Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Evidence for the involvement of a SchistoFLRF-amide-like peptide in the neural control of locust oviduct

  • 43 Accesses

  • 84 Citations

Summary

The presence of a SchistoFLRFamide-like peptide associated with the oviducts of Locusta migratoria has been shown using sequential reversed-phase high performance liquid chromatography separation coupled with radioimmunoassay and bioassay. The peptide is present in areas of the oviduct which receive extensive innervation, with sixfold less peptide in areas that receive little innervation. Material with FMRFamide-like immunoreactivity (determined by radioimmunoassay) is also present in the oviducal nerve and VIIth abdominal ganglion.

SchistoFLRFamide is a potent modulator of contraction of this visceral muscle, inhibiting or reducing the amplitude and frequency of spontaneous contractions, relaxing basal tonus, and reducing the amplitude of neurally-evoked, proctolin-induced, glutamate-induced and high potassium-induced contractions. The FMRFamide-like immunoreactivity within the oviducts which co-elutes with SchistoFLRFamide on two separations is also capable of reducing the amplitude of neurally-evoked and proctolin-induced contractions, and of inhibiting spontaneous contractions and relaxing basal tonus.

The effects of SchistoFLRFamide upon this visceral muscle are not abolished by the α-adrenergic receptor antagonist phentolamine and do not appear to be mediated by cyclic AMP. Thus the receptors for Schisto-FLRFamide are distinct from those of octopamine which mediate similar physiological effects but which are blocked by phentolamine and which are coupled to adenylate cyclase.

The results indicate that SchistoFLRFamide, or a very similar peptide, which has previously been identified as a modulator of locust heart beat, is also associated with visceral muscle of the reproductive system, and may play a neural role in concert with octopamine, at modulating muscular activity.

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

Abbreviations

BPP :

Bovine pancreatic polypeptide

BSA :

Bovine serum albumin

EJP :

Excitatory junctional potential

FaRPs :

FMRFamide-related peptides

FLI :

FMRFamide-like immuno-reactivity

LMS :

Leucomyosuppressin

RIA :

Radioimmunoassay

RP-HPLC :

Reversed-phase high performance liquid chromatography

TFA :

Trifluoroacetic acid

References

  1. Baines RA, Tyrer NM, Mason JC (1989) The innervation of locust salivary gland. II. Physiology of excitation and modulation. J Comp Physiol A 165:407–413

  2. Bishop CA, O'Shea M (1982) Neuropeptide proctolin (H-Arg-Tyr-Leu-Pro-Thr-OH): Immunocytochemical mapping of neurons in the central nervous system of the cockroach. J Comp Neurol 207:223–238

  3. Boer HH, Schot LPC, Veenstra JA, Reichelt D (1980) Immunocytochemical identification of neural elements in the central nervous systems of a snail, some insects, a fish, and a mammal with an antiserum to the molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell Tissue Res 213:21–27

  4. Bulloch AGM, Price DA, Murphy AD, Lee TD, Bowes HN (1988) FMRFamide peptides in Helisoma: Identification and physiological actions at a peripheral synapse. J Neurosci 8:3459–3469

  5. Carroll LS, Carrow GM, Calabrese RL (1986) Localization and release of FMRFamide-like immunoreactivity in the cerebral neuroendocrine system of Manduca sexta. J Exp Biol 126:1–14

  6. Colombaioni L, Paupardin-Tritsch D, Vidal PP, Gerschenfeld HM (1985) The neuropeptide FMRFamide decreases both the Ca2+ conductance and a cyclic 3′,5′-adenosine monophosphate-dependent K+ conductance in identified moll neurons. J Neurosci 5:2533–2538

  7. Cottrell GA, Davies NW (1987) Multiple receptor site for a molluscan peptide (FMRFamide) and related peptides of Helix. J Physiol 382:51–68

  8. Cottrell GA, Greenberg MJ, Price DA (1983) Differential effects of the molluscan neuropeptide FMRFamide and the related met-enkephalin derivative YGGFMRFamide on the Helix tentacle retractor muscle. Comp Biochem Physiol 75C: 373–375

  9. Cuthbert BA, Evans PD (1989) A comparison of the effects of FMRFamide-like peptides on locust heart and skeletal muscle. J Exp Biol 144:395–415

  10. Evans PD, Cournil I (1990) Co-localization of FLRF- and vasopressin-like immunoreactivity in a single pair of sexually dimorphic neurones in the nervous system of the locust. J Comp Neurol 292:331–348

  11. Evans PD, Myers CM (1986) The modulatory actions of FMRFamide and related peptides on locust skeletal muscle. J Exp Biol 126:403–422

  12. Evans PD, Robb S, Cuthbert BA (1989) Insect neuropeptides — Identification, establishment of functional roles and novel target sites for pesticides. Pestic Sci 25:71–83

  13. Holman GM, Cook BJ, Nachman RJ (1986a) Leucomyosuppressin: a decapeptide that inhibits hindgut contractile activity in Leucophaea maderae. In: Borkovec AB, Gelman DB (eds) Insect neurochemistry and neurophysiology. Humana Press, Clifton, NJ, pp 203–206

  14. Holman GM, Cook BJ, Nachman RJ (1986b) Isolation, primary structure and synthesis of leucomyosuppressin, an insect neuropeptide that inhibits spontaneous contractions of the cockroach hindgut. Comp Biochem Physiol 85C: 329–333

  15. Hooper SL, Marder E (1984) Modulation of a central pattern generator by two neuropeptides, proctolin and FMRFamide. Brain Res 305:186–191

  16. Lange AB, Orchard I (1984a) Some pharmacological properties of neuromuscular transmission in the oviduct of the locust, Locusta migratoria. Arch Insect Biochem Physiol 1:231–241

