rafaeli A, Jurenka RA (2001) Pyrokinin/PBAN-like peptides in the central nervous system of Drosophila melanogaster. Cell Tissue Res 306:459–465

    Article  PubMed  CAS  Google Scholar 

  • Choi M-Y, Lee JM, Han KS, Boo KS (2004) Identification of a new member of PBAN family and immunoreactivity in the central nervous system from Adoxophyes sp. (Lepidoptera: Tortricidae). Insect Biochem Mol Biol 34:927–935

    Article  PubMed  CAS  Google Scholar 

  • Davis NT, Homberg U, Teal PE, Altstein M, Agricola HJ, Hildebrand JG (1996) Neuroanatomy and immunocytochemistry of the median neuroendocrine cells of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: immunoreactivities to PBAN and other neuropeptides. Microsc Res Tech 35:201–229

    Article  PubMed  CAS  Google Scholar 

  • Duportets L, Gadenne C, Dufour MC, Couillaud F (1998) The pheromone biosynthesis activating neuropeptide (PBAN) of the black cutworm moth, Agrotis ipsilon: immunohistochemistry, molecular characterization and bioassay of its peptide sequence. Insect Biochem Mol Biol 28:591–599

    Article  PubMed  CAS  Google Scholar 

  • Foster SP, Bergh JC, Rose S, Harris MO (1991) Aspects of pheromone biosynthesis in the Hessian fly, Mayetiola destructor (Say). J Insect Physiol 37:899–906

    Article  CAS  Google Scholar 

  • Gäde G (1997) The explosion of structural information on insect neuropeptides. Pro Chem Organic Natural Products 71:1–128

    Google Scholar 

  • Holman GM, Cook BJ, Nachman RJ (1986) Isolation, primary structure and synthesis of a blocked neuropeptide isolated from the cockroach, Leucophaea maderae. Comp Biochem Physiol 85C:219–224

    CAS  Google Scholar 

  • Hummon AB, Richmond TA, Verleyen P, Baggerman G, Huybrechts J, Ewing MA, Vierstraete E, Rodriguez-Zas SL, Schoofs L, Robinson GE, Sweedler JV (2006) From the genome to the proteome: uncovering peptides in the Apis brain. Science 314:647–649

    Article  PubMed  CAS  Google Scholar 

  • Kingan TG, Blackburn MB, Raina A (1992) The identification of pheromone-biosynthesis-activating neuropeptide (PBAN) immunoreactivity in the central nervous system of the corn earworm, Helicoverpa zea. Cell Tissue Res 270:229–240

    Article  CAS  Google Scholar 

  • Li B, Predel R, Neupert S, Hauser F, Tanaka Y, Cazzamali G, Williamson M, Arakane Y, Verleyen P, Schoofs L, Schachtner J, Grimmelikhuijzen CJ, Park Y (2008) Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Res 18:113–122

    Article  PubMed  CAS  Google Scholar 

  • Ma PWK, Roelofs WL (1995) Sites of synthesis and release of PBAN-like factor in the female European corn borer, Ostrinia nubilalis. J Insect Physiol 41:339–350

    Article  CAS  Google Scholar 

  • Ma PWK, Roelofs WL, Jurenka RA (1996) Characterization of PBAN and PBAN-encoding gene neuropeptides in the central nervous system of corn earworm moth, Helicoverpa zea. J Insect Physiol 42:257–266

    Article  CAS  Google Scholar 

  • Matsumoto S, Kitamura A, Nagasawa H, Kataoka H, Orikasa C, Mitsui T, Suzuki A (1990) Functional diversity of a neurohormone produced by the suboesophageal ganglion: molecular identity of melanization and reddish colouration hormone and pheromone biosynthesis activating neuropeptide. J Insect Physiol 36:427–432

    Article  CAS  Google Scholar 

  • Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3:e305

    Article  PubMed  Google Scholar 

  • Nachman RJ, Holman GM, Cook BJ (1986) Active fragments and analogs of the insect neuropeptide Leucopyrokinin: structure-function studies. Biochem Biophys Res Comm 137:936–942

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR (1996) Neuropeptides, amines and amino acids in an elementary insect ganglion: functional and chemical anatomy of the unfused abdominal ganglion. Prog Neurobiol 48:325–420

    Article  PubMed  CAS  Google Scholar 

  • Niven JE, Graham CM, Burrows M (2008) Diversity and evolution of the insect ventral nerve cord. Annu Rev Entomol 53:253–271

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Eckert M (2000a) Neurosecretion: peptidergic systems in insects. Naturwissenschaften 87:343–350

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Eckert M (2000b) Tagma-specific distribution of FXPRLamides in the nervous system of the American cockroach. J Comp Neurol 419:352–363

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Nachman RJ (2001) Efficacy of native FXPRLamides (pyrokinins) and synthetic analogs on visceral muscles of the American cockroach. J Insect Physiol 47:287–293

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Herbert Z, Eckert M (2003) Neuropeptides in perisympathetic organs of Manduca sexta: specific composition and changes during the development. Peptides 24:1457–1464

    Article  PubMed  CAS  Google Scholar 

  • Rafaeli A, Jurenka R (2003) PBAN regulation of pheromone biosynthesis in female moths. In: Blomquist G, Vogt R (eds) Insect Pheromone Biochemistry and Molecular Biology. Academic Press, New York, pp 53–80

