Exploring Octopamine: Immunohistochemical research of a spionid worm Pygospio elegans nervous system

Authors

  • Zinaida Starunova Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-9582-9668
  • Ksenia Shunkina Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-9257-1078
  • Elena Novikova Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, Saint Petersburg, 199034, Russian Federation; Department of Embryology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-3740-600X
  • Viktor Starunov Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-9001-2069

DOI:

https://doi.org/10.21638/spbu03.2024.106

Abstract

Octopamine is a biogenic amine specific for invertebrates distributed in all groups from Cnidaria to Echinodermata. Our study is aimed to investigate the octopamine-positive elements in the nervous system of the spionid worm Pygospio elegans. Immunohistochemistry was used to detect octopamine-positive elements in the central and peripheral nervous systems. While the central nervous system exhibited weak staining, the peripheral nervous system showed specifically octopamine-like elements in the palps, peristomium, and body segments. The detected octopamine-like elements were compared with other neurotransmitters in the P. elegans nervous system. Our results contribute to the data on annelid octopaminergic nervous system structure.

Keywords:

Pygospio elegans, nervous system, peripheral nervous system, octopamine, immunohistochemistry, confocal microscopy

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References

Adamo, S. A. and Baker, J. L. 2011. Conserved features of chronic stress across phyla: The effects of long-term stress on behavior and the concentration of the neurohormone octopamine in the cricket, Gryllus texensis. Hormones and Behavior 60(5):478–483. https://doi.org/10.1016/j.yhbeh.2011.07.015

Barmasova, G. A., Starunova, Z. I., Novikova, E. L., and Starunov, V. V. 2022. Organization of catecholaminergic system of Pygospio elegans and Platynereis dumerilii. Invertebrate Zoology 19(4):335–350. https://doi.org/10.15298/invert-zool.19.4.02

Barna, J., Csoknya, M., Lázár, Z., Barthó, L., Hámori, J., and Elekes, K. 2001. Distribution and action of some putative neurotransmitters in the stomatogastric nervous system of the earthworm, Eisenia fetida (Oligochaeta, Annelida). Journal of Neurocytology 30(4):313–325. https://doi.org/10.1023/a:1014456329814

Battelle, B. A., Calman, B. G., and Hart, M. K. 1999. Cellular distributions and functions of histamine, octopamine, and serotonin in the peripheral visual system, brain, and circumesophageal ring of the horseshoe crab Limulus polyphemus. Microscopy Research and Technique 44(2–3):70–80. https://doi.org/10.1002/(SICI)1097-0029(19990115/01)44:2/3%3C70::AID-JEMT2%3E3.0.CO;2-V

Belanger, J. H. and Orchard, I. 1986. Leydig cells: Octopaminergic neurons in the leech. Brain Research 382(2):387–391. https://doi.org/10.1016/0006-8993(86)91349-1

Busch, S., Selcho, M., Ito, K., and Tanimoto, H. 2009. A map of octopaminergic neurons in the Drosophila brain. The Journal of Comparative Neurology 513(6):643–667. https://doi.org/10.1002/cne.21966

Crisp, K. M., Klukas, K. A., Gilchrist, L. S., Nartey, A. J., and Mesce, K. A. 2002. Distribution and development of dopamine- and octopamine-synthesizing neurons in the medicinal leech. The Journal of Comparative Neurology 442(2):115–129. https://doi.org/10.1002/cne.10077

Csoknya, M., Barna, J., Banvolgyi, T., Hiripi, L., Eckert, M., Hamori, J., and Elekes, K. 1997. Octopamine-containing neurons in the alimentary tract of the earthworm (Eisenia fetida). Brain Research 778(2):414–417. https://doi.org/10.1016/S0006-8993(97)01117-7

Csoknya, M., Lengvari, I., Hiripi, L., Eckert, M., Rapus, J., and Elekes, K. 1996. Octopamine in the central nervous system of Oligochaeta: An immunocytochemical and biochemical study. Cell and Tissue Research 285(1):27–37. https://doi.org/10.1007/s004410050617

Ehinger, B. and Myhrberg, H. E. 1971. Neuronal localization of dopamine, noradrenaline and 5-hydroxytryptamine in the central and peripheral nervous system of Lumbricus terrestris (L.), Histochemie 28(4):265–275. https://doi.org/10.1007/BF00702632

Elekes, K., Eckert, M., and Rapus, J. 1993. Small sets of putative interneurons are octopamine-immunoreactive in the central nervous system of the pond snail, Lymnaea stagnalis. Brain Research 608(2):191–197. https://doi.org/10.1016/0006-8993(93)91458-5

