Morphometric Analysis of Serotoninergic Structures in the Nervous System of Planarian Schmidtea mediterranea

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Abstract

The nervous system of planarians includes cerebral ganglia situated in the anterior part of the body and a pair of well-defined ventral nerve cords that extend throughout the whole animal. Serotoninergic components of the nervous system were determined by indirect method of immunocytochemical staining of whole mount tissue preparations of planarians Schmidtea mediterranea, followed by analysis using a fluorescence microscope. The results obtained show the presence of serotoninergic components in the central and peripheral parts of the nervous system of planarians S. mediterranea. The morphological parameters of serotonin-immunopositive structures were estimated, as well as neuron counts in the cerebral ganglion were done. The measurements were carried out on micrographs taken through a digital camera from stained whole mount preparations. The size of serotonin neurons in three areas of the body, the thickness of the nerve trunks and cerebral ganglion, and the distance between the nerve cords and transversal commissures were taken into consideration. For the first time, the new quantitative data were obtained characterizing the morphological properties of the nervous system of planarian S. mediterranea. Also, the observation of the eyes regeneration in planarians in response to decapitation and exposure to serotonin was performed. It was found that exogenous serotonin at concentrations of 0.01–1 μm accelerated eye differentiation during the regeneration of the head end of S. mediterranea planarian.

About the authors

G. V Kuznetsov

Institute of Cell Biophysics, Russian Academy of Sciences

Institutskaya ul. 3, Pushchino, Moscow Region, 142290 Russia

D. Е Mitkovskii

Serpukhov college

Centralnaya ul. 154, Serpukhov, Moscow Region, 142207 Russia

N. D Kreshchenko

Institute of Cell Biophysics, Russian Academy of Sciences

Email: nkreshch@rambler.ru
Institutskaya ul. 3, Pushchino, Moscow Region, 142290 Russia

