Skip to main content

Advertisement

Log in

Novel markers identify nervous system components of the holothurian nervous system

  • Original Paper
  • Published:
Invertebrate Neuroscience

Abstract

Echinoderms occupy a key position in the evolution of deuterostomes. As such, the study of their nervous system can shed important information on the evolution of the vertebrate nervous system. However, the study of the echinoderm nervous system has lagged behind when compared to that of other invertebrates due to the lack of tools available. In this study, we tested three commercially available antibodies as markers of neural components in holothurians. Immunohistological experiments with antibodies made against the mammalian transcription factors Pax6 and Nurr1, and against phosphorylated histone H3 showed that these markers identified cells and fibers within the nervous system of Holothuria glaberrima. Most of the fibers recognized by these antibodies were co-labeled with the well-known neural marker, RN1. Additional experiments showed that similar immunoreactivity was found in the nervous tissue of three other holothurian species (Holothuria mexicana, Leptosynapta clarki and Sclerodactyla briareus), thus extending our findings to the three orders of Holothuroidea. Furthermore, these markers identified different subdivisions of the holothurian nervous system. Our study presents three additional markers of the holothurian nervous system, expanding the available toolkit to study the anatomy, physiology, development and evolution of the echinoderm nervous system.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agca C, Elhajj MC, Klein WH, Venuti JM (2011) Neurosensory and neuromuscular organization in tube feet of the sea urchin Strongylocentrotus purpuratus. J Comp Neurol 519(17):3566–3579. doi:10.1002/cne.22724

    Article  PubMed  Google Scholar 

  • Bishop CD, Burke RD (2007) Ontogeny of the holothurian larval nervous system: evolution of larval forms. Dev Genes Evol 217(8):585–592. doi:10.1007/s00427-007-0169-9

    Article  PubMed  Google Scholar 

  • Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T et al (2006a) A genomic view of the sea urchin nervous system. Dev Biol 300(1):434–460. doi:10.1016/j.ydbio.2006.08.007

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Burke RD, Osborne L, Wang D, Murabe N, Yaguchi S, Nakajima Y (2006b) Neuron-specific expression of a synaptotagmin gene in the sea urchin Strongylocentrotus purpuratus. J Comp Neurol 496(2):244–251. doi:10.1002/cne.20939

    Article  PubMed  CAS  Google Scholar 

  • Byrne M, Cisternas P (2002) Development and distribution of the peptidergic system in larval and adult Patiriella: comparison of sea star bilateral and radial nervous systems. J Comp Neurol 451(2):101–114. doi:10.1002/cne.10315

    Article  PubMed  CAS  Google Scholar 

  • Chee F, Byrne M (1999) Development of the larval serotonergic nervous system in the sea star Patiriella regularis as revealed by confocal imaging. Biol Bull 197:123–131

    Article  Google Scholar 

  • Cobb JL (1978) An ultrastructural study of the dermal papulae of the starfish, Asterias rubens, with special reference to innervation of the muscles. Cell Tissue Res 187(3):515–523

    Article  PubMed  CAS  Google Scholar 

  • Cottrell GA, Pentreath VW (1970) Localization of catecholamines in the nervous system of a starfish, Asterias rubens, and of a brittlestar, Ophiothrix fragilis. Comp Gen Pharmacol 1(1):73–81

    Article  PubMed  CAS  Google Scholar 

  • Czerny T, Busslinger M (1995) DNA-binding and transactivation properties of Pax-6: three amino acids in the paired domain are responsible for the different sequence recognition of Pax-6 and BSAP (Pax-5). Mol Cell Biol 15(5):2858–2871

    PubMed  CAS  PubMed Central  Google Scholar 

  • Diaz-Balzac CA, Santacana-Laffitte G, San Miguel-Ruiz JE, Tossas K, Valentin-Tirado G, Rives-Sanchez M et al (2007) Identification of nerve plexi in connective tissues of the sea cucumber Holothuria glaberrima by using a novel nerve-specific antibody. Biol Bull 213(1):28–42

