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Coelomocyte replenishment in adult Asterias rubens: the possible ways

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Abstract

The origin of cells involved in regeneration in echinoderms remains an open question. Replenishment of circulatory coelomocytes—cells of the coelomic cavity in starfish—is an example of physiological regeneration. The coelomic epithelium is considered to be the main source of coelomocytes, but many details of this process remain unclear. This study examined the role of coelomocytes outside circulation, named marginal coelomocytes and small undifferentiated cells of the coelomic epithelium in coelomocyte replenishment in Asterias rubens. A qualitative and quantitative comparison of circulatory and marginal coelomocytes, as well as changes of circulatory coelomocyte concentrations in response to injury at different physiological statuses, was analysed. The presence of cells morphologically similar to coelomocytes in the context of coelomic epithelium was evaluated by electron microscopy. The irregular distribution of small cells on the surface and within the coelomic epithelium was demonstrated and the origin of small undifferentiated cells and large agranulocytes from the coelomic epithelium was suggested. Two events have been proposed to mediate the replenishment of coelomocytes in the coelom: migration of mature coelomocytes of the marginal cell pool and migration of small undifferentiated cells of the coelomic epithelium. The proteomic analysis of circulatory coelomocytes, coelomic epithelial cells and a subpopulation of coelomic epithelial cells, enriched in small undifferentiated cells, revealed proteins that were common and specific for each cell pool. Among these molecules were regulatory proteins, potential participants of regenerative processes.

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References

  • Alvarado AS, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7(11):873–884

    CAS  Google Scholar 

  • Araki T, Milbrandt J (1996) Ninjurin, a novel adhesion molecule, is induced by nerve injury and promotes axonal growth. Neuron 17:353–361

    CAS  PubMed  Google Scholar 

  • Bateman A, Bennet HPJ (2009) The granulin gene family: from cancer to dementia. BioEssays 31:1245–1254

    CAS  PubMed  Google Scholar 

  • Ben Khadra Y, Ferrario C, Benedetto CD, Said K, Bonasoro F, Candia Carnevali MD, Sugni M (2015a) Wound repair during arm regeneration in the red starfish Echinaster sepositus. Wound Rep Reg 23(4):611–622

    Google Scholar 

  • Ben Khadra Y, Ferrario C, Benedetto CD, Said K, Bonasoro F, Carnevali MD, Sugni M (2015b) Re–growth, morphogenesis, and differentiation during starfish arm regeneration. Wound Repair Regen 23(4):623–634

    PubMed  Google Scholar 

  • Ben Khadra Y, Sugni M, Ferrario C, Bonasoro B, Coelho AV, Martinez P, Candia Carnevali MD (2017) An integrated view of asteroid regeneration: tissues, cells and molecules. Cell Tiss Res 370(1):13–28

    CAS  Google Scholar 

  • Ben Khadra Y, Sugni M, Ferrario C, Bonasoro F, Oliveri P, Martinez P, Candia Carnevali MD (2018) Regeneration in stellate echinoderms: Crinoidea, Asteroidea and Ophiuroidea. Results Probl Cell Differ 65:285–320

    CAS  PubMed  Google Scholar 

  • Blanpain C, Fuchs E (2014) Plasticity of epithelial stem cells in tissue regeneration. Science 344(6189):1242281

    PubMed  PubMed Central  Google Scholar 

  • Blowes LM, Egertová M, Liu Y, Davis GR, Terrill NJ, Gupta HS, Elphick MR (2017) Body wall structure in the starfish Asterias rubens. J Anat 231(3):325–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burke RD (1999) Invertebrate integrins: structure, function, and evolution. Int Rev Cytol 191:257–284

    CAS  PubMed  Google Scholar 

  • Candelaria AG, Murray G, File SK, García-Arrarás JE (2006) Contribution of mesenterial muscle dedifferentiation to intestine regeneration in the sea cucumber Holothuria glaberrima. Cell Tissue Res 1:55–65

    Google Scholar 

  • Candia Carnevali MD (2006) Regeneration in Echinoderms: repair, regrowth, cloning. ISJ 3:64–76

    Google Scholar 

  • Candia-Carnevali MD, Thorndyke MC, Matranga V (2009) Regenerating Echinoderms: a promise to understand stem cells potential. In: Rinkevich B, Matranga V (eds) Stem cells in marine organisms. SpringerLink, London, pp 165–186

