Skip to main content
SpringerLink
Log in

Nerve–granular cell communication in the atrium of the snail Achatina achatina occurs via the cardioexcitatory transmitters serotonin and FMRFamide

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

In the present study, the anatomical association and functional interaction between nerve fibres and granular cells in the atrium of the snail Achatina achatina are investigated using a combination of scanning electron microscopy (SEM), pharmacological and immunofluorescence techniques. The SEM studies support a close anatomical association of axons with granular cells and new features of surface morphology are revealed. Pharmacological experiments showed that both serotonin and FMRFamide were able to induce degranulation of granular cells and the release of cysteine-rich atrial secretory protein. Serotonin- and FMRFamide-immunoreactive nerve fibres were observed at variable distances from granular cells, ranging from close contact to distances as far as the diameter of a muscle bundle. These results suggest that serotonin and FMRFamide play a role as paracrine excitatory transmitters in nerve-to-granular cell communication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akagawa M, Furukawa Y, Kobayashi M (1988) Dual effects of 5-hydroxytryptamine on the heart of a pulmonate, Achatina fulica Férussac. Comp Biochem Physiol C 89:327–331

    Article  Google Scholar 

  • Amsellem J, Nicaise G (1976) Distribution of the glio-interstitial system in molluscs. Cell Tissue Res 165:171–184

    Article  CAS  PubMed  Google Scholar 

  • Andrews EB (1976) The fine structire of the heart of some prosobranch and pulmonate snail in relation to filtration. J Molluscan Stud 42:199–216

    Google Scholar 

  • Andrews EB, Taylor PM (1988) Fine structure, mechanism of heart function and haemodynamics in the prosobranch gastropod molluscLittorina littorea (L.). J Comp Physiol B 158:247–262

    Article  Google Scholar 

  • Boyd PJ, Osborne NN, Walker RJ (1984) The pharmacological actions of 5-hydroxytryptamine, FMRF-amide and substance P and their possible occurrence in the heart of the snail Helix aspersa L. Neurochem Int 6:633–640

    Article  CAS  PubMed  Google Scholar 

  • Bystrova OA, Shabelnikov SV, Martynova MG (2014) The process of granule exocytosis in non-stimulated atrial granular cells of the snail, Achatina achatina: An ultrastructural, histochemical and immunocytochemical study. Acta Histochem 116:14–19

    Article  CAS  PubMed  Google Scholar 

  • Cottrell GA, Osborne N (1969) A neurosecretory system terminating in the Helix heart. Comp Biochem Physiol 28:1455–1459

    Article  Google Scholar 

  • Dieringer N, Koester J, Weiss KR (1978) Adaptive changes in heart rate of Aplysia californica. J Comp Physiol 123:11–21

    Article  Google Scholar 

  • Duval A, Runham NW (1981) The arterial system of six species of terrestrial slug. J Molluscan Stud 47:43–52

    Google Scholar 

  • Elekes K (2000) Ultrastructural aspects of peptidergic modulation in the peripheral nervous system of Helix pomatia. Microsc Res Tech 49:534–546

    Article  CAS  PubMed  Google Scholar 

  • Elekes K, Ude J (1994) Peripheral connections of FMRFamide-like immunoreactive neurons in the snail, Helix pomatia: an immunogold electron microscopic study. J Neurocytol 23:758–769

    Article  CAS  PubMed  Google Scholar 

  • Erdelyi L, Halasz N (1972) Electron-microscopical observations on the auricle of snail heart (Helix pomatia L.) with special regard to the structure of granulated cells. Acta Biol Szeged 18:253–267

    Google Scholar 

  • Fujimoto K, Ohta N, Yoshida M, Kubota I, Muneoka Y, Kobayashi M (1990) A novel cardio-excitatory peptide isolated from the atria of the African giant snail, Achatinafulica. Biochem Biophys Res Commun 167:777–783

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto k, Kubota I, Yasuda-Kamatani Y, Minakata H, Nomoto K, Yoshida M, Harada A, Muneoka Y, Kobayashi M (1991) Purification of achatin-I from the atria of the African giant snail, Achatina fulica, and its possible function. Biochem Biophys Res Commun 177:847–853

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara-Sakata M, Kobayashi M (1994) Localization of FMRFamide- and ACEP-1-like immunoreactivities in the nervous system and heart of a pulmonate mollusc, Achatina fulica. Cell Tissue Res 278:451–460

    Article  CAS  PubMed  Google Scholar 

  • Furukawa Y, Kobayashi M (1987a) Neural control of heart beat in the African giant snail, Achatina fulica Férussac: I. Identification of the heart regulatory neurones. J Exp Biol 129:279–293

    Google Scholar 

  • Furukawa Y, Kobayashi M (1987b) Neural control of heart beat in the African giant snail, Achatina fulica Ferussac: II Interconnections among the heart regulatory neurones. J Exp Biol 129:295–307

    Google Scholar 

  • Harris LL, Lesser W, Ono JK (1995) FMRFamide is endogenous to the Aplysia heart. Cell Tissue Res 282:331–341

