Insights into the fish thioredoxin system: Expression profile of thioredoxin and thioredoxin reductase in rainbow trout (Oncorhynchus mykiss) during infection and in vitro stimulation

D Pacitti, T Wang, S A M Martin, J Sweetman, C J Secombes

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Production of reactive oxygen species (ROS) is the first biological response during a disease outbreak and after injury. ROS are highly reactive molecules that can either endanger cell homeostasis or mediate cell signaling in several physiological pathways, including the immune response. Thioredoxin (Trx) and thioredoxin reductase (TrxR) are the essential components of the thioredoxin system, one of the main intracellular redox systems and are therefore important regulators of ROS accumulation. Through the regulation of the intracellular redox milieu, the thioredoxin system plays a key role within the immune system, linking immunology and free radical science. In this study we have firstly identified TrxRs in fish and used this new sequence information to reevaluate the evolution of the thioredoxin system within the vertebrate lineage. We next measured the expression of rainbow trout (Oncorhynchus mykiss) Trx and TrxR transcripts during infection in vivo and in vitro after stimulation of a macrophage cell line and primary macrophage cultures with pathogen associated molecular patterns (PAMPs). Our results showed that both Trx and TrxR were induced during infection at the transcriptional level, confirming their likely involvement in the innate immune response of fish. Since TrxRs are selenium-containing proteins (selenoproteins), we also measured the modulation of their expression upon organic and inorganic selenium exposure in vitro. TrxR was found to be responsive to selenium exposure in vitro, suggesting that it may represent a key mediator in the selenium modulation of innate immunity. In conclusion, our study highlights the need to investigate the involvement of the cell antioxidant pathways, especially the thioredoxin system, within the immune system of vertebrate species.
Original languageEnglish
Pages (from-to)261-277
Number of pages17
JournalDevelopmental and Comparative Immunology
Volume42
Issue number2
Early online date1 Oct 2013
DOIs
Publication statusPublished - Feb 2014

Fingerprint

Thioredoxin-Disulfide Reductase
Thioredoxins
Oncorhynchus mykiss
Fishes
Selenium
Infection
Reactive Oxygen Species
Innate Immunity
Oxidation-Reduction
Vertebrates
Immune System
Macrophages
In Vitro Techniques
Allergy and Immunology
Free Radicals
Disease Outbreaks
Homeostasis
Antioxidants
Cell Line
Wounds and Injuries

Keywords

  • fish
  • thioredoxin system
  • ROS
  • innate immunity
  • inflammation
  • selenium

Cite this

@article{e99437d2878f4f72ae96d09c4fc37570,
title = "Insights into the fish thioredoxin system: Expression profile of thioredoxin and thioredoxin reductase in rainbow trout (Oncorhynchus mykiss) during infection and in vitro stimulation",
abstract = "Production of reactive oxygen species (ROS) is the first biological response during a disease outbreak and after injury. ROS are highly reactive molecules that can either endanger cell homeostasis or mediate cell signaling in several physiological pathways, including the immune response. Thioredoxin (Trx) and thioredoxin reductase (TrxR) are the essential components of the thioredoxin system, one of the main intracellular redox systems and are therefore important regulators of ROS accumulation. Through the regulation of the intracellular redox milieu, the thioredoxin system plays a key role within the immune system, linking immunology and free radical science. In this study we have firstly identified TrxRs in fish and used this new sequence information to reevaluate the evolution of the thioredoxin system within the vertebrate lineage. We next measured the expression of rainbow trout (Oncorhynchus mykiss) Trx and TrxR transcripts during infection in vivo and in vitro after stimulation of a macrophage cell line and primary macrophage cultures with pathogen associated molecular patterns (PAMPs). Our results showed that both Trx and TrxR were induced during infection at the transcriptional level, confirming their likely involvement in the innate immune response of fish. Since TrxRs are selenium-containing proteins (selenoproteins), we also measured the modulation of their expression upon organic and inorganic selenium exposure in vitro. TrxR was found to be responsive to selenium exposure in vitro, suggesting that it may represent a key mediator in the selenium modulation of innate immunity. In conclusion, our study highlights the need to investigate the involvement of the cell antioxidant pathways, especially the thioredoxin system, within the immune system of vertebrate species.",
keywords = "fish, thioredoxin system, ROS, innate immunity, inflammation, selenium",
author = "D Pacitti and T Wang and Martin, {S A M} and J Sweetman and Secombes, {C J}",
note = "Copyright {\circledC} 2013 Elsevier Ltd. All rights reserved. Acknowledgements This work was supported by Alltech and the Marine Alliance for Science and Technology Scotland (MASTS).",
year = "2014",
month = "2",
doi = "10.1016/j.dci.2013.09.013",
language = "English",
volume = "42",
pages = "261--277",
journal = "Developmental and Comparative Immunology",
issn = "0145-305X",
publisher = "Elsevier Limited",
number = "2",

