Advertisement

Individual and combined effects of salinity and lipopolysaccharides on the immune response of juvenile Takifugu fasciatus

  • Dan Wang
  • Quanquan Cao
  • Wenxu Zhu
  • Yadong Hu
  • Xinyu Zhang
  • Shaowu YinEmail author
  • Tao WangEmail author
Article

Abstract

Lipopolysaccharides (LPS) and salinity are important variables in aquatic environments. High concentration of LPS and large changes in salinity seriously threat the survival of a variety of organisms, including fish. To reveal the effects of salinity and LPS on a fish immune response, we measured the immune-related parameters (total leukocyte count, total serum protein, albumin and globulin concentrations, complement C3 concentration, and lysozyme activity) and genes (the expressions of TNF-α, IL-1β, and SOCS1–3 at the mRNA and protein levels) of juvenile Takifugu fasciatus exposed to phosphate buffered saline (PBS) or LPS (25 μg mL−1) under different salinities (0, 15, and 30 ppt) for 24 h. Changes in key immunological indicators suggested that the LPS challenge induced considerable damage to T. fasciatus, whereas an increase in salinity mitigated the harmful effects. Moreover, although the immune responses in blood and other selected tissues (gill and kidney) were suppressed with an increase in salinity, the increased response in liver in saltwater enabled T. fasciatus to conquer large salinity variation during migration. The appropriate addition of salts appeared to be a sensible strategy to mitigate LPS-induced toxicity in the aquaculture of T. fasciatus.

Keywords

Salinity Lipopolysaccharides Immune response Takifugu fasciatus 

Abbreviations

LPS

Lipopolysaccharides

T. fasciatus

Takifugu fasciatus

IL-1β

Interleukin-1β

TNF-α

Tumor necrosis factor-α

SOCS

Suppressors of cytokine signaling

ROS

Reactive oxygen species

GCs

Glucocorticoids

qRT-PCR

Quantitative real-time PCR

AKI

Acute kidney injury

Notes

Funding

The authors received financial support from the National Natural Science Foundation of China (31800436), The National Spark Program of China (2015GA690040), The National Finance Projects of Agro-technical popularization (TG15-003), Project Foundation of the Academic Program Development of Jiangsu Higher Education Institution (PAPD), National Key R & D Program of China (2018YFD0900301), and Natural Science Foundation(NSF) of Jiangsu Province of China (BK20180728).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Supplementary material

10695_2018_607_MOESM1_ESM.docx (30 kb)
ESM 1 (DOCX 29 kb)

