Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?

Earthworms are affected by physical stress, like injury, and by exposure to xenobiotics, such as the toxic metal cadmium (Cd), which enters the environment mainly through industry and agriculture. The stress response to the single and the combination of both stressors was examined in regenerative an...

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Main Authors: Gerhard P. Aigner, Veronika Peer, Birgit Fiechtner, Cláudio Adriano Piechnik, Martina Höckner
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1272191/full
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author Gerhard P. Aigner
Veronika Peer
Birgit Fiechtner
Cláudio Adriano Piechnik
Martina Höckner
author_facet Gerhard P. Aigner
Veronika Peer
Birgit Fiechtner
Cláudio Adriano Piechnik
Martina Höckner
author_sort Gerhard P. Aigner
collection DOAJ
description Earthworms are affected by physical stress, like injury, and by exposure to xenobiotics, such as the toxic metal cadmium (Cd), which enters the environment mainly through industry and agriculture. The stress response to the single and the combination of both stressors was examined in regenerative and unharmed tissue of Lumbricus terrestris to reveal if the stress response to a natural insult like injury (amputation) interferes with Cd detoxification mechanisms. We characterized the roles of metallothionein 1 (MT1) and MT2 isoforms, heat shock protein 70 as well as immune biomarkers such as the toll-like receptors (TLR) single cysteine cluster TLR and multiple cysteine cluster TLR. The role of the activated transcription factors (ATFs) ATF2, ATF7, and the cAMP responsive element binding protein as putative regulatory intersection as well as a stress-dependent change of the essential trace elements zinc and calcium was analyzed. Phosphorylated AMP activated protein kinase, the cellular energy sensor, was measured to explore the energy demand, while the energy status was determined by detecting carbohydrate and protein levels. Taken together, we were able to show that injury rather than Cd is the driving force that separates the four treatment groups – Control, Cd exposure, Injury, Cd exposure and injury. Interestingly, we found that gene expression differed regarding the tissue section that was analyzed and we hypothesize that this is due to the migration of coelomocytes, earthworm immune cells, that take over a key role in protecting the organism from a variety of environmental challenges. Surprisingly, we discovered a role for MT1 in the response to multiple stressors and an isoform-specific function for the two newly characterized TLRs. In conclusion, we gathered novel information on the relation of innate immunity, wound healing, and Cd detoxification mechanisms in earthworms.
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spelling doaj.art-e025ddaa9e084152933b4e258c1ff4b02023-12-05T07:53:18ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-12-011410.3389/fimmu.2023.12721911272191Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?Gerhard P. AignerVeronika PeerBirgit FiechtnerCláudio Adriano PiechnikMartina HöcknerEarthworms are affected by physical stress, like injury, and by exposure to xenobiotics, such as the toxic metal cadmium (Cd), which enters the environment mainly through industry and agriculture. The stress response to the single and the combination of both stressors was examined in regenerative and unharmed tissue of Lumbricus terrestris to reveal if the stress response to a natural insult like injury (amputation) interferes with Cd detoxification mechanisms. We characterized the roles of metallothionein 1 (MT1) and MT2 isoforms, heat shock protein 70 as well as immune biomarkers such as the toll-like receptors (TLR) single cysteine cluster TLR and multiple cysteine cluster TLR. The role of the activated transcription factors (ATFs) ATF2, ATF7, and the cAMP responsive element binding protein as putative regulatory intersection as well as a stress-dependent change of the essential trace elements zinc and calcium was analyzed. Phosphorylated AMP activated protein kinase, the cellular energy sensor, was measured to explore the energy demand, while the energy status was determined by detecting carbohydrate and protein levels. Taken together, we were able to show that injury rather than Cd is the driving force that separates the four treatment groups – Control, Cd exposure, Injury, Cd exposure and injury. Interestingly, we found that gene expression differed regarding the tissue section that was analyzed and we hypothesize that this is due to the migration of coelomocytes, earthworm immune cells, that take over a key role in protecting the organism from a variety of environmental challenges. Surprisingly, we discovered a role for MT1 in the response to multiple stressors and an isoform-specific function for the two newly characterized TLRs. In conclusion, we gathered novel information on the relation of innate immunity, wound healing, and Cd detoxification mechanisms in earthworms.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1272191/fullAnnelidastressinjuryamputationinnate immunityimmune cells
spellingShingle Gerhard P. Aigner
Veronika Peer
Birgit Fiechtner
Cláudio Adriano Piechnik
Martina Höckner
Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
Frontiers in Immunology
Annelida
stress
injury
amputation
innate immunity
immune cells
title Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
title_full Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
title_fullStr Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
title_full_unstemmed Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
title_short Wound healing and Cadmium detoxification in the earthworm Lumbricus terrestris – a potential case for coelomocytes?
title_sort wound healing and cadmium detoxification in the earthworm lumbricus terrestris a potential case for coelomocytes
topic Annelida
stress
injury
amputation
innate immunity
immune cells
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1272191/full
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