Cell and Tissue Research

, Volume 377, Issue 3, pp 469–474 | Cite as

Immune activity at the gut epithelium in the larval sea urchin

  • Katherine M. BuckleyEmail author
  • Jonathan P. RastEmail author
Mini Review


The embryo of the purple sea urchin has been a fruitful model for the study of developmental gene regulatory networks. For similar reasons, the feeding sea urchin larva provides a gene regulatory model to investigate immune interactions at the gut epithelium. Here we describe what is known of the gut structure and immune cells of the sea urchin larva, and the cellular and gene expression response of the larva to gut-associated immune challenge. As a focused example of how the sea urchin larva can be compared with vertebrate systems, we discuss the expression and function of the IL-17 signalling system in the course of the larval immune response.


Mucosal immunity IL-17 Inflammation Vibrio Barrier immunity 


Funding information

JPR is supported by a grant from the Natural Sciences and Engineering Research Council (RGPIN-2017-06247).

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.


  1. Alcami A (2003) Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 3:36–50CrossRefGoogle Scholar
  2. Annunziata R, Perillo M, Andrikou C et al (2014) Pattern and process during sea urchin gut morphogenesis: the regulatory landscape. Genesis 52:251–268. CrossRefGoogle Scholar
  3. Buckley KM, Rast JP (2015) Diversity of animal immune receptors and the origins of recognition complexity in the deuterostomes. Dev Comp Immunol 49:179–189. CrossRefGoogle Scholar
  4. Buckley KM, Rast JP (2017) An organismal model for gene regulatory networks in the gut-associated immune response. Front Immunol 8:1297Google Scholar
  5. Buckley KM, Ho ECH, Hibino T et al (2017) IL17 factors are early regulators in the gut epithelium during inflammatory response to Vibrio in the sea urchin larva. Elife 6:e23481.
  6. Burke RD (1981) Structure of the digestive tract of the pluteus larva of Dendraster excentricus (Echinodermata: Echinoida). Zoomorphology 98:209–225CrossRefGoogle Scholar
  7. Carrier TJ, Reitzel AM (2018) Convergent shifts in host-associated microbial communities across environmentally elicited phenotypes. Nat Commun 9:952. CrossRefGoogle Scholar
  8. Chang SH, Reynolds JM, Pappu BP et al (2011) Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity 35:611–621. CrossRefGoogle Scholar
  9. Coates CJ, McCulloch C, Betts J, Whalley T (2018) Echinochrome a release by red spherule cells is an iron-withholding strategy of sea urchin innate immunity. J Innate Immunol 10:119–130. CrossRefGoogle Scholar
  10. Ernst SG (2011) Offerings from an urchin. Dev Biol 358:285–294. CrossRefGoogle Scholar
  11. Erwin DH, Laflamme M, Tweedt SM et al (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334(80):1091–1097. CrossRefGoogle Scholar
  12. Furukawa R, Takahashi Y, Nakajima Y et al (2009) Defense system by mesenchyme cells in bipinnaria larvae of the starfish, Asterina pectinifera. Dev Comp Immunol 33:205–215. CrossRefGoogle Scholar
  13. Furukawa R, Funabashi H, Matsumoto M, Kaneko H (2012) Starfish ApDOCK protein essentially functions in larval defense system operated by mesenchyme cells. Immunol Cell Biol 90:955–965. CrossRefGoogle Scholar
  14. Ghosh J, Buckley KM, Nair SV et al (2010) Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev Comp Immunol 34:235–245CrossRefGoogle Scholar
  15. Gibson AW, Burke RD (1985) The origin of pigment cells in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Biol 107:414–419CrossRefGoogle Scholar
  16. Hibino T, Loza-Coll M, Messier C et al (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365. CrossRefGoogle Scholar
