Abstract
Labeling of 5-HT-immunoreactive structures was performed on eye slices of freshwater molluscs Lymnaea stagnalis and Pomacea canaliculata. In the periocular region of both species an increased density of 5-HTergic fibers forming structurally distinct plexuses and partially penetrating into the retina was detected. Transcription of serotonin receptor genes was detected in eye tissues: two types in L.stagnalis and three in P.canaliculata. Its relative level is significantly upregulated compared with central ganglia of the nervous system and tentacles. Additionally transcription of the 5HT transporter gene was recorded in P.canaliculata tissues.The obtained results are discussed in terms of a possible serotonergic mechanism of modulation of processes in the retina of gastropods.
References
Tierney AJ (2018) Invertebrate serotonin receptors: a molecular perspective on classification and pharmacology. J Exp Biol 221(Pt 19):jeb184838. s://doi.org/10.1242/jeb.184838
Bacqué-Cazenave J, Bharatiya R, Barrière G, Delbecque JP, Bouguiyoud N, Di Giovanni G, Cattaert D, De Deurwaerdère P (2020) Serotonin in Animal Cognition and Behavior. Int J Mol Sci 21(5):1649. s://doi.org/10.3390/ijms21051649
Sizemore TR, Hurley LM, Dacks AM (2020) Serotonergic modulation across sensory modalities. J Neurophysiol 123(6):2406–2425. s://doi.org/10.1152/jn.00034.2020
Yamoah EN, Crow T (1996) Protein kinase and G-protein regulation of Ca2+ currents in Hermissenda photoreceptors by 5-HT and GABA. J Neurosci 16(15):4799–4809. s://doi.org/10.1523/JNEUROSCI.16-15-04799.1996
Razy-Krajka F, Brown ER, Horie T, Callebert J, Sasakura Y, Joly JS, Kusakabe TG, Vernier P. (2012) Monoaminergic modulation of photoreception in ascidian: evidence for a proto-hypothalamo-retinal territory. BMC Biol 10:45. s://doi.org/10.1186/1741-7007-10-45
Colwell CS (1990) Light and serotonin interact in affecting the circadian system of Aplysia. J Comp Physiol A 167(6):841–845. s://doi.org/10.1007/BF00189772.
Masson J (2019) Serotonin in retina. Biochimie 161:51–55. s://doi.org/10.1016/j.biochi.2018.11.006.
Kito-Yamashita T, Haga C, Hirai K, Uemura T, Kondo H, Kosaka K (1990) Localization of serotonin immunoreactivity in cephalopod visual system. Brain Res 521(1-2):81–88. s://doi.org/10.1016/0006-8993(90)91527-n.
Takahashi JS, Nelson DE, Eskin A (1989) Immunocytochemical localization of serotonergic fibers innervating the ocular circadian system of Aplysia. Neuroscience 28(1):139–147. s://doi.org/10.1016/0306-4522(89)90238-8.
Michel S, Schoch K, Stevenson PA (2000) Amine and amino acid transmitters in the eye of the mollusc Bulla gouldiana: an immunocytochemical study. J Comp Neurol 425(2):244–256. s://doi.org/10.1002/1096-9861(20000918)425:2
Zhukov VV (2007) On the problem of retinal transmitters of the freshwater mollusc Lymnaea stagnalis. J Evol Biochem Phys 43:524–532. s://doi.org/10.1134/S0022093007050118
Zhukov VV, Tuchina OP, Meyer-RochowVB (2012) Serotonin immunoreactivity in the eye and optic nerve of pulmonate gastropod molluscs. J Evol Biochem Phys 48:471–473. s://doi.org/10.1134/S0022093012040123
Sugamori KS, Sunahara RK, Guan HC, Bulloch AG, Tensen CP, Seeman P, Niznik HB, Van Tol HH (1993) Serotonin receptor cDNA cloned from Lymnaea stagnalis. Proc Natl Acad Sci U S A 90(1):11–15. s://doi.org/10.1073/pnas.90.1.11
Gerhardt CC, Leysen JE, Planta RJ, Vreugdenhil E, Van Heerikhuizen H (1996) Functional characterisation of a 5-HT2 receptor cDNA cloned from Lymnaea stagnalis. Eur J Pharmacol 311(2-3):249–258. s://doi.org/10.1016/0014-2999(96)00410-4
Benatti C, Colliva C, Blom JMC, Ottaviani E, Tascedda F (2017) Transcriptional effect of serotonin in the ganglia of Lymnaea stagnalis. ISJ 14(1):251–258. s://doi.org/10.25431/1824-307X/isj.v14i1.251-258
OligoArchitectTM Online. Glossary of Parameters. https://www.sigmaaldrich.com/deepweb/assets/sigmaaldrich/marketing/global/documen ts/200/845/oligo-architect-glossary-br3011en-mk.pdf. (Date of address: 17.11.2022)
Young AP, Landry CF, Jackson DJ, Wyeth RC (2019). Tissue-specific evaluation of suitable reference genes for RT-qPCR in the pond snail, Lymnaea stagnalis. PeerJ 7:e7888. s://doi.org/10.7717/peerj.7888
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. s://doi.org/10.1006/meth.2001.1262
Gillette R (2006) Evolution and function in serotonergic systems. Integr Comp Biol 46(6):838–846. s://doi.org/10.1093/icb/icl024
Longley RD, Peterman M (2013) Neuronal control of pedal sole cilia in the pond snail Lymnaea stagnalis appressa. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 99(1):71–86. s://doi.org/10.1007/s00359-012-0770-x
Aonuma H, Mezheritskiy M, Boldyshev B, Totani Y, Vorontsov D, Zakharov I, Ito E, Dyakonova V (2020) The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis. Front Physiol 11:221. s://doi.org/10.3389/fphys.2020.00221
Жуков ВВ, Кононенко НЛ, Панормов ИБ., Борисенко ИЛ (2006) Серотонин изменяет электрические реакции глаза Lymnaea stagnalis на световую стимуляцию. Сенсорные системы 20(4): 270–278. [Zhukov VV, Kononenko NL, Panormov IB, Borisenko IL (2006) Serotonin izmenyaet elektricheskie reakcii glaza Lymnaea stagnalis na svetovuyu stimulyaciyu. Sensornye sistemy 20(4): 270-–278. (In Russ)].