References

  1. Е. А. Нервная система Anoplodium mediale (Turbellaria, Anoplodiidae). Паразитология, 20 (2), 149–151 (1986).
  2. Reuter M. and Gustafsson M. The flatworms nervous system – pattern and phylogeny. In: The nervous system of Invertebrate - Evolutionary and Comparative Approach., Ed. by O. Breidbach and W. Kutsch (Birkhauser Verlag, Basel, 1995), pp. 25−59.
  3. Evolution and regeneration of the planarian central nervous system. Develop. Growth Differ. Develop. Growth Differ., 51, 185–195 (2009). doi: 10.1111/j.1440-169X.2009.01099.x
  4. Durant F., Lobo D., Hammelman J., and Levin M., Physiological controls of large-scale patterning in planarian regeneration: a molecular and computational perspective on growth and form. Regeneration, 3 (2), 78–103 (2016). doi: 10.1002/reg2.54
  5. Chachain N. F., Abdulhadi F. S. and Mzhr N. N. Systems of the body as a planaria, biology, ecology and regeneration: a review. Biochem. Cell. Arch., 20 (1), 1619–1622 (2020).
  6. Крещенко Н. Д. Изучение механизмов действия FMRF-подобных пептидов на мышечное сокращение у планарий (Platyhelminthes). Биофизика, 66 (3), 555–566 (2021). doi: 10.31857/S0006302921030157
  7. Robb S. M. C., Gotting K., Ross E., and Sanchez Alvarado A. SmedGD 2.0: The Schmidtea mediterranea genome database. Genesis, 53 (8), 535–546 (2015). doi: 10.1002/dvg.22872
  8. Schmidt D., Reuter H., Hüttner K., Ruhe L., Rabert F., Seebeck F., Irimia M., Solana J., and Bartscherer K., The Integrator complex regulates differential snRNA processing and fate of adult stem cells in the highly regenerative planarian Schmidtea mediterranea. PLoS Genet., 14 (12), e1007828 (2018). doi: 10.1371/journal.pgen.1007828
  9. Bagunà J. Mitosis in the intact and regenerating planarian Dugesia mediterranea N. sp. J. Exp. Zool., 195 (1), 65–79 (1976).
  10. Kotikova E. A. Comparative characterization of the nervous system of the Turbellaria. Hydrobiologia, 132, 89–92 (1986).
  11. Котикова Е. А. Ортогон плоских червей и основные пути его эволюции. Морфологические основы филогенетики плоских червей. Тр. Зоол. инта АН СССР, 241, 88–111 (1991).
  12. Joffe B. I. and Reuter M. The nervous system of Bothriomolus balticus (Proseriata) − a contribution to the knowledge of the orthogon in the Plathelminthes. Zoomorphology, 113, 113–127 (1993).
  13. Reuter M., Maule A. G., Halton D. W., Gustafsson M. K. S., and Shaw C. The organization of the nervous system in Plathelminthes. The neuropeptide F-immunoreactive pattern in Catenulida, Macrostomida, Proceriata. Zoomorphology, 115, 83–97 (1995).
  14. Reuter M., Mäntylä K., and Gustafsson M. K. S. Organization of the orthogon – main and minor nerve cords. Hydrobiologia, 383, 175–182 (1998).
  15. Koopowitz H. Primitive Nervous Systems. A Sensory Nerve-Net in the Polyclad Flatworm Notoplana acticola. Biol. Bull., 145 (2), 352–359 (1973).
  16. Baguna J. and Ballester R. The nervous system in Planarians: peripheral and gastrodermal plexuses, pharynx innervation, and the relationship between central nervous system structure and the acoelomate organization. J. Morph., 155, 237–252 (1978).
  17. Reuter M. and Gustafsson M. K. S. “Neuorendocrine cells” in flatworms Progenitors to metazoan neurones? Arch. Histol. Cytol., 52, 253–263 (1989).
  18. Reuter M. and Halton D. W. Comparative neurobiology of Platyhelminthes. In: Interrelationships of Platyhelminthes, Ed. by D. T. J. Littlewood and R. A. Bray (Taylor & Francis, London, New York, 2001), pp. 239–249.
  19. Morita M. and Best J. B. Electron microscopic studies on Planaria. 11. Fine structure of the neurosecretory system in the planarian Dugesia dorotocephala. J. Ultrastruc. Res., 13 (5/6), 398–408 (1965).
  20. Lender T. The role of neurosecretion in freshwater planarians. In: Biology of the Turbellaria, Ed. by N. W. Riser and M. P. Morse (Mc Craw-Hill, London, 1974), pp. 460–475.
  21. Кудикина Н. П. Организация эндокринной функции у плоских червей. Вест. Балтийского федерального университета им. И. Канта, 7, 126–131 (2011).
  22. Тирас Х. П., Шейман И. М. и Сахарова Н. Ю. Активность АХЭ в нервной системе некоторых трикладид (класс ресничных червей). Журн. эволюц. биохимии и физиологии, 11 (4), 427–429 (1975).
  23. Котикова Е. А. и Иоффе Б. И. Катехоламины и холинэстеразы в нервной системе турбеллярии. Provortex karlingi. Журн. эволюц. биохимии и физиологии, 24 (2), 142148 (1988).
  24. Lentz T. L. Histochemical localization of acetylcholinesterase activity in a planarian. Comp. Biochem. Physiol., 27 (3), 715–716 (1968). doi: 10.1016/0010-406X(68)90612-9