  17. Ho ECH, Buckley KM, Schrankel CS et al (2016) Perturbation of gut bacteria induces a coordinated cellular immune response in the purple sea urchin larva. Immunol Cell Biol 94:861–874. CrossRefGoogle Scholar
  18. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 cells. Annu Rev Immunol 27(285):517. Google Scholar
  19. Lebedev AV, Ivanova MV, Levitsky DO (2008) Iron chelators and free radical scavengers in naturally occurring polyhydroxylated 1,4-naphthoquinones. Hemoglobin 32:165–179. CrossRefGoogle Scholar
  20. Liu L, Yang J, Qiu L et al (2011) A novel scavenger receptor-cysteine-rich (SRCR) domain containing scavenger receptor identified from mollusk mediated PAMP recognition and binding. Dev Comp Immunol 35:227–239. CrossRefGoogle Scholar
  21. McCormack R, De Armas L, Shiratsuchi M, Podack ER (2013) Killing machines: three pore-forming proteins of the immune system. Immunol Res 57:268–278. CrossRefGoogle Scholar
  22. McDermott AJ, Huffnagle GB (2014) The microbiome and regulation of mucosal immunity. Immunology 142:24–31. CrossRefGoogle Scholar
  23. McFall-Ngai MJ, Hadfield MG, Bosch TCG et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236. CrossRefGoogle Scholar
  24. McGeachy MJ, Cua DJ, Gaffen SL (2019) The IL-17 family of cytokines in health and disease. Immunity 50:892–906. CrossRefGoogle Scholar
  25. Metchnikoff I (1891) Lectures on the comparative pathology of inflammation delivered at the Pasteur Institute in 1891. Dover, New YorkGoogle Scholar
  26. Perillo M, Wang YJ, Leach SD, Arnone MI (2016) A pancreatic exocrine-like cell regulatory circuit operating in the upper stomach of the sea urchin Strongylocentrotus purpuratus larva. BMC Evol Biol 16:117. CrossRefGoogle Scholar
  27. Pfeifer P, Voss M, Wonnenberg B et al (2013) IL-17C is a mediator of respiratory epithelial innate immune response. Am J Respir Cell Mol Biol 48:415–421. CrossRefGoogle Scholar
  28. Ramirez-Carrozzi V, Sambandam A, Luis E et al (2011) IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. 12:1159–66.
  29. Schrankel CS, Solek CM, Buckley KM et al (2016) A conserved alternative form of the purple sea urchin HEB/E2-2/E2A transcription factor mediates a switch in E-protein regulatory state in differentiating immune cells. Dev Biol 416:149–161. CrossRefGoogle Scholar
  30. Secombes CJ, Cunningham C (2004) Cytokines: an evolutionary perspective. Dev Comp Immunol 28:373–374CrossRefGoogle Scholar
  31. Service M, Wardlaw AC (1984) Echinochrome-A as a bactericidal substance in the coelomic fluid of Echinus esculentus (L.). Comp Biochem Physiol Part B Comp Biochem 79:161–165. CrossRefGoogle Scholar
  32. Smith LC, Arizza V, Barela Hudgell MA et al (2018) Echinodermata: the complex immune system in echinoderms. In: Advances in comparative immunology. Springer International Publishing, Cham, pp 409–501CrossRefGoogle Scholar
  33. Solek CM, Oliveri P, Loza-Coll M et al (2013) An ancient role for Gata-1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol 382:280–292. CrossRefGoogle Scholar
  34. Song X, Zhu S, Shi P et al (2011) IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat Immunol 12.
  35. Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730CrossRefGoogle Scholar
  36. Stumpp M, Hu MY, Tseng Y-C et al (2015) Evolution of extreme stomach pH in bilateria inferred from gastric alkalization mechanisms in basal deuterostomes. Sci Rep 5:10421. CrossRefGoogle Scholar
  37. Tamboline CR, Burke RD (1992) Secondary mesenchyme of the sea urchin embryo: ontogeny of blastocoelar cells. J Exp Zool 262:51–60CrossRefGoogle Scholar
  38. Yaguchi J, Yaguchi S (2019) Evolution of nitric oxide regulation of gut function. Proc Natl Acad Sci U S A 116:5607–5612. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA
  2. 2.Emory University School of Medicine, Pathology & Laboratory MedicineAtlantaUSA

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