Regulated hypothermia in response to endotoxin in birds

Detalhes bibliográficos
Autor(a) principal: Amaral-Silva, Lara do [UNESP]
Data de Publicação: 2021
Outros Autores: Gargaglioni, Luciane H. [UNESP], Steiner, Alexandre A., Oliveira, Marcos T. [UNESP], Bicego, Kenia Cardoso [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1113/JP281385
http://hdl.handle.net/11449/210292
Resumo: Key points The costs associated with immune and thermal responses may exceed the benefits to the host during severe inflammation. In this case, regulated hypothermia instead of fever can occur in rodents as a beneficial strategy to conserve energy for vital functions with consequent tissue protection and hypoxia prevention. We tested the hypothesis that this phenomenon is not exclusive to mammals, but extends to the other endothermic group, birds. A decrease in metabolic rate without any failure in mitochondrial respiration, nor oxygen delivery, is the main evidence supporting the regulated nature of endotoxin-induced hypothermia in chicks. Thermolytic mechanisms such as tachypnea and cutaneous vasodilatation can also be recruited to facilitate body temperature decrease under lipopolysaccharide treatment, especially in the cold. Our findings bring a new perspective for evolutionary medicine studies on energy trade-off in host defence because regulated hypothermia may be a phenomenon spread among vertebrates facing a severe immune challenge. A switch from fever to regulated hypothermia can occur in mammals under circumstances of reduced physiological fitness (e.g. sepsis) to direct energy to defend vital systems. Birds in which the cost to resist a pathogen is additive to the highest metabolic rate and body temperature (T-b) among vertebrates may also benefit from regulated hypothermia during systemic inflammation. Here, we show that the decrease in T-b observed during an immune challenge in birds is a regulated hypothermia, and not a result of metabolic failure. We investigated O-2 consumption (thermogenesis index), ventilation (respiratory heat loss), skin temperature (sensible heat loss) and muscle mitochondrial respiration (thermogenic tissue) during T-b fall in chicken chicks challenged with endotoxin [lipopolysaccharide (LPS)]. Chicks injected with LPS were also tested regarding the capacity to raise O-2 consumption to meet an increased demand driven by 2,4-dinitrophenol. LPS decreased T-b and the metabolic rate of chicks without affecting muscle uncoupled, coupled and non-coupled mitochondrial respiration. LPS-challenged chicks were indeed capable of increasing metabolic rate in response to 2,4-dinitrophenol, indicating no O-2 delivery limitation. Additionally, chicks did not attempt to prevent T-b from falling during hypothermia but, instead, activated cutaneous and respiratory thermolytic mechanisms, providing an additional cooling force. These data provide the first evidence of the regulated nature of the hypothermic response to endotoxin in birds. Therefore, it changes the current understanding of bird's thermoregulation during severe inflammation, indicating that regulated hypothermia is either a convergent trait for endotherms or a conserved response among vertebrates, which adds a new perspective for evolutionary medicine research.