Gallo V. P., Accordi, F., Chimenti, C., Civinini, A., and Crivellato, E. 2016. Catecholaminergic system of invertebrates: Comparative and evolutionary aspects in comparison with the octopaminergic system. The International Review of Cell and Molecular Biology 322:363–394. https://doi.org/10.1016/bs.ircmb.2015.12.006

Gilchrist, L. S., Klukas, K. A., Jellies, J., Rapus, J., Eckert, M., and Mesce, K. A. 1995. Distribution and developmental expression of octopamine-immunoreactive neurons in the central nervous system of the leech. The Journal of Comparative Neurology 353(3):451–463. https://doi.org/10.1002/cne.903530312

Hashemzadeh-Gargari, H. and Friesen, W. O. 1989. Modulation of swimming activity in the medicinal leech by serotonin and octopamine. Comparative Biochemistry & Physiology Part C: Toxicology and Pharmacology 94(1):295–302. https://doi.org/10.1016/0742-8413(89)90182-5

Karhunen, T., Airaksinen, M. S., Tuomisto, L., and Panula, P. 1993. Neurotransmitters in the nervous system of Macoma balthica (Bivalvia). The Journal of Comparative Neurology 334(3):477–488. https://doi.org/10.1002/cne.903340311

Long, T. F. and Murdock, L. L. 1983. Stimulation of blowfly feeding behavior by octopaminergic drugs. Proceedings of the National Academy of Sciences of the United States of America 80(13):4159–4163. https://doi.org/10.1073/pnas.80.13.4159

Orchard, I. 1982. Octopamine in insects: neurotransmitter, neurohormone, and neuromodulator. Canadian Journal of Zoology 60(4):659–669. https://doi.org/10.1139/z82-095

Pflüger, H.-J. and Stevenson, P. A. 2005. Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Structure & Development 34(3):379–396. https://doi.org/10.1016/j.asd.2005.04.004

Roeder, T. 1999. Octopamine in invertebrates. Progress in Neurobiology 59(5):533–561. https://doi.org/10.1016/s0301-0082(99)00016-7

Schneider, H., Trimmer, B. A., Rapus, J., Eckert, M., Valentine, D. E., and Kravitz, E. A. 1993. Mapping of octopamine-immunoreactive neurons in the central nervous system of the lobster. The Journal of Comparative Neurology 329(1):129–142. https://doi.org/10.1002/cne.903290109

Shunkina, K. V., Starunova, Z. I., Novikova, E. L., and Starunov V. V. 2023. Mass start or time trial? Structure of the nervous system and neuroregeneration in Pygospio elegans (Spionidae, Annelida). Biology 12(11):1412. https://doi.org/10.3390/biology12111412

Sinakevitch, I., Niwa, M., and Strausfeld, N. J. 2005. Octopamine-like immunoreactivity in the honey bee and cockroach: Comparable organization in the brain and subesophageal ganglion. The Journal of Comparative Neurology 488(3):233–254. https://doi.org/10.1002/cne.20572

Sombati, S. and Hoyle, G. 1984. Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. Journal of Neurobiology 15(6):481–506. https://doi.org/10.1002/neu.480150607

Starunova, Z. I., Shunkina, K. V., Novikova, E. L., and Starunov, V. V. 2022. Histamine and Gamma-aminobutyric acid in the nervous system of Pygospio elegans (Annelida: Spionidae). Structure and recovery during reparative regeneration. BMC Zoology 7(1):58. https://doi.org/10.1186/s40850-022-00160-7

Stevenson, P. A. and Pflüger, H. J. 1994. Colocalization of octopamine and FMRFamide related peptide in identified heart projecting (DUM) neurones in the locust revealed by immunocytochemistry. Brain Research 638(1–2):117–125. https://doi.org/10.1016/0006-8993(94)90640-8

Storch, V. and Gaill, F. 1986. Ultrastructural observations on feeding appendages and gills of Alvinella pompejana (Annelida, Polychaeta). Helgoland Marine Research 40:309–319. https://doi.org/10.1007/BF01983738

Vehovszky, Á., Elliott, C. J. H., Voronezhskaya, E. E., Hiripi, L., and Elekes, K. 1998. Octopamine: A new feeding modulator in Lymnaea. Philosophical Transactions of the Royal Society B 86(2):792–808. https://doi.org/10.1152/jn.2001.86.2.792

Zaitseva, O. V., Smirnov, R. V., Starunova, Z. I., Vedenin, A. A., and Starunov V. V. 2022. Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000. BMC Zoology 7(1):16. https://doi.org/10.1186/s40850-022-00114-z

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Published

2024-05-31

How to Cite

Starunova, Z., Shunkina, K., Novikova, E., & Starunov, V. (2024). Exploring Octopamine: Immunohistochemical research of a spionid worm <em>Pygospio elegans</em> nervous system. Biological Communications, 69(1), 50–55. https://doi.org/10.21638/spbu03.2024.106

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