References

  1. Abdollahi R, Heidari B, Aghamaali M (2016) Evaluation of lysozyme, complement C3, and total protein in different developmental stages of Caspian kutum (Rutilus frisii kutum K.). Arch Pol Fish 24:15–22CrossRefGoogle Scholar
  2. Afaq S, Rana KS (2009) Toxicological effects of leather dyes on total leukocyte count of fresh water teleost, Cirrhinus mrigala (Ham). Biol Med 1:134–138Google Scholar
  3. Bayne CJ, Gerwick L (2001) The acute phase response and innate immunity of fish. Dev Comp Immunol 25:725–743CrossRefGoogle Scholar
  4. Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immunol 20:239–262CrossRefGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  6. Calcagni E, Elenkov I (2010) Stress system activity, innate and T helper cytokines, and susceptibility to immune-related diseases. Ann N Y Acad Sci 1069:62–76CrossRefGoogle Scholar
  7. Chen Y, Huang X, Wang J, Li C (2017) Effect of pure microcystin-LR on activity and transcript level of immune-related enzymes in the white shrimp (Litopenaeus vannamei ). Ecotoxicology 26:1–9CrossRefGoogle Scholar
  8. De SAR, Penalva LO, Marcotte EM, Vogel C (2009) Global signatures of protein and mRNA expression levels. Mol BioSyst 5:1512–1526Google Scholar
  9. Dowd WW, Harris BN, Cech JJ, Kültz D (2010) Proteomic and physiological responses of leopard sharks (Triakis semifasciata) to salinity change. J Exp Biol 213:210–224CrossRefGoogle Scholar
  10. Elasely AM, Abbass AA, Austin B (2014) Honey bee pollen improves growth, immunity and protection of Nile tilapia (Oreochromis niloticus) against infection with Aeromonas hydrophila. Fish Shellfish Immunol 40:500–506CrossRefGoogle Scholar
  11. Harikrishnan R, Balasundaram C, Heo MS (2010) Effect of probiotics enriched diet on Paralichthys olivaceus infected with lymphocystis disease virus (LCDV). Fish Shellfish Immunol 29:868–874CrossRefGoogle Scholar
  12. Huising MO, Stet RJ, Savelkoul HF, Verburg-van Kemenade BM (2004) The molecular evolution of the interleukin-1 family of cytokines; IL-18 in teleost fish. Dev Comp Immunol 28:395–413CrossRefGoogle Scholar
  13. Ichiki S, Kato-Unoki Y, Somamoto T, Nakao M (2012) The binding spectra of carp C3 isotypes against natural targets independent of the binding specificity of their thioester. Dev Comp Immunol 38:10–16CrossRefGoogle Scholar
  14. Jin HJ, Shao JZ, Xiang LX, Wang H, Sun LL (2008) Global identification and comparative analysis of SOCS genes in fish: insights into the molecular evolution of SOCS family. Mol Immunol 45:1258–1268CrossRefGoogle Scholar
  15. Kalbus E, Zekri S, Karimi A (2016) Intervention scenarios to manage seawater intrusion in a coastal agricultural area in Oman. Arab J Geosci 9:1–12CrossRefGoogle Scholar
  16. Kato A, Doi H, Nakada T, Sakai H, Hirose S (2005) Takifugu obscurus is a euryhaline fugu species very close to Takifugu rubripes and suitable for studying osmoregulation. BMC Physiol 5:18CrossRefGoogle Scholar
  17. Kile BT, Alexander WS (2001) The suppressors of cytokine signalling (SOCS). Cell Mol Life Sci 58:1627–1635CrossRefGoogle Scholar
  18. Kültz D (2012) The combinatorial nature of osmosensing in fishes. Physiology 27:259–275CrossRefGoogle Scholar
  19. Loro VL, Jorge MB, Silva KR, Wood CM (2012) Oxidative stress parameters and antioxidant response to sublethal waterborne zinc in a euryhaline teleost Fundulus heteroclitus: protective effects of salinity. Aquat Toxicol 110-111:187–193CrossRefGoogle Scholar
  20. Maeda M, Lee WJ, Taga N (1983) Distribution of lipopolysaccharide, an indicator of bacterial biomass, in subtropical areas of the sea. Mar Biol 76:257–262CrossRefGoogle Scholar
  21. Magnadóttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151CrossRefGoogle Scholar
  22. Magnadottir B, Lange S, Gudmundsdottir S, Bøgwald J, Dalmo RA (2005) Ontogeny of humoral immune parameters in fish. Fish Shellfish Immunol 19:429–439CrossRefGoogle Scholar
  23. Marc AM, Quentel CA, Lebail PY, Boeuf G (2010) Changes in some endocrinological and non-specific immunological parameters during seawater exposure in the brown trout. J Fish Biol 46:1065–1081CrossRefGoogle Scholar
  24. Novoa B, Bowman TL, Figueras A (2009) LPS response and tolerance in the zebrafish (Danio rerio). Fish Shellfish Immunol 26:326–331CrossRefGoogle Scholar
  25. Paulsen SM, Lunde H, Engstad RE, Robertsen B (2003) In vivo effects of beta-glucan and LPS on regulation of lysozyme activity and mRNA expression in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 14:39–54CrossRefGoogle Scholar
