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Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off

Although skeletal muscle is a specialized tissue that provides the motor for movement, it also participates in other functions, including the immune response. However, little is known about the effects of this multitasking on muscle. We show that muscle loses some of its capacity while it is partici...

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Autores principales: Adamo, Shelley A., Corkum, Emily, Kim, Jongseok, Lee, Tingyat M., Miller, Dylan W., Song, Sungwoo, Wright, Christopher, Zacher, Isaac D., Zbarsky, Jeffrey S., McMillan, Laura E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399994/
https://www.ncbi.nlm.nih.gov/pubmed/37334669
http://dx.doi.org/10.1242/jeb.245861
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author Adamo, Shelley A.
Corkum, Emily
Kim, Jongseok
Lee, Tingyat M.
Miller, Dylan W.
Song, Sungwoo
Wright, Christopher
Zacher, Isaac D.
Zbarsky, Jeffrey S.
McMillan, Laura E.
author_facet Adamo, Shelley A.
Corkum, Emily
Kim, Jongseok
Lee, Tingyat M.
Miller, Dylan W.
Song, Sungwoo
Wright, Christopher
Zacher, Isaac D.
Zbarsky, Jeffrey S.
McMillan, Laura E.
author_sort Adamo, Shelley A.
collection PubMed
description Although skeletal muscle is a specialized tissue that provides the motor for movement, it also participates in other functions, including the immune response. However, little is known about the effects of this multitasking on muscle. We show that muscle loses some of its capacity while it is participating in the immune response. Caterpillars (Manduca sexta) were exposed to an immune challenge, predator stress or a combination of immune challenge and predator stress. The expression of immune genes (toll-1, domeless, cactus, tube and attacin) increased in body wall muscle after exposure to an immune challenge. Muscle also showed a reduction in the amount of the energy storage molecule glycogen. During an immune challenge, the force of the defensive strike, an important anti-predator behaviour in M. sexta, was reduced. Caterpillars were also less able to defend themselves against a common enemy, the wasp Cotesia congregata, suggesting that the effect on muscle is biologically significant. Our results support the concept of an integrated defence system in which life-threatening events activate organism-wide responses. We suggest that increased mortality from predation is a non-immunological cost of infection in M. sexta. Our study also suggests that one reason non-immunological costs of infection exist is because of the participation of diverse organs, such as muscle, in immunity.
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spelling pubmed-103999942023-08-04 Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off Adamo, Shelley A. Corkum, Emily Kim, Jongseok Lee, Tingyat M. Miller, Dylan W. Song, Sungwoo Wright, Christopher Zacher, Isaac D. Zbarsky, Jeffrey S. McMillan, Laura E. J Exp Biol Research Article Although skeletal muscle is a specialized tissue that provides the motor for movement, it also participates in other functions, including the immune response. However, little is known about the effects of this multitasking on muscle. We show that muscle loses some of its capacity while it is participating in the immune response. Caterpillars (Manduca sexta) were exposed to an immune challenge, predator stress or a combination of immune challenge and predator stress. The expression of immune genes (toll-1, domeless, cactus, tube and attacin) increased in body wall muscle after exposure to an immune challenge. Muscle also showed a reduction in the amount of the energy storage molecule glycogen. During an immune challenge, the force of the defensive strike, an important anti-predator behaviour in M. sexta, was reduced. Caterpillars were also less able to defend themselves against a common enemy, the wasp Cotesia congregata, suggesting that the effect on muscle is biologically significant. Our results support the concept of an integrated defence system in which life-threatening events activate organism-wide responses. We suggest that increased mortality from predation is a non-immunological cost of infection in M. sexta. Our study also suggests that one reason non-immunological costs of infection exist is because of the participation of diverse organs, such as muscle, in immunity. The Company of Biologists Ltd 2023-07-25 /pmc/articles/PMC10399994/ /pubmed/37334669 http://dx.doi.org/10.1242/jeb.245861 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Adamo, Shelley A.
Corkum, Emily
Kim, Jongseok
Lee, Tingyat M.
Miller, Dylan W.
Song, Sungwoo
Wright, Christopher
Zacher, Isaac D.
Zbarsky, Jeffrey S.
McMillan, Laura E.
Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title_full Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title_fullStr Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title_full_unstemmed Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title_short Muscle in the caterpillar Manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
title_sort muscle in the caterpillar manduca sexta responds to an immune challenge, but at a cost, suggesting a physiological trade-off
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399994/
https://www.ncbi.nlm.nih.gov/pubmed/37334669
http://dx.doi.org/10.1242/jeb.245861
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