Summary
Proctolin-like immunoreactivity (PLI) was found in different parts of the arthropod central nervous system and in nerve fibers of muscles. In order to examine whether this PLI is related to a uniform type of secretory vesicle, hindgut musculature and frontal and hypocerebral ganglia were examined with the immunogold technique. PLI occurs exclusively within membran-bounded secretory granules. Neither granular ER nor Golgi stacks show PLI. In some cases close relationships between PLI-bearing granules and lysosomes were observed. In presynaptic areas, PLI-reactive granules are associated with numerous clear synaptic vesicles and restricted to an area distinctly separate from the presynaptic membrane. Three types of granules were found, differing in diameter and electron density: (1) dense, 80 nm; (2) dense, 150 nm; (3) low density, 150 nm. The results demonstrate that: (1) the PLI of the produced peptide occurs shortly after its separation from the Golgi stack; (2) the occurrence of PLI in three different granule types could be the morphological expression of the common occurrence of proctolin with other neuroactive substances. However, a possible cross-reactivity with other, hitherto unknown substances must be considered as well.
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References
Agricola H, Eckert M, Ude J, Birkenbeil H, Penzlin H (1985) The distribution of a proctolin-like immunoreactive material in the terminal ganglion of the cockroach, Periplaneta americana L. Cell Tissue Res 239:203–209
Beltz BS, Kravitz EA (1987) Physiological identification, morphological analysis and development of identified serotonin-proctolin containing neurones in the lobster ventral nerve cord. J Neurosci 7:533–541
Benson JA, Sullivan RE, Watson WH, Augustine GD (1981) The pentapeptide proctolin acts directly on limulus cardiac muscle to increase the amplitude of contraction. Brain Res 213:449–454
Bernstein HG, Eckert M, Penzlin H, Dorn A (1984) Proctolinrelated material in the mouse brain as revealed by immunocytochemistry. Neurosci Lett 45:229–232
Berry RW (1981) Proteolytic processing in the biogenesis of the neurosecretory egg-laying hormone in Aplysia. I. Precursors, intermediates and products. Biochemistry 20:6200–6205
Bishop CA, O'Shea M (1982) Neuropeptide proctolin (H-ArgTyr-Leu-Pro-Thr-OH): immunocytochemical mappings of neurones in the central nervous system of the cockroach. J Comp Neurol 207:223–238
Brown BE (1975) Proctolin: A peptide transmitter candidate in insects. Life Sci 17:1241–1252
Brown BE (1977) Occurrence of proctolin in six orders of insects. J Insect Physiol 23:861–864
Brown BE, Starratt AN (1975) Isolation of proctolin: a myotropic peptide from Periplaneta americana. J Insect Physiol 21:1879–1881
Cook BJ, Holman GM (1985) The role of proctolin and glutamate in the excitation-contraction coupling of insect visceral muscle. Comp Biochem Physiol 80C: 65–73
Cook BJ, Meola S (1978) The oviduct musculature of the horsefly Tabanus sulcifrons, and its response to 5-hydroxytryptamine and proctolin. Physiol Ent 3:273–280
Eckert M, Ude J (1983) Immunocytochemical techniques for the identification of peptidergic neurons. In: Strausfeld NJI (ed) Functional neuroanatomy. Springer Series in Experimental Entomology. Springer, Berlin Heidelberg New York, pp 267–301
Eckert M, Agricola H, Penzlin H (1980) Immunocytochemical identification of proctolinlike immunoreactivity in the terminal ganglion and hindgut of the cockroach Periplaneta americana (L.). Cell Tissue Res 217:633–645
Fricker LD (1985) Neuropeptide processing enzymes: focus on the carboxypeptidase processing enzyme. TINS 8:210–213
Gainer HG, Peng Loh Y, Sarne Y (1977) Biosynthesis of neuronal peptides. In: Gainer H (ed) Peptides in Neurobiology. Plenum Press, New York, pp 183–219
Halban PA, Wollheim CB (1980) Intracellular degradation of insulin stores by rat pancreatic islets in vitro. An alternative pathway for homeostasis of pancreatic insulin content. J Biol Chem 255:6003–6006