    Article  CAS  PubMed  Google Scholar 

  • Haszprunar G, Wanninger A (2012) Molluscs. Curr Biol 22:R510–R514

    Article  CAS  PubMed  Google Scholar 

  • Hill RB (1987) Cardiovascular control in Mollusca. Experientia 43:953–956

    Article  Google Scholar 

  • Hill RB, Welsh JH (1966) Heart, circulation, and blood cells. In: Wilbur KM, Yonge CV (eds) Physiology of Mollusca, vol 2. Academic, San Diego, pp 125–174

  • Hori K, Furukawa Y, Kobayashi M (1990) Regulatory actions of 5-hydroxytryptamine and some neuropeptides on the heart of the African giant snail, Achatina fulica Ferussac: Physiology. Zool Sci 7:377–384

    CAS  Google Scholar 

  • Horsfield GI (1965) The effect of compound 48/80 on the rat mast cell. J Pathol Bacteriol 90:599–605

    Article  CAS  PubMed  Google Scholar 

  • Jones HD (1983) The circulatory systems of Gastropods and Bivalves. In: Wilbur KM, Saleuddin ASM (eds) The Mollusca, vol 5. Academic Press, San Diego, pp 189–238

    Chapter  Google Scholar 

  • Keith IM, Jin J, Saban R (1995) Nerve-mast cell interaction in normal guinea pig urinary bladder. J Comp Neurol 363:28–36

    Article  CAS  PubMed  Google Scholar 

  • Kodirov SA (2011) The neuronal control of cardiac functions in Molluscs. Comp Biochem Physiol A 160:102–116

    Article  CAS  Google Scholar 

  • Lambracht-Hall M, Konstantinidou AD, Theoharides TC (1990) Serotonin release from rat brain mast cells in vitro. Neuroscience 39:199–207

    Article  CAS  PubMed  Google Scholar 

  • Lee FO, Cheng TC (1971) Schistosoma mansoni infection in Biomphalaria glabrata: Alterations in heart rate and thermal tolerance in the host. J Invertebr Pathol 18:412–418

    Article  CAS  PubMed  Google Scholar 

  • Margulis L, Hinkle G (1992) Large symbiotic spyrochetes: Clevelandina, Cristispira, Diplocalyx, Hollandina, and Pillotina. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The Procaryotes. Springer, New York, pp 3965–3978

    Chapter  Google Scholar 

  • Martin AW (1983) Excretion. In: Wilbur KM, Saleuddin ASM (eds) The Mollusca, vol 5. Academic Press, San Diego, pp 353–405

    Chapter  Google Scholar 

  • Martynova MG (2004) Proliferation and differentiation processes in the heart muscle elements in different phylogenetic groups. International Review of Cytology, vol Volume 235. Academic, San Diego, pp 215-250

  • Martynova MG, Bystrova OA, Shabelnikov SV, Margulis BA, Prokofjeva DS (2007) Hsp70 in the atrial neuroendocrine units of the snail, Achatina fulica. Cell Biol Int 31:413–419

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Chápuli R, Carmona R, Guadix JA, Macías D, Pérez-Pomares JM (2005) The origin of the endothelial cells: an evo-devo approach for the invertebrate/vertebrate transition of the circulatory system. Evol Dev 7:351–358

    Article  PubMed  Google Scholar 

  • Nicaise G (1973) The gliointerstitial system of Molluscs. In: Bourne GH, Danielli JF (eds) International Review of Cytology, vol 34. Academic, San Diego, pp 251-332

  • Plesch B (1977) An ultrastructural study of the musculature of the pond snail Lymnaea stagnalis (L.). Cell Tissue Res 180:317–340

    Article  CAS  PubMed  Google Scholar 

  • Romero SMB, Hoffmann A (1996) Heart rate and temperature in the snail Megalobulimus sanctipauli: role of the cardiac nerve. Can J Physiol Pharmacol 74:1362–1365

    Article  CAS  PubMed  Google Scholar 

  • Romero SMB, Hoffmann A (2006) Role of the cardiac nerve in the effect of a novel innocuous stimulus on the heart rate of Megalobulimus mogianensis. Braz J Med Biol Res 39:833–837

    Article  CAS  PubMed  Google Scholar 

  • Romero SMB, Hoffmann A (2008) Role of the cardiac nerve in the adaptive changes of heart rate in response to an aversive stimulus in Megalobulimus mogianensis. Braz J Med Biol Res 41:432–436

    Article  CAS  PubMed  Google Scholar 

  • Rozniecki JJ, Dimitriadou V, Lambracht-Hall M, Pang X, Theoharides TC (1999) Morphological and functional demonstration of rat dura mater mast cell–neuron interactions in vitro and in vivo. Brain Res 849:1–15

    Article  CAS  PubMed  Google Scholar 

  • S.-Rózsa K (1979) Heart regulatory neural network in the central nervous system of Achatina fulica (férussac) (Gastropoda: Pulmonata). Comp Biochem Physiol A 63:435–445