Aonuma H, Totani Y, Sakakibara M, Lukowiak K, Ito E (2018) Comparison of brain monoamine content in three populations of Lymnaea that correlates with taste-aversive learning ability. Biophys Physicobiol 15:129–135. s://doi.org/10.2142/biophysico.15.0_129.
Horváth R, Battonyai I, Maász G, Schmidt J, Fekete ZN, Elekes K (2020) Chemical-neuroanatomical organization of peripheral sensory-efferent systems in the pond snail (Lymnaea stagnalis). Brain Struct Funct 225(8):2563–2575. s://doi.org/10.1007/s00429-020-02145-z
Ivashkin EG, Khabarova MYu, Melnikova VI, Kharchenko OA, Voronezhskaya EE (2017) Local serotonin-immunoreactive plexus in the female reproductive system of hermaphroditic gastropod mollusc Lymnaea stagnalis. Invertebrate Zoology14(2):134–139. s://doi.org/10.15298/invertzool.14.2.06
Azmitia EC (2007) Serotonin and brain: evolution, neuroplasticity, and homeostasis. Int Rev Neurobiol 77:31–56. s://doi.org/10.1016/S0074-7742(06)77002-7
Repérant J, Ward R, Miceli D, Rio JP, Médina M, Kenigfest NB, Vesselkin NP (2006) The centrifugal visual system of vertebrates: a comparative analysis of its functional anatomical organization. Brain Res Rev 52(1):1–57. s://doi.org/10.1016/j.brainresrev.2005.11.00
Rodríguez-Sosa L, Calderón-Rosete G, Villalobos MGP, Mendoza Zamora E, González VA (2006) Serotonin modulation of caudal photoreceptor in crayfish. Comp Biochem Physiol C Toxicol Pharmacol 142(3-4):220–230. s://doi.org/10.1016/j.cbpc.2005.10.006
Aréchiga H, Bañuelos E, Frixione E, Picones A, Rodríguez-Sosa L (1990) Modulation of crayfish retinal sensitivity by 5-hydroxytryptamine. J Exp Biol 150:123–143. s://doi.org/10.1242/jeb.150.1.123
Calderón-Rosete G, Flores G, Rodríguez-Sosa L (2006) Diurnal rhythm in the levels of the serotonin 5-HT1A receptors in the crayfish eyestalk. Synapse 59(6):368–373. s://doi.org/10.1002/syn.20252
Chen B, Meinertzhagen IA, Shaw SR (1999) Circadian rhythms in light-evoked responses of the fly's compound eye, and the effects of neuromodulators 5-HT and the peptide PDF. J Comp Physiol A 185(5):393–404. s://doi.org/10.1007/s003590050400
Muñoz JL, López Patiño MA, Hermosilla C, Conde-Sieira M, Soengas JL, Rocha F, Míguez JM (2011) Melatonin in octopus (Octopus vulgaris): tissue distribution, daily changes and relation with serotonin and its acid metabolite. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197(8):789–797. s://doi.org/10.1007/s00359-011-0641-x
Crow T, Bridge MS (1985) Serotonin modulates photoresponses in Hermissenda type-B photoreceptors. Neurosci Lett 60(1):83–88. s://doi.org/10.1016/0304-3940(85)90385-4
Farley J, Wu R (1989) Serotonin modulation of Hermissenda type B photoreceptor light responses and ionic currents: implications for mechanisms underlying associative learning. Brain Res Bull 22(2):335–351. s://doi.org/10.1016/0361-9230(89)90061-0
Grover LM, Farley J, Auerbach SB (1989) Serotonin involvement during in vitro conditioning of Hermissenda. Brain Res Bull 22(2):363–372. s://doi.org/10.1016/0361-9230(89)90063-4
Seyer JO, Nilsson DE, Warrant E (1998) Spatial vision in the prosobranch gastropod Ampularia sp. J Exp Biol 201 (Pt 10):1673–1679. s://doi.org/10.1242/jeb.201.10.1673
Zieger MV, Meyer-Rochow VB (2008) Understanding the cephalic eyes of pulmonate gastropods: A review. Amer Malac Bull 26: 47–66. s://doi.org/10.4003/006.026.0206
Block GD, Khalsa SB, McMahon DG, Michel S, Guesz M (1993) Biological clocks in the retina: cellular mechanisms of biological timekeeping. Int Rev Cytol146:83–144. s://doi.org/10.1016/s0074-7696(08)60381-2
Zhukov VV, Tuchina, OP (2008) Structure of visual pathways in the nervous system of freshwater pulmonate molluscs. J Evol Biochem Phys 44:341–353. s://doi.org/10.1134/S0022093008030113
Zaitseva OV (1994) Structural organization of the sensory systems of the snail. Neurosci Behav Physiol 24(1):47–57. s://doi.org/10.1007/BF02355652