Regulated hypothermia in response to endotoxin in birds
Autor(a) principal: | |
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Data de Publicação: | 2021 |
Outros Autores: | , , , |
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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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 |
|
_version_ |
1799965760348487680 |