  17. Lange AB, Orchard I (1984b) Dorsal unpaired median neurons, and ventral bilaterally paired neurons, project to a visceral muscle in an insect. J Neurobiol 15:441–453

  18. Lange AB, Orchard I (1986) Identified octopaminergic neurons modulate contractions of locust visceral muscle via adenosine 3′,5′-monophosphate (cyclic AMP). Brain Res 363:340–349

  19. Lange AB, Orchard I, Adams ME (1986) Peptidergic innervation of insect reproductive tissue: The association of proctolin with oviduct visceral musculature. J Comp Neurol 254:279–286

  20. Lange AB, Orchard I, Lam W (1987) Mode of action of proctolin on locust visceral muscle. Arch Insect Biochem Physiol 5:285–295

  21. Li C, Calabrese RL (1987) FMRFamide-like substances in the leech. III Biochemical characterization and physiological action. J Neurosci 7:595–603

  22. Matsumoto S, Brown MR, Crim JW, Vigna SR, Lea AO (1989) Isolation and primary structure of neuropeptides from the mosquito, Aedes aegypti, immunoreactive to FMRFamide antiserum. Insect Biochem 19:277–283

  23. Myers CM, Evans PD (1985a) The distribution of bovine pancreatic polypeptide/FMRFamide-like immunoreactivity in the ventral nervous system of the locust. J Comp Neurol 234:1–16

  24. Myers CM, Evans PD (1985b) An FMRFamide antiserum differentiates between populations of antigens in the ventral nervous system of the locust, Schistocerca gregaria. Cell Tissue Res 242:109–114

  25. Nachman RJ, Holman GM, Cooke BJ, Haddon WF, Ling N (1986a) Leucosulfakinin-II, a blocked sulfated insect neuropeptide with homology to cholecystokinin and gastrin. Biochem Biophys Res Comm 140:357–364

  26. Nachman RJ, Holman GM, Haddon WF, Ling N (1986b) Leucosulfakinin, a sulfated insect neuropeptide with homology to gastrin and cholecystokinin. Science 234:71–73

  27. Nambu JR, Murphy-Erdosh C, Andrews PC, Feistner GJ, Scheller RH (1988) Isolation and characterization of a Drosophila neuropeptide gene. Neuron 1:55–61

  28. Orchard I, Lange AB (1985) Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol 16:171–181

  29. Orchard I, Lange AB (1986) Neuromuscular transmission in an insect visceral muscle. J Neurobiol 17:359–372

  30. O'Shea M, Adams ME (1981) Pentapeptide (proctolin) associated with an identified neuron. Science 213:567–569

  31. Painter SD, Greenberg MJ (1982) A survey of the responses of bivalve hearts to the molluscan neuropeptide FMRFamide and to 5-hydroxytryptamine. Biol Bull 162:311–332

  32. Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671

  33. Price DA, Greenberg MJ (1980) The pharmacology of the molluscan cardioexcitatory neuropeptide FMRFamide. Gen Pharmacol 11:237–241

  34. Price DA, Greenberg MJ (1989) The hunting of the FaRPs: The distribution of FMRFamide-related peptides. Biol Bull 177:198–205

  35. Robb S, Packman LC, Evans PD (1989) Isolation, primary structure and bioactivity of SchistoFLRF-amide, a FMRF-amide-like neuropeptide from the locust, Schistocerca gregaria. Biochem Biophys Res Comm 160:850–856

  36. Schiebe M, Orchard I, Watts R, Lange AB, Atwood HL (1990) Characterization and partial purification of different factors with contraction-potentiating activities from neurohaemal organs of the locust. J Comp Neurol 291:305–312

  37. Spencer AN (1988) Effects of Arg-Phe-amide peptides on identified motor neurons in the hydromedusa Polyorchis penicillatus. Can J Zool 66:639–645

  38. Trimmer BA, Kobierske LA, Kravitz EA (1987) Purification and characterization of FMRFamidelike immunoreactive substances from the lobster nervous system: Isolation and sequence analysis of two closely related peptides. J Comp Neurol 266:16–26

  39. Veenstra JA, Schooneveld H (1984) Immunocytochemical localization of peptidergic neurons in the nervous system of the Colorado potato beetle with antisera against FMRFamide and bovine pancreatic polypeptide. Cell Tissue Res 235:303–308

  40. Walther C, Schäfer S (1988) FMRFamide-like immunoreactivity in the metathoracic ganglion of the locust (Schistocerca gregaria). Cell Tissue Res 253:489–491

  41. Walther C, Schiebe M, Voigt KH (1984) Synaptic and non-synaptic effects of molluscan cardioexcitatory neuropeptides on locust skeletal muscle. Neurosci Lett 45:99–104

  42. Walther C, Schiebe M (1987) FMRF-NH2-like factor from neurohaemal organ modulates neuromuscular transmission in locust. Neurosci Lett 77:209–214

  43. Weiss S, Goldberg JI, Chohan KS, Stell WK, Drummond GI, Lukowiak K (1984) Evidence for FMRF-amide as a neurotransmitter in the gill of Aplysia californica. J Neurosci 4:1994–2000

  44. Witten JL, O'Shea M (1985) Peptidergic innervation of insect skeletal muscle: Immunochemical observations. J Comp Neurol 242:93–101

Download references

Author information

Correspondence to Angela B. Lange.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lange, A.B., Orchard, I. & Te Brugge, V.A. Evidence for the involvement of a SchistoFLRF-amide-like peptide in the neural control of locust oviduct. J Comp Physiol A 168, 383–391 (1991). https://doi.org/10.1007/BF00198357

Download citation

Key words

  • FMRFamide-like immunoreactivity
  • SchistoFLRFamide
  • RP-HPLC
  • Neural control
  • Visceral muscle
  • Oviduct
  • Insect