Skip to main content
Log in

The distribution of pheromone-biosynthesis-activating neuropeptide (PBAN) immunoreactivity in the central nervous system of the corn earworm moth, Helicoverpa zea

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript


Production of sex pheromone in several species of moths has been shown to be under the control of a neuropeptide termed pheromone-biosynthesis-activating neuropeptide (PBAN). We have produced an antiserum to PBAN from Helicoverpa zea (Lepidoptera: Noctuidae) and used it to investigate the distribution of immunoreactive peptide in the brain-suboesophageal ganglion complex and its associated neurohemal structures, and the segmental ganglia of the ventral nerve cord. Immunocytochemical methods reveal three clusters of cells along the ventral midline in the suboesophageal ganglion (SOG), one cluster each in the presumptive mandibular (4 cells), maxillary (12–14 cells), and labial neuromeres (4 cells). The proximal neurites of these cells are similar in their dorsal and lateral patterns of projection, indicating a serial homology among the three clusters. Members of the mandibular and maxillary clusters have axons projecting into the maxillary nerve, while two additional pairs of axons from the maxillary cluster project into the ventral nerve cord. Members of the labial cluster project to the retrocerebral complex (corpora cardiaca and cephalic aorta) via the nervus corpus cardiaci III (NCC III). The axons projecting into the ventral nerve cord appear to arborize principally in the dorsolateral region of each segmental ganglion; the terminal abdominal ganglion is distinct in containing an additional ventromedial arborization in the posterior third of the ganglion. Quantification of the extractable immunoreactive peptide in the retrocerebral complex by ELISA indicates that PBAN is gradually depleted during the scotophase, then restored to maximal levels in the photophase. Taken together, our findings provide anatomical evidence for both neurohormonal release of PBAN as well as axonal transport via the ventral nerve cord to release sites within the segmental ganglia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others





brain-suboesophageal ganglion complex


corpus cardiacum


phosphate-buffered saline


PBAN-like immunoreactivity


terminal abdominal ganglion


ventral nerve cord


  • Altman JS, Kien J (1987) Functional organization of the subesophageal ganglion in arthropods. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. Wiley, New York

    Google Scholar 

  • Altstein M, Gazit Y, Dunkleblum E (1990) Regulation of sex pheromone biosynthesis in Chrysodexis chalcites and Heliothis peltigera by PBAN. In: Bořkovek AB, Masler EP (eds) Insect neurochemistry and neurophysiology, Humana, Clifton NJ, pp 303–307

    Google Scholar 

  • Bestman HJ, Herrig H, Attygalle AB, Hupe M (1989) Regulatory steps in sex pheromone biosynthesis in Mamestra brassicae L. (Lepidoptera: Noctuidae). Experientia 45:778–781

    Google Scholar 

  • Bindokas VP, Adams ME (1988) Hemolymph composition of the tobacco budworm, Heliothis virescens F. (Lepidoptera: Noctuidae). Comp Biochem Physiol [A] 90:151–155

    Google Scholar 

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

  • Boer HH, Schot LPC, Roubos EW, terMaat A, Lodder JC, Reichelt D, Swaab DF (1979) ACTH-like immunoreactivity in two electrotonically coupled giant neurons in the pond snail Lymnea stagnalis. Cell Tissue Res 202:231–240

    Google Scholar 

  • Christensen TA, Itagaki H, Teal PEA, Jasensky RD, Tumlinson JH, Hildebrand JG (1991) Innvervation and neural regulation of the sex pheromone gland in female Heliothis moths. Proc Natl Acad Sci USA 88:4971–4975

    Google Scholar 

  • Copenhaver PF, Truman JW (1986) Metamorphosis of the cerebral neuroendocrine system in the moth Manduca sexta. J Comp Neurol 249:186–204

    Google Scholar 

  • Eaton JL (1988) Lepidopteran anatomy. Wiley, New York

    Google Scholar 

  • Hewes RS, Truman JW (1991) The roles of central and peripheral eclosion hormone release in the control of ecdysis behavior in Manduca sexta. J Comp physiol [A] 168:697–707

    Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1990) Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259:401–419

    Google Scholar 

  • Jurenka RA, Jacquin E, Roelofs WL (1991a) Control of the pheromone biosynthetic pathway in Helicoverpa zea by the pheromone biosynthesis activating neuropeptide. Arch Insect Biochem Physiol 17:81–91

    Google Scholar 

  • Jurenka RA, Jacquin E, Roelofs WL (1991b) Stimulation of pheromone biosynthesis in the moth Helicoverpa zea: action of a brain hormone on pheromone glands involves Ca2+ and cAMP as second messengers. Proc Natl Acad Sci USA 88:8621–8625

    Google Scholar 

  • King DG (1976) Organization of crustacean neuropil. I. Patterns of synaptic connections in lobster stomatogastric ganglion. J Neurocytol 5:207–237

    Google Scholar 

  • Kingan TG (1989) A competitive enzyme-linked immunosorbent assay: applications in the assay of peptides, steroids, and cyclic nucleotides. Anal Biochem 183:283–289