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Balzac CA, Abreu-Arbelo JE, Garcia-Arraras JE (2010a) Neuroanatomy of the tube feet and tentacles in Holothuria glaberrima (Holothuroidea, Echinodermata). Zoomorphology 129(1):33–43. doi:10.1007/s00435-009-0098-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Diaz-Balzac CA, Mejias W, Jimenez LB, Garcia-Arraras JE (2010b) The catecholaminergic nerve plexus of Holothuroidea. Zoomorphology 129(2):99–109. doi:10.1007/s00435-010-0103-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Diaz-Balzac CA, Lazaro-Pena MI, Garcia-Rivera EM, Gonzalez CI, Garcia-Arraras JE (2012) Calbindin-D32k is localized to a subpopulation of neurons in the nervous system of the sea cucumber Holothuria glaberrima (Echinodermata). PLoS One 7(3):e32689. doi:10.1371/journal.pone.0032689

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Diaz-Miranda L, Blanco RE, Garcia-Arraras JE (1995) Localization of the heptapeptide GFSKLYFamide in the sea cucumber Holothuria glaberrima (Echinodermata): a light and electron microscopic study. J Comp Neurol 352(4):626–640. doi:10.1002/cne.903520410

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Miranda L, Pardo-Reoyo CF, Martinez R, Garcia-Arraras JE (1996) Galanin-like immunoreactivity in the sea cucumber Holothuria glaberrima. Cell Tissue Res 286(3):385–391

    Article  PubMed  CAS  Google Scholar 

  • Dupont S, Thorndyke W, Thorndyke MC, Burke RD (2009) Neural development of the brittlestar Amphiura filiformis. Dev Genes Evol 219(3):159–166. doi:10.1007/s00427-009-0277-9

    Article  PubMed  Google Scholar 

  • Elphick MR, Newman SJ, Thorndyke MC (1995) Distribution and action of SALMFamide neuropeptides in the starfish Asterias rubens. J Exp Biol 198(Pt 12):2519–2525

    PubMed  CAS  Google Scholar 

  • Friocourt G, Kanatani S, Tabata H, Yozu M, Takahashi T, Antypa M et al (2008) Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J Neurosci 28(22):5794–5805. doi:10.1523/JNEUROSCI.1067-08.2008

    Article  PubMed  CAS  Google Scholar 

  • García-Arrarás JE (1993) Localization of peptides: double-labeling immunohistochemistry. In: De Pablo F, Scanes C, Weintraub B (eds) Handbook of endocrine research treatment. Academic Press, San Diego, pp 207–225

    Google Scholar 

  • Garcia-Arraras JE, Diaz-Miranda L, Torres II, File S, Jimenez LB, Rivera-Bermudez K et al (1999) Regeneration of the enteric nervous system in the sea cucumber Holothuria glaberrima. J Comp Neurol 406(4):461–475

    Article  PubMed  CAS  Google Scholar 

  • Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM et al (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354(6354):522–525. doi:10.1038/354522a0

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa T, Komatsu M, Nakajima Y (2008) Development of the nervous system in the brittle star Amphipholis kochii. Dev Genes Evol 218(1):15–21. doi:10.1007/s00427-007-0196-6

    Article  PubMed  Google Scholar 

  • Hoekstra LA, Moroz LL, Heyland A (2012) Novel insights into the echinoderm nervous system from histaminergic and FMRF aminergic-like cells in the sea cucumber Leptosynapta clarki. PLoS One 7(9):e44220. doi:10.1371/journal.pone.0044220

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hyman LH (1955) The invertebrates: echinodermata, vol 4. McGraw-Hill, New York

    Google Scholar 

  • Inoue M, Tamori M, Motokawa T (2002) Innervation of holothurian body wall muscle: inhibitory effects and localization of 5-HT. Zool Sci 19(11):1217–1222