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spelling Regulated hypothermia in response to endotoxin in birdsanapyrexiabirdshypothermiainflammationmetabolic rateperipheral vasodilatationtachypneaKey points The costs associated with immune and thermal responses may exceed the benefits to the host during severe inflammation. In this case, regulated hypothermia instead of fever can occur in rodents as a beneficial strategy to conserve energy for vital functions with consequent tissue protection and hypoxia prevention. We tested the hypothesis that this phenomenon is not exclusive to mammals, but extends to the other endothermic group, birds. A decrease in metabolic rate without any failure in mitochondrial respiration, nor oxygen delivery, is the main evidence supporting the regulated nature of endotoxin-induced hypothermia in chicks. Thermolytic mechanisms such as tachypnea and cutaneous vasodilatation can also be recruited to facilitate body temperature decrease under lipopolysaccharide treatment, especially in the cold. Our findings bring a new perspective for evolutionary medicine studies on energy trade-off in host defence because regulated hypothermia may be a phenomenon spread among vertebrates facing a severe immune challenge. A switch from fever to regulated hypothermia can occur in mammals under circumstances of reduced physiological fitness (e.g. sepsis) to direct energy to defend vital systems. Birds in which the cost to resist a pathogen is additive to the highest metabolic rate and body temperature (T-b) among vertebrates may also benefit from regulated hypothermia during systemic inflammation. Here, we show that the decrease in T-b observed during an immune challenge in birds is a regulated hypothermia, and not a result of metabolic failure. We investigated O-2 consumption (thermogenesis index), ventilation (respiratory heat loss), skin temperature (sensible heat loss) and muscle mitochondrial respiration (thermogenic tissue) during T-b fall in chicken chicks challenged with endotoxin [lipopolysaccharide (LPS)]. Chicks injected with LPS were also tested regarding the capacity to raise O-2 consumption to meet an increased demand driven by 2,4-dinitrophenol. LPS decreased T-b and the metabolic rate of chicks without affecting muscle uncoupled, coupled and non-coupled mitochondrial respiration. LPS-challenged chicks were indeed capable of increasing metabolic rate in response to 2,4-dinitrophenol, indicating no O-2 delivery limitation. Additionally, chicks did not attempt to prevent T-b from falling during hypothermia but, instead, activated cutaneous and respiratory thermolytic mechanisms, providing an additional cooling force. These data provide the first evidence of the regulated nature of the hypothermic response to endotoxin in birds. Therefore, it changes the current understanding of bird's thermoregulation during severe inflammation, indicating that regulated hypothermia is either a convergent trait for endotherms or a conserved response among vertebrates, which adds a new perspective for evolutionary medicine research.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Sao Paulo State Univ, Dept Anim Morphol & Physiol, 321 McIver St,312 Eberhart Bldg,Greensboro 27412, Jaboticabal, SP, BrazilSao Paulo State Univ, Dept Technol, Jaboticabal, SP, BrazilUniv Sao Paulo, Inst Biomed Sci, Dept Immunol, Sao Paulo, SP, BrazilSao Paulo State Univ, Dept Anim Morphol & Physiol, 321 McIver St,312 Eberhart Bldg,Greensboro 27412, Jaboticabal, SP, BrazilSao Paulo State Univ, Dept Technol, Jaboticabal, SP, BrazilFAPESP: 2017/12 627-9FAPESP: 2014/0 2253-6FAPESP: 2018/0 3418-0FAPESP: 2017/00864-6Wiley-BlackwellUniversidade Estadual Paulista (Unesp)Universidade de São Paulo (USP)Amaral-Silva, Lara do [UNESP]Gargaglioni, Luciane H. [UNESP]Steiner, Alexandre A.Oliveira, Marcos T. [UNESP]Bicego, Kenia Cardoso [UNESP]2021-06-25T15:03:57Z2021-06-25T15:03:57Z2021-05-03info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article2969-2986http://dx.doi.org/10.1113/JP281385Journal Of Physiology-london. Hoboken: Wiley, v. 599, n. 11, p. 2969-2986, 2021.0022-3751http://hdl.handle.net/11449/21029210.1113/JP281385WOS:000646294700001Web of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengJournal Of Physiology-londoninfo:eu-repo/semantics/openAccess2021-10-23T20:17:26Zoai:repositorio.unesp.br:11449/210292Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462021-10-23T20:17:26Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Regulated hypothermia in response to endotoxin in birds
title Regulated hypothermia in response to endotoxin in birds
spellingShingle Regulated hypothermia in response to endotoxin in birds
Amaral-Silva, Lara do [UNESP]
anapyrexia
birds
hypothermia
inflammation
metabolic rate
peripheral vasodilatation
tachypnea
title_short Regulated hypothermia in response to endotoxin in birds
title_full Regulated hypothermia in response to endotoxin in birds
title_fullStr Regulated hypothermia in response to endotoxin in birds
title_full_unstemmed Regulated hypothermia in response to endotoxin in birds
title_sort Regulated hypothermia in response to endotoxin in birds
author Amaral-Silva, Lara do [UNESP]
author_facet Amaral-Silva, Lara do [UNESP]
Gargaglioni, Luciane H. [UNESP]
Steiner, Alexandre A.
Oliveira, Marcos T. [UNESP]
Bicego, Kenia Cardoso [UNESP]
author_role author
author2 Gargaglioni, Luciane H. [UNESP]
Steiner, Alexandre A.