    Google Scholar 

  • Kingan TG, Raina AK, Blackburn M, Ma M (1990a) Distribution of PBAN-like immunoreactivity in the CNS of the corn earworm, Heliothis zea. Soc Neurosci Abstr 16:856

    Google Scholar 

  • Kingan TG, Teplow DB, Phillips JM, Riehm JP, Rao KR, Hildebrand JG, Homberg U, Kammer AE, Jardine I, Griffin PR, Hunt DF (1990b) A new peptide in the FMRFamide family isolated from the CNS of the hawkmoth, Manduca sexta. Peptides 11:849–856

    Google Scholar 

  • Iitamura A, Nagasawa H, Kataoka H, Inoue T, Matsumoto S, Ando T, Suzuki A (1989) Amino acid sequence of pheromonebiosynthesis-activating neuropeptide (PBAN) of the silkworm, Bombyx mori. Biochem Biophys Res Commun 163:520–526

    Google Scholar 

  • Kondoh Y, Hisada M (1986) Regional specialization in synaptic input and output in an identified local nonspiking interneuron of the crayfish revealed by light and electron microscopy. J Comp Neurol 251:334–348

    Google Scholar 

  • Martinez T, Camps F (1988) Stimulation of sex pheromone production by head extract in Spodoptera littoralis at different times in the photoperiod. Arch Insect Biochem Physiol 9:211–220

    Google Scholar 

  • Ohguchi Y, Taksuki S, Usui K, Arai K, Kurihara M, Uchiumi K, Fukami J (1985) Hormone-like substance present in the cephalic organs of the female moth, chilo suppressalis (Walker) (Lepidoptera: Pyralidae) and controlling sex pheromone production. Jpn J Appl Entomol Zool 29:265–269

    Google Scholar 

  • Qui Y, Cao M (1989) Mechanism of the control of sex pheromone production in female Asiatic corn borer (Ostrinia furnicalis Guenee). J Xiamen Univ 28:88–91

    Google Scholar 

  • Rafaeli A, Hirsch J, Soroker V, Kamensky B, Raina AK (1991) Spatial and temporal distribution of PBAN in Helicoverpa (Heliothis) armigera using RIA and in vitro bioassay. Arch Insect Biochem Physiol 18:119–129

    Google Scholar 

  • Raina AK, Klun JA (1984) Brain factor control of sex pheromone production in the female corn earworm moth. Science 225:531–533

    Google Scholar 

  • Raina AK, Menn JJ (1987) Endocrine regulation of pheromone production in Lepidoptera. In: Prestwich GD, Blomquist GJ (eds) Pheromone biochemistry. Academic Press, Orlando, Fla, pp 159–174

    Google Scholar 

  • Raina AK, Klun JA, Stadelbacher EA (1986) Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 79:128–131

    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

    Google Scholar 

  • Raina AK, Kempe TG, Jaffe H (1991) Pheromone biosynthesis-activating neuropeptide: regulation of pheromone production in moths. In: Menn JJ, Kelly TJ, Masler EP (eds) Insect neuropeptides: chemistry, biology, and action. American Chemical Society, Washington DC, pp 100–109

    Google Scholar 

  • Soroker V, Rafaeli A (1989) In vitro hormonal stimulation of [14C]acetate incorporation by Heliothis armigera pheromone glands. Insect Biochem 19:1–5

    Google Scholar 

  • Tang JD, Charlton RE, Jurenka RA, Wolf WA, Phelan PL, Streng L, Roelofs WL (1989) Regulation of pheromone biosynthesis by a brain hormone in two moth species. Proc Natl Acad Sci USA 86:1806–1810

    Google Scholar 

  • Teal PEA, Tumlinson JH, Oberlander H (1989) Neural regulation of sex pheromone biosynthesis in Heliothis moths. Proc Natl Acad Sci USA 86:2488–2493

    Google Scholar 

  • Veenstra JA (1984) Immunocytochemical demonstration of a homology in peptidergic neurosecretory cells in the subesophageal ganglion of a beetle and a locust with antisera to bovine pancreatic polypeptide, FMRFamide, vasopressin and α-MSH. Neurosci Lett 48:185–190

    Google Scholar 

  • Zitnan D, Verhaert P, De Loof A, Grimmelikhuijzen CJP (1988) Differences in the distribution of immunoreactivity to FMRF-amide and bovine pancreatic polypeptide antisera in the larval and imaginal central nervous system of Galleria mellonella (Lepidoptera). In: Sehnal F, Zabza A, Denlinger DL (eds) Endocrinological frontiers in physiological insect ecology, vol 2. Wroclaw University Press, Wroclaw, Poland, pp 847–857

    Google Scholar 

Download references

Author information

Authors and Affiliations


Rights and permissions

Reprints and permissions

About this article

Cite this article

Kingan, T.G., Blackburn, M.B. & Raina, A.K. The distribution of pheromone-biosynthesis-activating neuropeptide (PBAN) immunoreactivity in the central nervous system of the corn earworm moth, Helicoverpa zea . Cell Tissue Res 270, 229–240 (1992).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Key words