Hertel W, Penzlin H (1986) Elektrophysiological studies of the effect of the neuropeptide proctolin on the hyperneural muscle of Periplaneta americana (L.). J Insect Physiol 32:239–248
Hertel W, Pass G, Penzlin H (1985) Electrophysiological investigation of the antennal heart of Periplaneta americana and its reactions to proctolin. J Insect Physiol 31:563–572
Holets VR, Hökfelt T, Ude J, Eckert M, Penzlin H, Verhofstad AAJ, Visser TJ (1987) A comparative study of the immunohistochemical localization of a presumptive proctolin-like peptide, thyrotropin-releasing hormon and 5-hydroxytryptamine in the rat central nervous system. Brain Res 408:141–153
Holman GM, Cook BJ (1979) Evidence for proctolin and a second myotropic peptide in the cockroach Leucophaea maderae, determined by bioassay and HPLC analysis. Insect Biochem 9:149–154
Holman GM, Cook BJ, Nachman RJ (1986) Primary structure and synthesis of a blocked myotropic neuropeptide isolated from the cockroach Leucophaea maderae. Comp Biochem Physiol 85C: 219–224
Kingan T, Titmus M (1983) Radioimmunologic detection of proctolin in arthropods. Comp Biochem Physiol 74C: 75–78
Marder E, Hooper SL, Siwicki KK (1986) Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric system nervous system. J Comp Neurol 243:454–467
Miller T (1979) Nervous versus neurohormonal control of insect heartbeat. Am Zool 19:77–86
O'Shea M, Witten J, Schaffer M (1984) Isolation and characterization of two myoactive neuropeptides. Further evidence of an invertebrate peptide family. J Neurosci 4:521–529
Roth J (1983) The colloid gold marker system for light- and electron microscopid cytochemistry. In: Bullock GR, Petrusz P (eds) Techniques in Immunocytochemistry, vol 2. Academic Press, London New York, pp 217–284
Schnell AH, Borg LAH (1985) Lysosomes and pancreatic islet function. Cell Tissue Res 239:537–545
Schooneveld H, Tesser GI, Veenstra JA, Romberg-Privee HM (1983) Adipokinetic hormone and AKH-like peptide demonstrated in the corpora cardiaca and nervous system of Locusta migratoria by immunohistochemistry. Cell Tissue Res 230:67–76
Schulz H, Schwarzberg H, Penzlin H (1981) The insect neuropeptide proctolin can affect the CNS and the smooth muscle of mammals. Acta Biol Med Germ 40:K1-K5
Siwicki KK, Bishop CA (1986) Mapping of proctolinlike immunoreactivity in the nervous systems of lobster and crayfish. J Comp Neurol 243:435–453
Siwicki KK, Beltz BS, Kravitz EA (1987) Proctolin in identified serotonergic, dopaminergic and cholinergic neurons in the lobster Homarus americanus. J Neurosci 7:522–532
Slot JW, Geuze HJ (1984) Gold markers for single and double immunolabelling of ultrathin cryosections. In: Polak JM, Varndell IM (eds) Immunolabelling for electron microscopy. Elsevier, Amsterdam New York Oxford, pp 129–142
Smith RE, Farquhar MG (1966) Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J Cell Biol 31:319–347
Sobek L, Eckert M, Penzlin H, Reissmann S (1986) Evidence for proctolinergic innervation of the cockroach oviduct. Zool Jb Physiol 90:461–466
Stoya G, Penzlin H (1988) The effect of different putative transmitters on spontaneous phasic contractions of cockroach oviduct. Zool Jb Physiol 92:301–311
Sullivan RE (1979) A proctolin-like peptide in crab pericardial organs. J Exp Zool 210:543–552
Turner AJ (1984) Neuropeptide processing enzymes. TINS 7:258–260
Walker RJ, James VA, Roberts CJ, Kerkut GA (1980) Neurotransmitter receptors in invertebrates. In: Sattelle DB (ed) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North Holland Amsterdam, pp 41–57
Watson III WH, Augustine GJ, Benson JA, Sullivan RE (1983) Proctolin and an endogenous proctolin-like peptide enhance the contractility of the Limulus heart. J Exp Biol 103:55–73
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Ude, J., Eckert, M. Submicroscopic characterization of proctolin-like immunoreactivity in the nervous system of the cockroach Periplaneta americana L.. Cell Tissue Res. 254, 197–202 (1988). https://doi.org/10.1007/BF00220034
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DOI: https://doi.org/10.1007/BF00220034