    Google Scholar 

  • Chi C, Liu JY, Fei S, Zhang C, Chang YQ, Liu XL, Wang GX (2014) Effect of intestinal autochthonous probiotics isolated from the gut of sea cucumber (Apostichopus japonicus) on immune response and growth of A. japonicas. Fish Shellfish Immunol 38(2):367–373

    CAS  PubMed  Google Scholar 

  • Chia FS, Xing J (1996) Echinoderm coelomocytes. Zool Stud 35(4):231–254

    Google Scholar 

  • Dogel VA (1981) Zoology of invertebrates (7th ed), Higher school, Moscow:606 (in Russian)

  • Dolmatov IY, Ferreri P, Bonasoro F, Candia Carnevali MD (2003) Visceral regeneration in the crinoid Antedon mediterranea. In: Feral JP, Bruno D (eds) Echinoderm research 2001. Balkema, Rotterdam, pp 215–220

    Google Scholar 

  • Eliseikina MG, Magarlamov TY (2002) Coelomocyte morphology in the holothurians Apostichopus japonicus (Aspidochirota: Stichopodidae) and Cucumaria japonica (Dendrochirotida: Cucumariidae). Russ J Mar Biol 28(3):197–202

    Google Scholar 

  • Eliseikina MG, Magarlamov TYu, Dolmatov IYu (2010) Stem cells of holothuroid coelomocytes. In: Harris LG, Bottger SA, Walker CW, Lesser MP (eds) Echinoderms: Proceedings from the 12th International Echinoderm Conference, August 2006, Durham, New Hampshire. Routledge:504

  • Fox RG, Park FD, Koechlein CS, Kritzik M, Reya (2015) Musashi signaling in stem cells and cancer. Annu Rev Cell Dev Biol 31:249–267

  • Franco CF, Santos R, Coelho AV (2011a) Exploring the proteome of an echinoderm nervous system: 2DE of the sea star radial nerve cord and the synaptosomal membranes subproteome. Proteomics 11:1359–1364

    CAS  PubMed  Google Scholar 

  • Franco CF, Santos R, Coelho AV (2011b) Proteome characterization of starfish coelomocytes–the innate immune effector cells of echinoderms. Proteomics 11:3587–3592

    CAS  PubMed  Google Scholar 

  • Franco C, Soares R, Pires E, Koci K, Almeida AM, Santos R, Coelho AV (2013) Understanding regeneration through proteomics. Proteomics 13(3–4):686–709

    CAS  PubMed  Google Scholar 

  • García-Arrarás JE, Dolmatov IY (2010) Echinoderms: potential model systems for studies on muscle regeneration. Curr Pharm Des 16(8):942–955

    PubMed  PubMed Central  Google Scholar 

  • Gorshkov AN, Blinova MI, Pinaev GP (2009) Ultrastructure of coelomic epithelium and coelomocytes of the starfish Asterias rubens L. in norm and after wounding. Cell Tiss Biol (Moscow) 3(5):477–490

    Google Scholar 

  • Gu M, Ma H, Mai K, Zhang W, Bai N, Wang X (2011) Effects of dietary b-glucan, mannan oligosaccharide and their combinations on growth performance, immunity and resistance against Vibrio splendidus of sea cucumber, Apostichopus japonicas. Fish Shellfish Immunol 31(2):303–309

    CAS  PubMed  Google Scholar 

  • Hennebert E, Leroy B, Wattiez R, Ladurner P (2015) An integrated transcriptomic and proteomic analysis of sea star epidermal secretions identifies proteins involved in defense and adhesion. J Proteome 128:83–91

    CAS  Google Scholar 

  • Holland ND, Phillips JH, Giese AC (1965) An autoradiographic investigation of coelomocyte production in the purple sea urchin (Strongylocentrotus purpuratus). Biol Bull 128:259–270

    Google Scholar 

  • Holm K, Dupont S, Skold H, Stenius A, Thorndyke M, Hernroth B (2008) Induced cell proliferation in putative haematopoietic tissues of the sea star, Asterias rubens (L.). J Exp Biol 211:2551–2558

    PubMed  Google Scholar 

  • Jangoux M, Vanden Bossche J-P (1975) Morphology and dynamics of the coelomocytes of Asterias rubens L. (Echinodermata, Asteroidea). Forma Functio 8:191–208

    Google Scholar 

  • Kaneshiro ES, Karp RD (1980) The ultrastructure of coelomocytes of the sea star Dermasterias imbricata. Biol Bull 159(2):295–310