  25. Erzen I. and Brzin M. Cholinergic mechanisms in Planaria torva. Comp. Biochem. Physiol., 64, 207–216 (1979). doi: 10.1016/0306-4492(79)90050-9
  26. Welsh J. H. and King E. C. Catecholamines in planarians. Comp. Biochem. Physiol., 36 (4), 683–686 (1970).
  27. Reuter M. and Eriksson K. Catecholamines demonstrated byglyoxylic acid-induced fluorescence and HPLC in same microturbellarians. Hydrobiologia, 227, 209–220 (1991).
  28. Joffe B. I. and Kotikova E. A. Distribution of catecholamines in turbellarians with a discussion of neuronal homologies in the Plathelminthes. In: Simpler Nervous Systems, Ed. by D. A. Sakharov, and W. Winlow (Manchester University Press, Manchester, NewYork, 1991), pp. 77–112.
  29. Wikgren M., Reuter M., Gustafsson M. K. S., and Lindroos P. Immunocytochemical localization of histamine in flatworms. Cell Tiss. Res., 260, 479–484 (1990). doi: 10.1007/BF00297227
  30. Eriksson K. S. Nitric oxide synthase in the pharynx of the planarian Dugesia tigrina. Cell Tiss. Res., 286, 407–410 (1996).
  31. Eriksson K. S. and Panula P. Gamma-aminobutyric acid in the nervous system of a planarian. J. Comp. Neurol., 345 (4), 528-533 (1994). doi: 10.1002/cne.903450405
  32. Nishimura K., Kitamura Y., Umesono Y., Takeuchi K., Takata K., Taniguchi T., and Agata K. Identification of glutamic acid decarboxylase gene and distribution of GABAergic nervous system in the planarian Dugesia japonica. Neuroscience, 153 (4), 1103-1114 (2008). doi: 10.1016/j.neuroscience.2008.03.026
  33. Shilt J., Richoux J. P., and Dubois M. P. Demonstration of peptides immunologically related to vertebrate neurogormones in Dugesia lugubris (Turbellaria, Tricladida). Gen. Comp. Endocrinol., 43 (3), 331-335 (1981).
  34. Carraway R., Ruane S. E. and Kim H.-R. Distribution and immunochemical character of neurotensin-like material in representative vertebrates and invertebrates: apparent conversation of the COOH-terminal region during evolution Peptides, 1, 115–123 (1982).
  35. Venturini G., Carolei A., Palladini G., Margotta V., and Lauro M. G. Radioimmunological and immunocytochemical demonstration of Met-enkephalin in planaria. Comp. Biochem. Physiol., 74, 23–25 (1983). doi: 10.1016/0742-8413(83)90141-x
  36. Kerschbaum H., Polhammer K., Hacker G., Treiblmayr K., and Adam H. Endorphin ähnliche Immunoreactivität bei Crenobia alpina (Turbellaria, Tricladida). Mikroskopie, 41, 30–33 (1984).
  37. Bautz A. and Shilt J. Somatostatin-like peptide and regeneration capacities in planarians. Gen. Comp. Endocrinol., 64, 267–272 (1986).
  38. Reuter M. Substance P immunoreactivity in sensory structures and the central and pharyngeal nervous system of Stenostomum leucops (Catenulida) and Microstomum lineare (Macrostomida). Cell Tiss. Res., 276, 173–180 (1994).
  39. Curry W. J., Shaw C., Johnston C. F., Thim L., and Buchanan K. D. Neuropeptide F: primary structure from the Turbellarian, Artioposthia triangulate. Comp. Biochem. Physiol., 110 (2), 269–274 (1992). doi: 10.1016/0742-8413(92)90272-9
  40. Johnston R. N., Shaw C., Halton D. W., Verhaert P., and Baguna J. GYIRFamide: a novel FMRFamide-related peptide (FaRP) from the triclad turbellarian, Dugesia tigrina. Biochem. Biophys. Res. Comm., 209, 689–697 (1995). doi: 10.1006/bbrc.1995.1554
  41. Johnston R. N., Shaw C., Halton D. W., Verhaert P.,Blair K. L., Brennan G. P., Price D. A., and Anderson P. A. Isolation, localization, and bioactivity of the FMRFamide-related neuropeptides GYIRFamide and YIRFamide from marine turbellarian Bdelloura candida. J. Neurochem., 67, 814–821 (1996). doi: 10.1046/j.1471-4159.1996.67020814.x
  42. Rapport M. M., Green A. A., and Page I. H. Crystalline Serotonin. Science, 108 (2804), 329–330 (1948).
  43. Gustafsson M. K., Fagerholm H. P., Halton D. W., Hanzelová V., Maule A. G., Reuter M., and Shaw C. Neuropeptides and serotonin in the cestode, Proteocephalus exiguus: an immunocytochemical study. Int. J. Parasitol., 25 (6), 673–682 (1995). doi: 10.1016/0020-7519(94)00169-o
  44. Tolstenkov O., Terenina N., Kreshchenko N., and Gustafsson M. The pattern of FMRFamide and serotonin immunoreactive elements in the nervous system of Aspidogaster conchicola К. Baer, 1827 (Aspidogastrea, Aspidogastridae). Belgian J. Zool., 144, 133–136 (2010).
  45. Плотникова С. И. и Кузьмина Л. В. Распределение нервных элементов, содержащих биогенные амины, у представителя плоских червей – молочно-белой планарии Dendrocoelum lacteum. В кн.: Физиология и биохимия беспозвоночных (Л.: Наука, 1968), сс. 23–29.
