Polar Biology

, Volume 41, Issue 10, pp 2065–2073 | Cite as

Detection of peroxiredoxin-like protein in Antarctic sea urchin (Sterechinus neumayeri) under heat stress and induced with pathogen-associated molecular pattern from Vibrio anguillarum

  • Byron Morales-Lange
  • Marcelo González-Aravena
  • Alejandro Font
  • Fanny Guzmán
  • Luis Mercado
Original Paper


Antarctic marine organisms have developed in an environment of low temperatures and high levels of stability. Consequently, these species have lost the ability to adapt to sudden changes in temperature. Rising ocean temperatures could make the Antarctic sea urchin Sterechinus neumayeri vulnerable to pathogens, triggering responses that increase oxidative stress. In order to understand how the immune system reacts, we can analyze the expression of anti-oxidant molecules such as the peroxiredoxins (Prxs). Prxs are an anti-oxidant protein family with conserved catalytic redox-active cysteine residues. In S. neumayeri, one full-length cDNA of the gene that encodes Prx (Sn-Prx) was characterized. The Sn-Prx cDNA contains a 786-bp open reading frame, which encodes 262 amino acids, including two conserved cysteine residues that are characteristic of the typical 2-Cys subgroup of the Prx family. An in silico analysis was performed to establish epitope molecules, which were then chemically synthesized and used to obtain antibodies. The antibodies were validated by indirect ELISA against a synthetic peptide and western blot against S. neumayeri proteins. In different tissues, the expression of Sn-Prx protein was increased after Vibrio anguillarum challenge. Heat stress also increased expression of Sn-Prx in coelomocytes after 7 days, but the availability of the protein decreased in digestive gland tissues after 2 and 3 weeks of heat stress. This may indicate the involvement of Prx in antioxidant response in S. neumayeri. The evidence presented in this study proposes anti-Prx antibody as an experimental evaluation tool that can be used to establish a baseline of the ability of S. neumayeri antioxidant response.


Heat stress Sterechinus neumayeri Prx Anti-oxidant Antarctica 



This study was supported by Fondo Nacional de Desarrollo Científico y Tecnológico 1131001 (2013–2015). BM is a fellow of Advanced Human Capital Formation of CONICYT, Chile (21151176).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.