    Google Scholar 

  • Kanungo KT (1982) In vitro studies on the effect of cell–free coelomic fluid, calcium, and/or magnesium on clumping of coelomocytes of the sea star Asterias forbesi (Echinodermata: Asteroidea). Biol Bull 163:438–452

    CAS  Google Scholar 

  • Klonz A, Wonigeit K, Pabst R, Westermann J (1996) The marginal blood pool of the rat contains not only granulocytes, but also lymphocytes, NK-cells and monocytes: a second intravascular compartment, its cellular composition, adhesion molecule expression and interaction with the peripheral blood pool. Scand J Immunol 44:461–469

    CAS  PubMed  Google Scholar 

  • Kozlova AB, Petukhova OA, Pinaev GP (2006) The analysis of cellular elements in coelomic fluid during early regeneration of the starfish Asterias rubens L. Tsitologiia 48:175–183 (in Russian)

    CAS  PubMed  Google Scholar 

  • Ma Y, Liu Z, Yang Z, Li M, Liu J, Song J (2013) Effects of dietary live yeast Hanseniaspora opuntiae C21 on the immune and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicas. Fish Shellfish Immunol 34(1):66–73

    CAS  PubMed  Google Scholar 

  • Mashanov VS, Garcia-Arraras JE (2011) Gut regeneration in holothurians: a snapshot of recent developments. Biol Bull 221:93–109

    CAS  PubMed  Google Scholar 

  • Mashanov VS, Dolmatov IY, Heinzeller T (2005) Transdifferentiation in holothurian gut regeneration. Biol Bull 209:184–193

    PubMed  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2014) Transcriptomic changes during regeneration of the central nervous system in an echinoderm. BMC Genomics 12(15):357

    Google Scholar 

  • Mashanov VS, Zueva OR, Garcia-Arraras JE (2015a) Expression of pluripotency factors in echinoderm regeneration. Cell Tiss Res 359(2):521–536

    CAS  Google Scholar 

  • Mashanov VS, Zueva OR, García-Arrarás JE (2015b) Heterogeneous generation of new cells in the adult echinoderm nervous system. Front Neuroanat 9:123

    PubMed  PubMed Central  Google Scholar 

  • Mashanov V, Zueva O, Mashanova D, García-Arrarás JE (2017) Expression of stem cell factors in the adult sea cucumber digestive tube. Cell Tiss Res 370(3):427–440

    CAS  Google Scholar 

  • Mayorova TD, Tian S, Cai W, Semmens DC, Odekunle EA, Zandawala M, Badi Y, Rowe ML, Egertová M, Elphick MR (2016) Localization of neuropeptide gene expression in larvae of an echinoderm, the starfish Asterias rubens. Front Neurosci 10:553

    PubMed  PubMed Central  Google Scholar 

  • Mladenov PV, Bisgrove B, Asotra S, Burke RD (1989) Mechanisms of arm tip regeneration in the sea star, Leptasterias hexactis. Rouxs Arch Dev Biol 198:19–28

    PubMed  Google Scholar 

  • Mozzi D, Dolmatov IY, Bonasoro F, Carnevali MD (2006) Visceral regeneration in the crinoid Antedon mediterranea: basic mechanisms, tissues and cells involved in gut regrowth. Cent Eur J Biol 1:609–635

    Google Scholar 

  • Müller UC, Zheng H (2012) Physiological functions of APP family proteins. Cold Spring Harb Perspect 4:a006288

    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(4):351–358

    PubMed  Google Scholar 

  • Nusse R (2005) Wnt signalling in disease and in development. Cell Res 15(1):28–32

    CAS  PubMed  Google Scholar 

  • Okano H, Imai T, Okabe M (2002) Musashi: a translational regulator of cell fate. J Cell Sci 115:1355–1359

    CAS  PubMed  Google Scholar 

  • Pellettieri J, Alvarado A (2007) Cell turnover and adult tissue homeostasis: from humans to planarians. Annu Rev Genet 41:83–105

    CAS  PubMed  Google Scholar 

  • Petukhova O, Sharlaimova N, Shabelnikov S, Bobkov D, Martynova M, Bystrova O (2018) Small undifferentiated cells from starfish Asterias rubens L.: candidates to the role of progenitor cells. Invert Surviv J 15:111–112

    Google Scholar 

  • Pinsino A, Thorndyke MC, Matranga V (2007) Coelomocytes and post–traumatic response in the common sea star Asterias rubens. Cell Stress Chaperones 12:331–341AR

  • Reinardy HC, Emerson CE, Manley JM, Bodnar AG (2015) Tissue regeneration and biomineralization in sea urchins: role of Notch signaling and presence of stem cell markers. PLoS One 10(8):e0133860

    PubMed  PubMed Central  Google Scholar 

  • Rinkevich B, Matranga V (Eds.) (2009) Stem cells in marine organisms. Heidelberg: Springerlink, London, 367 pp.