    Article  Google Scholar 

  • S.-Rózsa K, Zs.-Nagy I (1967) Physiological and histochemical evidence for neuroendocrine regulation of heart activity in the snail Lymnaea stagnalis L. Comp Biochem Physiol 23:373–382

    Article  Google Scholar 

  • Schmidt G (1916) Blutgefäßsystem und mantelhöhle der weinbergschnecke (Helix pomatia). Z Wiss Zool 115:201–216

    Google Scholar 

  • Shabelnikov S, Kiselev A (2015) Cysteine-rich strial secretory protein from the snail Achatina achatina: purification and structural characterization. PLoS ONE 10:e0138787

    Article  PubMed  PubMed Central  Google Scholar 

  • Shabelnikov SV, Bystrova OA, Ivanov VA, Margulis BA, Martynova M (2009) Atrial granular cells of the snail Achatina fulica release proteins into hemolymph after stimulation of the heart nerve. J Exp Biol 212:3211–3220

    Article  CAS  PubMed  Google Scholar 

  • Sitnikova T, Michel E, Tulupova Y, Khanaev I, Parfenova V, Prozorova L (2012) Spirochetes in gastropods from Lake Baikal and North American freshwaters: new multi-family, multi-habitat host records. Symbiosis 56:103–110

    Article  Google Scholar 

  • Suzuki R, Furuno T, McKay DM, Wolvers D, Teshima R, Nakanishi M, Bienenstock J (1999) Direct neurite-mast cell communication in vitro occurs via the neuropeptide substance P. J Immunol 163:2410–2415

    CAS  PubMed  Google Scholar 

  • Suzuki A, Suzuki R, Furuno T, Teshima R, Nakanishi M (2004) N-Cadherin plays a role in the synapse-like structures between mast cells and neurites. Biol Pharm Bull 27:1891–1894

    Article  CAS  PubMed  Google Scholar 

  • Theoharides TC, Singh LK, Boucher W, Pang X, Letourneau R, Webster E, Chrousos G (1998) Corticotropin-releasing hormone Induces skin mast cell degranulation and increased vascular permeability, a possible explanation for its proinflammatory effects. Endocrinology 139:403–413

    CAS  PubMed  Google Scholar 

  • Volkmer-Ribeiro C (1970) Enterochromaffin properties of granular cells in the heart of the snails Helix aspersa and Strophocheilus oblongus. Comp Biochem Physiol 37:481–492

    Article  Google Scholar 

  • Weatherill D, Chase R (2005) Modulation of heart activity during withdrawal reflexes in the snail Helix aspersa. J Comp Physiol A 191:355–362

    Article  Google Scholar 

  • Wendelaar Bonga SE, Boer HH (1969) Ultrastructure of the reno-pericardial system in the pond snailLymnaea stagnalis (L.). Z Zellforsch Mikrosk Anat 94:513–529

    Article  CAS  PubMed  Google Scholar 

  • Weragoda RMS, Walters ET (2007) Serotonin induces memory-like, rapamycin-sensitive hyperexcitability in sensory axons of Aplysia that contributes to injury responses. J Neurophysiol 98:1231–1239

    Article  CAS  PubMed  Google Scholar 

  • Yasuda-Kamatani Y, Kobayashi M, Yasuda A, Fujita T, Minakata H, Nomoto K, Nakamura M, Sakiyama F (1997) A novel d-amino acid-containing peptide, fulyal, coexists with fulicin gene-related peptides in Achatina atria. Peptides 18:347–354

    Article  CAS  PubMed  Google Scholar 

  • Zhuravlev V, Bugaj V, Kodirov S, Safonova T, Staruschenko A (2001) Giant multimodal heart motoneurons of Achatina fulica: a new cardioregulatory input in pulmonates. Comp Biochem Physiol A 130:183–196

    Article  CAS  Google Scholar 

  • Zhuravlev V, Safonova T, Bugaj V, Kodirov S (2002) Mechanisms of viscerocardial reflexes in land pulmonate mollusc, Achatina fulica F. Zool Polon 47:5–19

    Google Scholar 

Download references

Acknowledgments

The author is grateful to Dr. Marina G. Martynova for helpful discussions. The author acknowledges Saint-Petersburg State University (http://eng.spbu.ru) for research grant 1.50.1042.2014 and the Russian Foundation for Basic Research (http://www.rfbr.ru) for research grant 16-04-00069.

Author information

Authors and Affiliations

  1. Department of Cytology and Histology, Saint-Petersburg State University, St. Petersburg, Russia

    Sergey Shabelnikov

  2. Laboratory of Cell Morphology, Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia

    Sergey Shabelnikov

Authors
  1. Sergey Shabelnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergey Shabelnikov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shabelnikov, S. Nerve–granular cell communication in the atrium of the snail Achatina achatina occurs via the cardioexcitatory transmitters serotonin and FMRFamide. Cell Tissue Res 366, 245–254 (2016). https://doi.org/10.1007/s00441-016-2483-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-016-2483-x

Keywords

Search

Navigation