  26. Philip AM, Daniel KS, Vijayan MM (2012) Cortisol modulates the expression of cytokines and suppressors of cytokine signaling (SOCS) in rainbow trout hepatocytes. Dev Comp Immunol 38:360–367CrossRefGoogle Scholar
  27. Philip AM, Jøgensen EH, Maule AG, Vijayan MM (2014) Tissue-specific molecular immune response to lipopolysaccharide challenge in emaciated anadromous Arctic charr. Dev Comp Immunol 45:133–140CrossRefGoogle Scholar
  28. Savan R, Sakai M (2004) Presence of multiple isoforms of TNF alpha in carp (Cyprinus carpio L.): genomic and expression analysis. Fish Shellfish Immunol 17:87–94CrossRefGoogle Scholar
  29. Selvaraj V, Sampath K, Sekar V (2009) Administration of lipopolysaccharide increases specific and non-specific immune parameters and survival in carp ( Cyprinus carpio ) infected with Aeromonas hydrophila. Aquaculture 286:176–183CrossRefGoogle Scholar
  30. Shepherd BS, Rees CB, Binkowski FP, Goetz FW (2012) Characterization and evaluation of sex-specific expression of suppressors of cytokine signaling (SOCS)-1 and −3 in juvenile yellow perch ( Perca flavescens ) treated with lipopolysaccharide. Fish Shellfish Immunol 33:468–481CrossRefGoogle Scholar
  31. Sieroslawska A, Rymuszka A, Velisek J, Pawlik-Skowrońska B, Svobodova Z, Skowroński T (2012) Effects of microcystin-containing cyanobacterial extract on hematological and biochemical parameters of common carp ( Cyprinus carpio L.). Fish Physiol Biochem 38:1159–1167CrossRefGoogle Scholar
  32. Skjesol A, Liebe T, Iliev DB, Thomassen EI, Tollersrud LG, Sobhkhez M, Lindenskov JL, Secombes CJ, Jørgensen JB (2014) Functional conservation of suppressors of cytokine signaling proteins between teleosts and mammals: Atlantic salmon SOCS1 binds to JAK/STAT family members and suppresses type I and II IFN signaling. Dev Comp Immunol 45:177–189CrossRefGoogle Scholar
  33. Taylor JF, Needham MP, North BP, Morgan A, Thompson K, Migaud H (2007) The influence of ploidy on saltwater adaptation, acute stress response and immune function following seawater transfer in non-smolting rainbow trout. Gen Comp Endocrinol 152:314–325CrossRefGoogle Scholar
  34. Wang J, Zhu X, Huang X, Lei G, Chen Y, Yang Z (2016a) Combined effects of cadmium and salinity on juvenile Takifugu obscurus: cadmium moderates salinity tolerance; salinity decreases the toxicity of cadmium. Sci Rep 6:30968CrossRefGoogle Scholar
  35. Wang L, Wu ZQ, Wang XL, Ren Q, Zhang GS, Liang FF, Yin SW (2016b) Immune responses of two superoxide dismutases ( SODs ) after lipopolysaccharide or Aeromonas hydrophila challenge in pufferfish, Takifugu obscurus. Aquaculture 459:1–7CrossRefGoogle Scholar
  36. Wang J, Tang H, Zhang X, Xue X, Zhu X, Chen Y, Yang Z (2017) Mitigation of nitrite toxicity by increased salinity is associated with multiple physiological responses: a case study using an economically important model species, the juvenile obscure puffer (Takifugu obscurus). Environ Pollut 232:137–145CrossRefGoogle Scholar
  37. Wiegertjes GF, Stet RJ, Parmentier HK, van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20:365–381CrossRefGoogle Scholar
  38. Xu D, Chen M, Ren X, Ren X, Wu Y (2014) Leonurine ameliorates LPS-induced acute kidney injury via suppressing ROS-mediated NF-κB signaling pathway. Fitoterapia 97:148–155CrossRefGoogle Scholar
  39. Yang Z, Chen YF (2008) Differences in reproductive strategies between obscure puffer Takifugu obscurus and ocellated puffer Takifugu ocellatus during their spawning migration. J Appl Ichthyol 24:569–573CrossRefGoogle Scholar
  40. Yang Z, Li JJ, Gu W, Liu Y, Wang W, Guo RX, Qin GX, Chen YF (2010) Effects of salinity on survival and Na+/K+ ATPase activity of obscure puffer Takifugu obscurus embryos. J Appl Ichthyol 26:449–452CrossRefGoogle Scholar
  41. Yang X, Guo JL, Ye JY, Zhang YX, Wang W (2015) The effects of Ficus carica polysaccharide on immune response and expression of some immune-related genes in grass carp, Ctenopharyngodon idella. Fish Shellfish Immunol 42:132–137CrossRefGoogle Scholar
  42. Ye HY, Jin J, Jin LW, Chen Y, Zhou ZH, Li ZY (2017) Chlorogenic acid attenuates lipopolysaccharide-induced acute kidney injury by inhibiting TLR4/NF-κB signal pathway. Inflammation 40:523–529CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of Life Sciences, College of Marine Sciences and EngineeringNanjing Normal UniversityNanjingChina
  2. 2.Co-Innovation Center for Marine Bio-Industry Technology of Jiangsu ProvinceLianyungangChina

Personalised recommendations