}

TY - JOUR

T1 - Insights into the fish thioredoxin system

T2 - Expression profile of thioredoxin and thioredoxin reductase in rainbow trout (Oncorhynchus mykiss) during infection and in vitro stimulation

AU - Pacitti, D

AU - Wang, T

AU - Martin, S A M

AU - Sweetman, J

AU - Secombes, C J

N1 - Copyright © 2013 Elsevier Ltd. All rights reserved. Acknowledgements This work was supported by Alltech and the Marine Alliance for Science and Technology Scotland (MASTS).

PY - 2014/2

Y1 - 2014/2

N2 - Production of reactive oxygen species (ROS) is the first biological response during a disease outbreak and after injury. ROS are highly reactive molecules that can either endanger cell homeostasis or mediate cell signaling in several physiological pathways, including the immune response. Thioredoxin (Trx) and thioredoxin reductase (TrxR) are the essential components of the thioredoxin system, one of the main intracellular redox systems and are therefore important regulators of ROS accumulation. Through the regulation of the intracellular redox milieu, the thioredoxin system plays a key role within the immune system, linking immunology and free radical science. In this study we have firstly identified TrxRs in fish and used this new sequence information to reevaluate the evolution of the thioredoxin system within the vertebrate lineage. We next measured the expression of rainbow trout (Oncorhynchus mykiss) Trx and TrxR transcripts during infection in vivo and in vitro after stimulation of a macrophage cell line and primary macrophage cultures with pathogen associated molecular patterns (PAMPs). Our results showed that both Trx and TrxR were induced during infection at the transcriptional level, confirming their likely involvement in the innate immune response of fish. Since TrxRs are selenium-containing proteins (selenoproteins), we also measured the modulation of their expression upon organic and inorganic selenium exposure in vitro. TrxR was found to be responsive to selenium exposure in vitro, suggesting that it may represent a key mediator in the selenium modulation of innate immunity. In conclusion, our study highlights the need to investigate the involvement of the cell antioxidant pathways, especially the thioredoxin system, within the immune system of vertebrate species.

AB - Production of reactive oxygen species (ROS) is the first biological response during a disease outbreak and after injury. ROS are highly reactive molecules that can either endanger cell homeostasis or mediate cell signaling in several physiological pathways, including the immune response. Thioredoxin (Trx) and thioredoxin reductase (TrxR) are the essential components of the thioredoxin system, one of the main intracellular redox systems and are therefore important regulators of ROS accumulation. Through the regulation of the intracellular redox milieu, the thioredoxin system plays a key role within the immune system, linking immunology and free radical science. In this study we have firstly identified TrxRs in fish and used this new sequence information to reevaluate the evolution of the thioredoxin system within the vertebrate lineage. We next measured the expression of rainbow trout (Oncorhynchus mykiss) Trx and TrxR transcripts during infection in vivo and in vitro after stimulation of a macrophage cell line and primary macrophage cultures with pathogen associated molecular patterns (PAMPs). Our results showed that both Trx and TrxR were induced during infection at the transcriptional level, confirming their likely involvement in the innate immune response of fish. Since TrxRs are selenium-containing proteins (selenoproteins), we also measured the modulation of their expression upon organic and inorganic selenium exposure in vitro. TrxR was found to be responsive to selenium exposure in vitro, suggesting that it may represent a key mediator in the selenium modulation of innate immunity. In conclusion, our study highlights the need to investigate the involvement of the cell antioxidant pathways, especially the thioredoxin system, within the immune system of vertebrate species.

KW - fish

KW - thioredoxin system

KW - ROS

KW - innate immunity

KW - inflammation

KW - selenium

U2 - 10.1016/j.dci.2013.09.013

DO - 10.1016/j.dci.2013.09.013

M3 - Article

C2 - 24095766

VL - 42

SP - 261

EP - 277

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

SN - 0145-305X

IS - 2

ER -