    Article  PubMed  CAS  Google Scholar 

  • Karashima T, Sugimoto A, Yamamoto M (2000) Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127(5):1069–1079

    PubMed  CAS  Google Scholar 

  • Katow H, Elia L, Byrne M (2009) Development of nervous systems to metamorphosis in feeding and non-feeding echinoid larvae, the transition from bilateral to radial symmetry. Dev Genes Evol 219(2):67–77. doi:10.1007/s00427-008-0266-4

    Article  PubMed  Google Scholar 

  • Lesser MP, Carleton KL, Bottger SA, Barry TM, Walker CW (2011) Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. Proc Biol Sci 278(1723):3371–3379. doi:10.1098/rspb.2011.0336

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Murabe N, Hatoyama H, Hase S, Komatsu M, Burke RD, Kaneko H et al (2008) Neural architecture of the brachiolaria larva of the starfish, Asterina pectinifera. J Comp Neurol 509(3):271–282. doi:10.1002/cne.21742

    Article  PubMed  CAS  Google Scholar 

  • Nakano H, Murabe N, Amemiya S, Nakajima Y (2006) Nervous system development of the sea cucumber Stichopus japonicus. Dev Biol 292(1):205–212. doi:10.1016/j.ydbio.2005.12.038

    Article  PubMed  CAS  Google Scholar 

  • Newman SJ, Thorndyke MC (1994) Localisation of gamma aminobutyric acid (GABA)-like immunoreactivity in the echinoderm Asterias rubens. Cell Tissue Res 278(1):177–185

    Article  PubMed  CAS  Google Scholar 

  • Newman SJ, Elphick MR, Thorndyke MC (1995) Tissue distribution of the SALMFamide neuropeptides S1 and S2 in the starfish Asterias rubens using novel monoclonal and polyclonal antibodies. I. Nervous and locomotory systems. Proc Biol Sci 261(1360):139–145. doi:10.1098/rspb.1995.0128

    Article  PubMed  CAS  Google Scholar 

  • Sun B, Salvaterra PM (1995) Characterization of nervana, a Drosophila melanogaster neuron-specific glycoprotein antigen recognized by anti-horseradish peroxidase antibodies. J Neurochem 65(1):434–443 (research support, U.S. Gov’t, P.H.S.)

    Article  PubMed  CAS  Google Scholar 

  • Ullrich-Luter EM, Dupont S, Arboleda E, Hausen H, Arnone MI (2011) Unique system of photoreceptors in sea urchin tube feet. Proc Natl Acad Sci U S A 108(20):8367–8372. doi:10.1073/pnas.1018495108 (research support, Non-U.S. Gov’t)

    Article  PubMed  PubMed Central  Google Scholar 

  • Yaguchi S, Yaguchi J, Burke RD (2006) Specification of ectoderm restricts the size of the animal plate and patterns neurogenesis in sea urchin embryos. Development 133(12):2337–2346. doi:10.1242/dev.02396

    Article  PubMed  CAS  Google Scholar 

  • Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T (1997) Dopamine neuron agenesis in Nurr1-deficient mice. Science 276(5310):248–250

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by NSF (IOS-0842870) and NIH (1SC1GM084770-01 and 1R03NS065275-01). CADB was funded by the UPR-RP MARC Program (5T34GM007821) and LDVF by the NIH ENDURE Program (R25 GM 097635-01). We also acknowledge partial support from NIH-RCMI (RRO-3641-01) and the University of Puerto Rico.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José E. García-Arrarás.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Díaz-Balzac, C.A., Vázquez-Figueroa, L.D. & García-Arrarás, J.E. Novel markers identify nervous system components of the holothurian nervous system. Invert Neurosci 14, 113–125 (2014). https://doi.org/10.1007/s10158-014-0169-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10158-014-0169-1

Keywords

Navigation