  • Rossi L, Bonuccelli L, Iacopetti P, Evangelista M, Ghezzani C, Tana L, Salvetti A (2014) Prohibitin 2 regulates cell proliferation and mitochondrial cristae morphogenesis in planarian stem cells. Stem Cell Rev and Rep (2014) 10(6):871–887

    CAS  Google Scholar 

  • Sanchez-Madrid F, del Pozo MA (1999) Leukocyte polarization in cell migration and immune interactions. EMBO J 18(3):501–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schoenmakers HJN, Colenbrander PHJM, Peute J, van Oordt PGWJ (1981) Anatomy of the ovaries of the starfish Asterias rubens (Echinodermata): a histological and ultrastructural study. Cell Tiss Res 217:577–597

    CAS  Google Scholar 

  • Shabelnikov SV, Bobkov DE, Sharlaimova NS, Petukhova OA (2019) Injury affects coelomic fluid proteome of the common starfish, Asterias rubens. J Exp Biol 6:222

    Google Scholar 

  • Sharlaimova NS, Petukhova OA (2012) Characteristics of populations of the coelomic fluid and coelomic epithelium cells from the starfish Asterias rubens L. able attach to and spread on various substrates. Cell Tiss Biol 6(2):176–188

    Google Scholar 

  • Sharlaimova NS, Pinaev GP, Petukhova OA (2010) Comparative analysis of behavior and proliferative activity in culture of cells of coelomic fluid and of cells of various tissues of the sea star Asterias rubens L. isolated from normal and injured animals. Cell Tiss Biol 4(3):280–288

    Google Scholar 

  • Sharlaimova N, Shabelnikov S, Petukhova O (2014) Small coelomic epithelial cells of the starfish Asterias rubens L. that are able to proliferate in vivo and in vitro. Cell Tiss Res 356(1):83–95

    CAS  Google Scholar 

  • Smith VJ (1981) The echinoderms. In: Ratcliffe NA, Rowley T (eds) Invertebrate blood cells. Academic Press, London, pp 513–562

    Google Scholar 

  • Steppich B, Dayyani F, Gruber R, Lorenz R, Mack M, Ziegler-Heitbrock HWL (2000) Selective mobilization of CD14(+) CD16(+) monocytes by exercise. Am J Physiol Cell Physiol 279:578–586

    Google Scholar 

  • Suárez-Castillo EC, García-Arrarás JE (2007) Molecular evolution of the ependymin protein family: a necessary update. BMC Evol Biol 7:23

    PubMed  PubMed Central  Google Scholar 

  • Vanden Bossche JP, Jangoux M (1976) Epithelial origin of starfish coelomocytes. Nature 261:227–228

    CAS  PubMed  Google Scholar 

  • Wang J, Guo C, Liu S, Qi H, Yin Y, Liang R, Sun MZ, Greenaway FT (2014) Annexin A11 in disease. Clin Chim Acta 431:164–168

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to the administration and staff of the White Sea Biological Station “Kartesh” of the Zoological Institute, Russian Academy of Sciences, for providing the conditions for the work and very valuable assistance.

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 15-04-07798 А), by the granting program “Molecular and cell biology” of the Russian Academy of Science (registration number AAAA-A17-117122790092-9).

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Authors and Affiliations

  1. Collection of Vertebrate Cell Cultures, Institute of Cytology, Russian Academy of Sciences, Tikhoretsky Ave. 4, St. Petersburg, Russian Federation, 194064

    Natalia Sharlaimova, Dan Bobkov & Olga Petukhova

  2. Cell Technologies Centre, Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russian Federation

    Sergey Shabelnikov

  3. Laboratory of Cell Morphology, Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russian Federation

    Marina Martynova & Olga Bystrova

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  1. Natalia Sharlaimova
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  2. Sergey Shabelnikov
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Correspondence to Olga Petukhova.

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No human subjects were involved in the study. The Asterias rubens is not regulated or endangered species.

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Sharlaimova, N., Shabelnikov, S., Bobkov, D. et al. Coelomocyte replenishment in adult Asterias rubens: the possible ways. Cell Tissue Res 383, 1043–1060 (2021). https://doi.org/10.1007/s00441-020-03337-z

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