  1. Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defense systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A 138:405–415CrossRefGoogle Scholar
  2. Abele D, Tesch C, Wencke P, Pfrtner HO (2001) How oxidative stress parameters relate to thermal tolerance in the Antarctic bivalve Yoldia eightsi? Antarct Sci 13:111–118CrossRefGoogle Scholar
  3. Bacano-Maningas MB, Koyama T, Kondo H, Hirono I, Aoki T (2008) A peroxiredoxin from kuruma shrimp, Marsupenaeus japonicus, inhibited by peptidoglycan. Dev Comp Immunol 32:198–203CrossRefGoogle Scholar
  4. Bethke J, Rojas V, Berendsen J, Cárdenas C, Guzmán F, Gallardo JA, Mercado L (2012) Development of a new antibody for detecting natural killer enhancing factor (NKEF)-like protein in infected salmonids. J Fish Dis 35:379–388CrossRefGoogle Scholar
  5. Borges JC, Porto-Nieto LR, Mangiaterra M, Jensch-Junior BE, da Silva J (2002) Phagocytosis in vitro and in vivo in the Antarctic sea urchin Sterechinus neumayeri at 0 °C. Polar Biol 25:891–897Google Scholar
  6. Branco PC, Pressinotti LN, Borges JCS, Iunes RS, Kfoury JR, da Silva MO et al (2012) Cellular biomarkers to elucidate global warming effects on Antarctic sea urchin Sterechinus neumayeri. Polar Biol 35:221–229CrossRefGoogle Scholar
  7. Brey T, Pearse J, Basch L, McClintock J, Slattery M (1995) Growth and production of Sterechinus neumayeri (Echinodea: Echinodermata) in McMurdo Sound, Antarctica. Mar Biol 124:279–292CrossRefGoogle Scholar
  8. Dang VT, Speck P, Benkendorff K (2012) Influence of elevated temperatures on the immune response of abalone, Haliotis rubra. Fish Shellfish Immunol 32:732–740CrossRefGoogle Scholar
  9. Du C, Anderson A, Lortie M, Parsons R, Bodnar A (2013) Oxidative damage and cellular defense mechanisms in sea urchin models of aging. Free Radic Biol Med 63:254–263CrossRefGoogle Scholar
  10. Esteban MA, Chaves-Pozo E, Arizcun M, Meseguer J, Cuesta A (2013) Regulation of natural killer enhancing factor (NKEF) genes in teleost fish, gilthead seabream and European sea bass. Mol Immunol 55:275–282CrossRefGoogle Scholar
  11. Ghosh J, Lun CM, Majeske AJ, Sacchi S, Schrankel CS, Smith LC (2011) Invertebrate immune diversity. Dev Comp Immunol 35:959–974CrossRefGoogle Scholar
  12. Gross PS, Al-Sharif WZ, Clow LA, Smith LC (1999) Echinoderm immunity and the evolution of the complement system. Dev Comp Immunol 23:429–442CrossRefGoogle Scholar
  13. Heck DE, Louis L, Gallo MA, Laskin JD (2000) Modulation of the development of plutei by nitric oxide in the sea urchin Arbacia punctulata. Biol Bull 199:195–197CrossRefGoogle Scholar
  14. Heise K, Puntarulo S, Pörtner HO, Abele D (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp Biochem Physiol C 134:79–90CrossRefGoogle Scholar
  15. Kang SW, Rhee SG, Chang TS, Jeong W, Choi MH (2005) 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med 11:571–578CrossRefGoogle Scholar
  16. Kelley LA, Mezulis S, Yates CM, Was MN, Sterberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858CrossRefGoogle Scholar
  17. Knoops B, Argyropoulou V, Becker S, Ferté L, Kuznetsova O (2016) Multiple roles of peroxiredoxins in inflammation. Mol Cells 39:60–64CrossRefGoogle Scholar
  18. Majeske AJ, Bayne CJ, Smith LC (2013) Aggregation of sea urchin phagocytes is augmented in vitro by lipopolysaccharide. PLoS ONE 8:e61419CrossRefGoogle Scholar
  19. Morales-Lange B, Bethke J, Schmitt P, Mercado L (2015) Phenotypical parameters as a tool to evaluate the immunostimulatory effects of laminarin in Oncorhynchus mykiss. Aquacult Res 46:2707–2715CrossRefGoogle Scholar
  20. Oláhová M, Taylor SR, Khazaipoul S, Wang J, Morgan BA, Matsumoto K, Blackwell TK, Veal EA (2008) A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc Natl Acad Sci USA 105:19839–19844CrossRefGoogle Scholar
  21. Park H, Ahn IY, Kim H, Cheon J, Kim M (2008) Analysis of ESTs and expression of two peroxiredoxins in the thermally stressed Antarctic bivalve Laternula elliptica. Fish Shellfish Immunol 25:550–559CrossRefGoogle Scholar
  22. Peck LS (2005) Prospect of survival in the Southern Ocean: vulnerability of benthic species to temperature change. Antarct Sci 17:497–507CrossRefGoogle Scholar
  23. Peck LS, Webb KE, Bailey DM (2004) Extreme sensibility if biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630CrossRefGoogle Scholar
  24. Rhee SG, Woo HA (2011) Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H2O2, and protein chaperones. Antioxid Redox Signal 15:781–794CrossRefGoogle Scholar
  25. Rojas V, Morales-Lange B, Guzmán F, Gallardo JA, Mercado L (2012) Immunological strategy for detecting the pro-inflammatory cytokine TNF-alpha in salmonids. Electron J Biotechnol 15:21CrossRefGoogle Scholar
  26. Schmitt P, Wacyk J, Morales-Lange B, Rojas V, Guzmán F, Dixon B, Mercado L (2015) Immunomodulatory effect of cathelicidins in response to a β-glucan in intestinal epithelial cells from rainbow trout. Dev Comp Immunol 51:160–169CrossRefGoogle Scholar
  27. Silva J (2013) Immunology in sea urchins. In: Lawrence JM (ed) Sea urchins: biology and ecology, 3rd edn. Elsevier, New York, pp 177–194Google Scholar
  28. Smith LC (2012) Innate immune complexity in the purple sea urchin: diversity of the sp185/333 system. Front Immunol 3:70PubMedPubMedCentralGoogle Scholar
  29. Smith LC, Ghosh J, Buckley KM, Clow LA, Dheilly NM, Haug T, Henson JH, Li C, Lun CM, Majeske AJ, Matranga V, Nair SV, Rast JP, Raftos DA, Roth M, Sacchi S, Schrankel CS, Stensvåg K (2010) Echinoderm immunity. In: Söderhäll K (ed) Invertebrate immunity. Springer, New York, pp 260–301CrossRefGoogle Scholar
  30. Tafalla C, Bøgwald J, Dalmo RA (2013) Adjuvants and immunostimulants in fish vaccines: current knowledge and future perspectives. Fish Shellfish Immunol 35:1740–1750CrossRefGoogle Scholar
  31. Tolomeo AM, Carraro A, Bakiu R, Toppo S, Place SP, Ferro D, Santovito G (2016) Peroxiredoxin 6 from the Antarctic emerald rockcod: molecular characterization of its response to warming. J Comp Physiol B 186:59–71CrossRefGoogle Scholar
  32. Trujillo M, Ferrer-Sueta G, Thomson L, Flohé L, Radi R (2007) Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite. In: Flohé L, Harris JR (eds) Peroxiredoxin systems. Springer, Dordrecht, pp 83–113CrossRefGoogle Scholar
  33. Wood ZA, Poole LB, Hantgan RR, Karplus PA (2002) Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41:5493–5504CrossRefGoogle Scholar
  34. Wood ZA, Schröder E, Robin Harris J, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:3–8CrossRefGoogle Scholar
  35. Zhang Q, Li F, Zhang J, Wang B, Gao H, Huang B, Jiang H, Xiang J (2007) Molecular cloning, expression of a peroxiredoxin gene in Chinese shrimp Fenneropenaeus chinensis and the antioxidant activity of its recombinant protein. Mol Immunol 44:3501–3509CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Grupo de Marcadores Inmunológicos en Organismos Acuáticos, Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Facultad de CienciasPontificia Universidad Católica de ValparaísoValparaísoChile
  2. 2.Laboratorio de Biorrecursos Antárticos, Departamento CientíficoInstituto Antártico ChilenoPunta ArenasChile
  3. 3.Nucleo Biotecnológico de CuraumaValparaísoChile

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