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First published April 2003

Distribution of PER Protein, Pigment-Dispersing Hormone, Prothoracicotropic Hormone, and Eclosion Hormone in the Cephalic Nervous System of Insects

Abstract

Investigations performed on adult insects revealed that putative components of the central pacemaker, the protein Period (PER) and the pigment-dispersing hormone (PDH), are immunocytochemically detectable in discrete sets of brain neurons throughout the class of Insecta, represented by a bristletail, mayfly, damselfly, 2 locust species, stonefly, 2 bug species, goldsmith beetle, caddisfly, honeybee, and 2 blowfly species. The PER-positive cells are localized in the frontal protocerebrum and in most species also in the optic lobes, which are their only location in damselfly and goldsmith beetle. Additional PER-positive cells occur in a few species either in the deuto- and tritocerebrum or in the suboesophageal ganglion. The PER staining was always confined to the cytoplasm. The PDH immunoreactivity consistently occurs in a cluster of perikarya located frontoventrally at the proximal edge of the medulla. The mayfly and both locust species possess additional PDH neurons in 2 posterior cell clusters at the proximal edge of the medulla, and mayfly, waterstrider, and 1 of the blowfly species in the central brain. PDH-positive fibers form a fanlike arrangement over the frontal side of the medulla. Two or just 1 bundle of PDH-positive fibers run from the optic lobe to the protocerebrum, with collaterals passing over to the contralateral optic lobe. Antisera to the prothoracicotropic (PTTH) and the eclosion (EH) hormones, which in some insects regulate the molting and ecdysis rhythms, respectively, typically react with a few neurons in the frontal protocerebrum. However, the PTTH-positive neurons of the mayfly and the damselfly and the EH-positive neurons of the caddisfly are located in the suboesophageal ganglion. No PTTH-like antigen was detected in locusts, and no EH-like antigens were detected in the damselfly, stonefly, locusts, and the honeybee. There are no signs of co-localization of the PER-, PDH-, PTTH-, and EH-like antigens in identical neurons.