    Google Scholar 

  • Raina AK, Kempe TG (1992) Structure activity studies of PBAN of Helicoverpa zea (Lepidoptera: Noctuidae). Insect Biochem Mol Biol 22:221–225

    Article  CAS  Google Scholar 

  • Raina AK, Jaffe H, Kempe TG, Keim P, Blacher RW, Fales HM, Riley CT, Klun JA, Ridgway RL, Hayes DK (1989) Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science 244:796–798

    Article  PubMed  CAS  Google Scholar 

  • Raina AK, Kingan TG, Kochansky JP (2003) A pheromonotropic peptide of Helicoverpa zea, with melanizing activity, interaction with PBAN, and distribution of immunoreactivity. Arch Insect Biochem Physiol 53:147–157

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Ikeda M, Yamashita O (1994) Neurosecretory cells expressing the gene for common precursor for diapause hormone and pheromone biosynthesis-activating neuropeptide in the suboesophageal ganglion of the silkworm, Bombyx mori. Gen Comp Endocrinol 96:27–36

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Shiomi K, Saito H, Imai K, Yamashita O (1998) Phe-X-Pro-Arg-Leu-NH(2) peptide producing cells in the central nervous system of the silkworm, Bombyx mori. J Insect Physiol 44:333–342

    Article  PubMed  CAS  Google Scholar 

  • Schoofs L, Tips A, Holman GM, Nachman RJ, DeLoof A (1992) Distribution of locustamyotropin-like immunoreactivity in the nervous system of Locusta migratoria. Regul Pept 37:237–254

    Article  PubMed  CAS  Google Scholar 

  • Sun JS, Zhang TY, Zhang QR, Xu WH (2003) Effect of the brain and suboesophageal ganglion on pupal development in Helicoverpa armigera through regulation of FXPRLamide neuropeptides. Regul Pept 116:163–171

    Article  PubMed  CAS  Google Scholar 

  • Suwan S, Isobe M, Yamashita O, Minakata H, Imai K (1994) Silkworm diapause hormone, structure-activity relationships and indispensable role of C-terminal amide. Insect Biochem Mol Biol 24:1001–1007

    Article  PubMed  CAS  Google Scholar 

  • Teal PEA (1998) Stimulation of sex pheromone production in corn earworm moths by injection of extracts of heads of males of the Caribbean fruit fly. Florida Entomologist 81:98–104

    Article  Google Scholar 

  • Tips A, Schoofs L, Paemen L, Ma M, Blackburn M, Raina A, Loof AD (1993) Co-localization of locustamyotropin- and pheromone biosynthesis activating neuropeptide-like immunoreactivity in the central nervous system of five insect species. Comp Biochem Physiol [A] 106:195–207

    Article  Google Scholar 

  • Vander Meer RK, Alonso LE (1998) Pheromone directed behavior in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, pp 159–192

    Google Scholar 

  • Vander Meer RK, Alonso LE (2002) Queen primer pheromone affects conspecific fire ant (Solenopsis invicta) aggression. Behav Ecol Sociobiol 51:122–130

    Article  Google Scholar 

  • Vargo EL (1998) Primer pheromones in ants. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview, Boulder, pp 293–313

    Google Scholar 

  • Wei Z-J, Hong G-Y, Jinag S-T, Tong Z-X, Lu C (2008) Characters and expression of the gene encoding DH, PBAN and other FXPRLamide family neuropeptides in Antheraea pernyi. J Appl Entomol 132:59–67

    Article  CAS  Google Scholar 

  • Xu WH, Denlinger DL (2003) Molecular characterization of prothoracicotropic hormone and diapause hormone in Heliothis virescens during diapause, and a new role for diapause hormone. Insect Mol Biol 12:509–516

    Article  PubMed  CAS  Google Scholar 

  • Zdarek J, Nachman RJ, Hayes TK (1997) Insect neuropeptides of the pyrokinin/PBAN family accelerate pupariation in the fleshfly (Sarcophaga bullata) larvae. Ann N Y Acad Sci 814:67–72

    Article  PubMed  CAS  Google Scholar 

  • Zhang TY, Sun JS, Zhang LB, Shen JL, Xu WH (2004) Cloning and expression of the cDNA encoding the FXPRL family of peptides and a functional analysis of their effect on breaking pupal diapause in Helicoverpa armigera. J Insect Physiol 50:25–33

    Article  PubMed  CAS  Google Scholar 

  • Zhao CH, Li Q, Gao W (2002) Stimulation of sex pheromone production by PBAN-like substance in the pine caterpillar moth, Dendrolimus punctatus (Lepidoptera: Lasiocampidae). Arch Insect Biochem Physiol 49:137–148

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank David Milne, Becky Blair, and Michele Custer for insect collection, rearing, and bioassay. Dr. Russell Jurenka kindly provided the anti-serum against Hez-PBAN. We also thank Drs. Jim Nation and Steve Valles for valuable review and comments.

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Correspondence to Man-Yeon Choi.

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This research was supported in part by a US-Israel Binational Science Foundation Grant (no. 2003367).

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Choi, MY., Raina, A. & Vander Meer, R.K. PBAN/pyrokinin peptides in the central nervous system of the fire ant, Solenopsis invicta . Cell Tissue Res 335, 431–439 (2009). https://doi.org/10.1007/s00441-008-0721-6

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