  46. Reuter M., Gustafsson M. K. S., Mäntylä K., and Grimmelikhuijzen C. J. P. The nervous system of Tricladida. III. Neuroanatomy of Dendrocoelum lacteum and Polycelis tenuis (Plathelminthes, Paludicola): an immunocytochemical study. Zoomorphology, 116, 111–122 (1996). doi: 10.1007/BF02526943
  47. Лурье Б. Л. Моноаминсодержащие нейроны планарии Polycelis nigra. Вестник МГУ. Сер. биол., 2, 3–13 (1975).
  48. Reuter M., Gustafsson M. K. S., Sheiman I. M., Terenina N., Halton D. W., Maule A. G., and Shaw C. The nervous system of Tricladida II. Neuroanatomy of Dugesia tigrina (Plaudicola, Dugesiidae): an immunocytochemical study. Invert. Neurosci., 1, 133–143 (1995). doi: 10.1007/BF02331911
  49. Itoh M. T. and Igarashi J. Circadian rhythm of sero-50. Fernandes M. C., Alvares E. P., Gama P., and Silveira M. Serotonin in the nervous system of the head region of the land planarian Bipalium kewense. Tissue Cell., 35 (6), 479–486 (2003). doi: 10.1016/s0040-8166(03)00074-0
  50. Kerschbaum H., Freiblmayer K., and Pohlhammer K. Localization of 5-HT and gastrin-cck-immunoreactivity Crenobia alpina (Tricladida, Plathelminthes). Fortschr. Zool., 36, 177 (1988).
  51. Kotikova E. A., Raikova O. I., Reuter M., and Gustafsson M. K. S. The nervous and muscular systems in the free-living flatworm Castrella truncata (Rhabdocoela): an immunocytochemical and phalloidin fluorescence study. Tissue Cell., 34 (5), 365–374 (2002).
  52. Kabotyanski E. A., Nezlin L. P., and Sakharov D. A. Serotonin neurons in planarian pharynx. Stud. Neurosci., 13, 138–152 (1991).
  53. Крещенко Н. Д. Иммуноцитохимическая идентификация серотонинергических нейронов у планарий Girardia tigrina. Биол. мембраны, 33 (5), 353–362 (2016).
  54. Cebrià F. Organization of the nervous system in the model planarian Schmidtea mediterranea: an immunocytochemical study. Neurosci. Res., 61 (4), 375–384 (2008).
  55. Крещенко Н. Д., Кузнецов Г. В., Митьковский Д. Е., Мочалова Н. В., Теренина Н. Б., Мовсесян С. О. Идентификация серотониновых нейронов у Hymenolepis diminuta и Schmidtea mediterranea c помощью конфокальной лазерной сканирующей микроскопии (CLSM). В сб. «Науч. труды VII съезда биофизиков России» (КубГТУ, Краснодар, 1, 2023), сс. 286–287. doi: 10.26297/SbR6.2023.001
  56. Prior D. J. and Uglem G. L. Behavioral and physiological aspects of swimming in cercariae of the digenetic trematode, Proterometra macrostoma. J. Exp. Biol., 83, 239–247 (1979).
  57. Hrckova G., Maule A., Velebny S., and Halton D. Mesocestoides corti (syn. M. vogae): Modulation of larval motility by neuropeptides, serotonin and acetylcholine. Parasitology, 124 (4), 409–421 (2002).
  58. Day T. A., Bennett J. L., and Pax R. A. Serotonin and its requirement for maintenance of contractility in muscle fibres isolated from Schistosoma mansoni. Parasitology, 108, 425–432 (1994).
  59. Ribeiro P., Gupta V., and El-Sakkary N. Biogenic amines and the control of neuromuscular signaling in schistosomes. Invertebr. Neuroscience, 12 (1), 13–28 (2012).
  60. Patocka N., Sharma N., Rashid M., and Ribeiro P. Serotonin signaling in Schistosoma mansoni: serotonintoninactivated G protein-coupled controls parasite movement. PLoS Pathog., 10 (1), e1003878 (2014). doi: 10.1371/journal.ppat.1003878
  61. Sakharov D. A., Golubev A. I., Malyutina L. V., Kabotyanski E. A., and Nezlin L. P. Serotoninergic control of ciliary locomotion in a turbellarian flatworm. In: Neurobiology of invertebrates: transmitters, modulators and receptors, Ed. by J. Salanki and K. S. Rózsa (Budapest, Akadémiai Kiadó, 1988), pp. 479–491.
  62. Franquinet R. The role of serotonin and catecholamines in the regeneration of the Planaria Polycelis tenuis. J. Embryol. Exp. Morphol., 51, 85–95 (1979).
  63. Шейман И. М., Крещенко Н. Д. и Нетреба М. В. Формирование функции фоторецепторной системы на ранних этапах развития. Биофизика, 55 (4), 680–685 (2010).
  64. Крещенко Н. Д., Гребенщикова Е. В. и Карпов А. Н. Влияние серотонина на регенерацию фоторецепторов планарий. В кн.: Сб. науч. статей по мат. межд. науч. конф. «Теория и практика борьбы с паразитарными болезнями» 20, 278–283 (2019). doi: 10.31016/978-5-9902340-8-6.2019.20
  65. Lambrus B. G., Cochet-Escartin O., Gao J., Newmark P. A., Collins E. M., and Collins J. J. Tryptophan hydroxylase is required for eye melanogenesis in the Planarian Schmidtea mediterranea. PLoS One, 10, e0127074 (2015). doi: 10.1371/journal.pone.0127074

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