References

Citri Y, Colot HV, Jacquier AC, Yu Q, Hall JC, Baltimore D, and Rosbash M (1987) A family of unusually spliced and biologically active transcripts encoded by Drosophila clock gene. Nature 326: 42-47.
Copenhaver PF and Truman JW (1986) Identification of the cerebral neurosecretory cells that contain eclosion hormone in the moth Manduca sexta. J Neurosci 6: 1738-1747.
Dai JD, Mizoguchi A, and Gilbert LI (1994) Immunoreactivity of neurosecretory granules in the brain-retrocerebral complex of Manduca sexta to heterologous antibodies against Bombyx prothoracicotropic hormone and bombyxin. Invertebr Reprod Dev 26: 187-196.
Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96: 271-290.
Frisch B, Fleissner G, Fleissner G, Brandes C, and Hall JC (1996) Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: Labeling of cells with possible importance for the beetle’s circadian rhythms. Cell Tissue Res 286: 411-429.
Hagberg M (1986) Ultrastructure and central projections of extraocular photoreceptors in caddisflies (Insecta: Trichoptera). Cell Tissue Res 245: 643-648.
Hall JC (1998) Genetics of biological rhythms in Drosophila. Adv Genet 33: 135-184.
Helfrich-Förster C (1995) The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 92: 612-616.
Helfrich-Förster C and Homberg U (1993) Pigment-dispersing-hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337: 177-190.
Helfrich-Förster C, Stengl M, and Homberg U (1998) Organization of the circadian system in insects. Chronobiol Internat 15: 567-594.
Helfrich-Förster C, Täuber M, Park JH, Mühlig-Versen M, Schneuwly S, and Hofbauer A (2000) Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. J Neurosci 20: 3339-3353.
Homberg U, Würden S, Dircksen H, and Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266: 343-357.
Honegger HW, Leser W, Loher W, and Siwicki KK (1991) Labelling of cells in the CNS of the cricket Teleogryllus commodus by an antibody to Drosophila per-protein. Sci Neurosci Abstr 17: 1239.
Horodyski FM, Ewer J, Riddiford LM, and Truman JW (1993) Isolation, characterization and expression of the eclosion hormone gene of Drosophila melanogaster. Eur J Biochem 215: 221-228.
Hunter-Ensor M, Ousley A, and Seghal A (1996) Regulation of the Drosophila protein timeless suggests a mechanism for resetting the circadian clock by light. Cell 84: 677-685.
Kaneko M, Helfrich-Förster C, and Hall JC (1997) Spatial and temporal expression of the period and timeless genes in the developing nervous system of Drosophila: Newly identified pacemaker candidates and novel features of clock gene product cycling. J Neurosci 17: 6745-6760.
Kataoka H, Nagasawa H, Isogai A, Tamura S, Mizoguchi A, Fujiwara Y, Suzuki C, Ishizaki H, and Suzuki A (1987) Isolation and partial characterization of a prothoracicotropic hormone of the silkworm, Bombyx mori. Agric Biol Chem 51: 1067-1076.
Kataoka H, Troetschler RG, Kramer SJ, Cesarin BJ, and Schooley DA (1987) Isolation and primary structure of the eclosion hormone of the tobacco hornworm, Manduca sexta. Biochem Biophys Res Commun 146: 746-750.
Kloss B, Price JL, Saez L, Blau J, Rothenfluh A, Wesley CS, and Young MW (1998) The Drosophila clock gene double-time encodes a protein closely related to human casein kinase I. Cell 94: 97-107.
Kono T, Nagasawa H, Isogai A, Fugo H, and Suzuki A (1987) Amino acid sequence of eclosion hormone of the silkworm, Bombyx mori. Agric Biol Chem 51: 2307-2308.
Levine JD, Sauman I, Imbalzano M, Reppert SM, and Jackson FR (1995) Period protein from the giant silkmoth Antheraea pernyi functions as a circadian clock element in Drosophila melanogaster. Neuron 15: 147-157.
Liu X, Lorenz L, Yu Q, Hall JC, and Rosbash M (1988) Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes Dev 2: 228-238.
Marti T, Takio K, Walsh KA, Terzi G, and Truman JW (1987) Microanalysis of the amino acid sequence of the eclosion hormone from the tobacco hornworm Manduca sexta. FEBS Lett 219: 415-418.
Naya S, Suzuki K, Fugo H, and Sehnal F (1994) Eclosion hormone-like immunoreactivity in the nervous system of Bombyx mori (Lepidoptera: Bombycidae) and Antheraea yamamai (Lepidoptera: Saturniidae) before and after hatching. Eur J Entomol 91: 189-196.
Page TL (1984) Neural organization of a circadian clock in the cockroach Leucophaea maderae. In Photoperiodic Regulation of Insect and Molluscan Hormones, R Porter and GM Collins, eds, pp 115-135, Pitman, London.
Persson MGS, Eklund MB, Dircksen H, Muren JE, and Nässel DR (2001) Pigment-dispersing factor in the locust abdominal ganglia may have roles as circulating neurohormone and central neuromodulator. J Neurobiol 48: 19-41.
Price JL, Blau J, Rothenfluh A, Adodeely M, Kloss B, and Young MW (1998) double-time is a new Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94: 83-95.
Rao KR (2001) Crustacean pigmentary-effector hormones: Chemistry and functions of RPCH, PDH, and related peptides. Amer Zool 41: 364-379.
Renn SCP, Park JH, Rosbash M, Hall JC, and Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802.
Reppert SM, Tsai T, Roca AL, and Sauman I (1994) Cloning of a structural homolog of the circadian clock gene period from the giant silkmoth Antheraea pernyi. Neuron 13: 1167-1176.
Reynolds SE and Truman JW (1983) Eclosion hormone. In Endocrinology of Insects, RGH Downer and H Laufer, eds, Vol 1, pp 217-233, Alan R. Liss, New York.
Rosbash M (1995) Molecular control of circadian rhythms. Curr Opin Genet Dev 5: 662-668.
Sassone-Corsi P (1996) Same clock, different works. Nature 384: 613-614.
Sauman I and Hashimi H (1999) Insect clocks: What are they telling us besides time? Entomol Sci 2: 589-596.
Sauman I and Reppert SM (1996a) Circadian clock neurons in the silkmoth Antheraea pernyi: Novel mechanisms of period protein regulation. Neuron 17: 889-900.
Sauman I and Reppert SM (1996b) Molecular characterization of prothoracicotropic hormone (PTTH) from the giant silkmoth Antheraea pernyi: Developmental appearance of PTTH-expressing cells and relationship to circadian clock cells in central brain. Dev Biol 178: 418-429.
Sauman I, Tsai T, Roca AL, and Reppert SM (1996) period protein is necessary for circadian control of egg hatching behavior in the silkmoth Antheraea pernyi. Neuron 17: 901-909.
Shionoya M, Matsubayashi H, Asahina M, Kuniyashi H, Nagata S, Riddiford RM, and Kataoka H (2000) SwissProt or GenBank Accession No. AY007724.
Simoes ZLP, Boleli IC, and Hartfelder K (1997) Occurrence of a prothoracicotropic hormone-like peptide in the developing nervous system of the honey bee (Apis mellifera L). Apidologie 28: 399-409.
Siwicki KK, Eastman C, Petersen G, Rosbash M, and Hall JC (1998) Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1: 141-150.
Stengl M and Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol 175: 203-213.
Truman JW (1972) Physiology of insect rhythms. II. The silkmoth brain as the location of the biological clock controlling eclosion. J Comp Physiol 81: 99-114.
Vafopoulou X and Steel CGH (2001) Induction of rhythmicity in prothoracicotropic hormone and ecdysteroids in Rhodnius prolixus: Roles of photic and neuroendocrine zeitgebers. J Insect Physiol 47: 935-941.
Wheeler WC, Whiting M, Wheeler QD, and Carpenter JM (2001) The phylogeny of extant hexapor orders. Cladistics 17: 113-169.
Williams JA and Sehgal A (2001) Molecular components of the circadian system in Drosophila. Annu Rev Physiol 63: 729-755.
Wise S, Davis NT, Tyndale E, Noveral J, Folwell MG, Bedian V, Emery IF, and Siwicki KK (2002) Neuroanatomical studies of period gene expression in the hawkmoth, Manduca sexta. J Comp Neurol 447: 366-380.
Žo�itnan D, Sehnal F, and Bryant PJ (1993) Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev Biol 156: 117-135.

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Article first published: April 2003
Issue published: April 2003

Keywords

  1. insect brain clock
  2. circadian rhythm
  3. PER
  4. PDH
  5. PTTH
  6. EH
  7. insect neuroanatomy

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© 2003.
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PubMed: 12693866

Authors

Affiliations

Radka Závodská
University of South Bohemia
Ivo Šauman
Czech Academy of Sciences
František Sehnal
Czech Academy of Sciences

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