Oliveira, Marcos T. [UNESP]
Bicego, Kenia Cardoso [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (Unesp)
Universidade de São Paulo (USP)
dc.contributor.author.fl_str_mv Amaral-Silva, Lara do [UNESP]
Gargaglioni, Luciane H. [UNESP]
Steiner, Alexandre A.
Oliveira, Marcos T. [UNESP]
Bicego, Kenia Cardoso [UNESP]
dc.subject.por.fl_str_mv anapyrexia
birds
hypothermia
inflammation
metabolic rate
peripheral vasodilatation
tachypnea
topic anapyrexia
birds
hypothermia
inflammation
metabolic rate
peripheral vasodilatation
tachypnea
description Key points The costs associated with immune and thermal responses may exceed the benefits to the host during severe inflammation. In this case, regulated hypothermia instead of fever can occur in rodents as a beneficial strategy to conserve energy for vital functions with consequent tissue protection and hypoxia prevention. We tested the hypothesis that this phenomenon is not exclusive to mammals, but extends to the other endothermic group, birds. A decrease in metabolic rate without any failure in mitochondrial respiration, nor oxygen delivery, is the main evidence supporting the regulated nature of endotoxin-induced hypothermia in chicks. Thermolytic mechanisms such as tachypnea and cutaneous vasodilatation can also be recruited to facilitate body temperature decrease under lipopolysaccharide treatment, especially in the cold. Our findings bring a new perspective for evolutionary medicine studies on energy trade-off in host defence because regulated hypothermia may be a phenomenon spread among vertebrates facing a severe immune challenge. A switch from fever to regulated hypothermia can occur in mammals under circumstances of reduced physiological fitness (e.g. sepsis) to direct energy to defend vital systems. Birds in which the cost to resist a pathogen is additive to the highest metabolic rate and body temperature (T-b) among vertebrates may also benefit from regulated hypothermia during systemic inflammation. Here, we show that the decrease in T-b observed during an immune challenge in birds is a regulated hypothermia, and not a result of metabolic failure. We investigated O-2 consumption (thermogenesis index), ventilation (respiratory heat loss), skin temperature (sensible heat loss) and muscle mitochondrial respiration (thermogenic tissue) during T-b fall in chicken chicks challenged with endotoxin [lipopolysaccharide (LPS)]. Chicks injected with LPS were also tested regarding the capacity to raise O-2 consumption to meet an increased demand driven by 2,4-dinitrophenol. LPS decreased T-b and the metabolic rate of chicks without affecting muscle uncoupled, coupled and non-coupled mitochondrial respiration. LPS-challenged chicks were indeed capable of increasing metabolic rate in response to 2,4-dinitrophenol, indicating no O-2 delivery limitation. Additionally, chicks did not attempt to prevent T-b from falling during hypothermia but, instead, activated cutaneous and respiratory thermolytic mechanisms, providing an additional cooling force. These data provide the first evidence of the regulated nature of the hypothermic response to endotoxin in birds. Therefore, it changes the current understanding of bird's thermoregulation during severe inflammation, indicating that regulated hypothermia is either a convergent trait for endotherms or a conserved response among vertebrates, which adds a new perspective for evolutionary medicine research.
publishDate 2021
dc.date.none.fl_str_mv 2021-06-25T15:03:57Z
2021-06-25T15:03:57Z
2021-05-03
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1113/JP281385
Journal Of Physiology-london. Hoboken: Wiley, v. 599, n. 11, p. 2969-2986, 2021.
0022-3751
http://hdl.handle.net/11449/210292
10.1113/JP281385
WOS:000646294700001
url http://dx.doi.org/10.1113/JP281385
http://hdl.handle.net/11449/210292
identifier_str_mv Journal Of Physiology-london. Hoboken: Wiley, v. 599, n. 11, p. 2969-2986, 2021.
0022-3751
10.1113/JP281385
WOS:000646294700001
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Journal Of Physiology-london
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 2969-2986
dc.publisher.none.fl_str_mv Wiley-Blackwell
publisher.none.fl_str_mv Wiley-Blackwell
dc.source.none.fl_str_mv Web of Science
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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