Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila

Anders Malmendal, Johannes Overgaard, Jacob G Bundy, Jesper G Sørensen, Niels Chr Nielsen, Volker Loeschcke, Martin Holmstrup

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

Frequent exposure of terrestrial insects to temperature variation has led to the evolution of protective biochemical and physiological mechanisms, such as the heat shock response, which markedly increases the tolerance to heat stress. Insight into such mechanisms has, so far, mainly relied on selective studies of specific compounds or characteristics or studies at the genomic or proteomic levels. In the present study, we have used untargeted NMR metabolomic profiling to examine the biological response to heat stress in Drosophila melanogaster. The metabolite profile was analyzed during recovery after exposure to different thermal stress treatments and compared with untreated controls. Both moderate and severe heat stress gave clear effects on the metabolite profiles. The profiles clearly demonstrated that hardening by moderate heat stress led to a faster reestablishment of metabolite homeostasis after subsequent heat stress. Several metabolites were identified as responsive to heat stress and could be related to known physiological and biochemical responses. The time course of the recovery of metabolite homeostasis mirrored general changes in gene expression, showing that recovery follows the same temporal pattern at these two biological levels. Finally, our data show that heat hardening permits a quicker return to homeostasis, rather than a reduction of the acute metabolic perturbation and that the reestablishment of homeostasis is important for obtaining maximal heat-hardening effect. The results display the power of NMR metabolomic profiling for characterization of the instantaneous physiological condition, enabling direct visualization of the perturbation of and return to homeostasis.
OriginalsprogEngelsk
TidsskriftAmerican Journal of Physiology: Regulatory, Integrative and Comparative Physiology
Vol/bind291
Udgave nummer1
Sider (fra-til)R205-12
ISSN0363-6119
DOI
StatusUdgivet - 1 jul. 2006
Udgivet eksterntJa

Citer dette

Malmendal, Anders ; Overgaard, Johannes ; Bundy, Jacob G ; Sørensen, Jesper G ; Nielsen, Niels Chr ; Loeschcke, Volker ; Holmstrup, Martin. / Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. I: American Journal of Physiology: Regulatory, Integrative and Comparative Physiology. 2006 ; Bind 291, Nr. 1. s. R205-12.
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title = "Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila",
abstract = "Frequent exposure of terrestrial insects to temperature variation has led to the evolution of protective biochemical and physiological mechanisms, such as the heat shock response, which markedly increases the tolerance to heat stress. Insight into such mechanisms has, so far, mainly relied on selective studies of specific compounds or characteristics or studies at the genomic or proteomic levels. In the present study, we have used untargeted NMR metabolomic profiling to examine the biological response to heat stress in Drosophila melanogaster. The metabolite profile was analyzed during recovery after exposure to different thermal stress treatments and compared with untreated controls. Both moderate and severe heat stress gave clear effects on the metabolite profiles. The profiles clearly demonstrated that hardening by moderate heat stress led to a faster reestablishment of metabolite homeostasis after subsequent heat stress. Several metabolites were identified as responsive to heat stress and could be related to known physiological and biochemical responses. The time course of the recovery of metabolite homeostasis mirrored general changes in gene expression, showing that recovery follows the same temporal pattern at these two biological levels. Finally, our data show that heat hardening permits a quicker return to homeostasis, rather than a reduction of the acute metabolic perturbation and that the reestablishment of homeostasis is important for obtaining maximal heat-hardening effect. The results display the power of NMR metabolomic profiling for characterization of the instantaneous physiological condition, enabling direct visualization of the perturbation of and return to homeostasis.",
author = "Anders Malmendal and Johannes Overgaard and Bundy, {Jacob G} and S{\o}rensen, {Jesper G} and Nielsen, {Niels Chr} and Volker Loeschcke and Martin Holmstrup",
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Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. / Malmendal, Anders; Overgaard, Johannes; Bundy, Jacob G; Sørensen, Jesper G; Nielsen, Niels Chr; Loeschcke, Volker; Holmstrup, Martin.

I: American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, Bind 291, Nr. 1, 01.07.2006, s. R205-12.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila

AU - Malmendal, Anders

AU - Overgaard, Johannes

AU - Bundy, Jacob G

AU - Sørensen, Jesper G

AU - Nielsen, Niels Chr

AU - Loeschcke, Volker

AU - Holmstrup, Martin

PY - 2006/7/1

Y1 - 2006/7/1

N2 - Frequent exposure of terrestrial insects to temperature variation has led to the evolution of protective biochemical and physiological mechanisms, such as the heat shock response, which markedly increases the tolerance to heat stress. Insight into such mechanisms has, so far, mainly relied on selective studies of specific compounds or characteristics or studies at the genomic or proteomic levels. In the present study, we have used untargeted NMR metabolomic profiling to examine the biological response to heat stress in Drosophila melanogaster. The metabolite profile was analyzed during recovery after exposure to different thermal stress treatments and compared with untreated controls. Both moderate and severe heat stress gave clear effects on the metabolite profiles. The profiles clearly demonstrated that hardening by moderate heat stress led to a faster reestablishment of metabolite homeostasis after subsequent heat stress. Several metabolites were identified as responsive to heat stress and could be related to known physiological and biochemical responses. The time course of the recovery of metabolite homeostasis mirrored general changes in gene expression, showing that recovery follows the same temporal pattern at these two biological levels. Finally, our data show that heat hardening permits a quicker return to homeostasis, rather than a reduction of the acute metabolic perturbation and that the reestablishment of homeostasis is important for obtaining maximal heat-hardening effect. The results display the power of NMR metabolomic profiling for characterization of the instantaneous physiological condition, enabling direct visualization of the perturbation of and return to homeostasis.

AB - Frequent exposure of terrestrial insects to temperature variation has led to the evolution of protective biochemical and physiological mechanisms, such as the heat shock response, which markedly increases the tolerance to heat stress. Insight into such mechanisms has, so far, mainly relied on selective studies of specific compounds or characteristics or studies at the genomic or proteomic levels. In the present study, we have used untargeted NMR metabolomic profiling to examine the biological response to heat stress in Drosophila melanogaster. The metabolite profile was analyzed during recovery after exposure to different thermal stress treatments and compared with untreated controls. Both moderate and severe heat stress gave clear effects on the metabolite profiles. The profiles clearly demonstrated that hardening by moderate heat stress led to a faster reestablishment of metabolite homeostasis after subsequent heat stress. Several metabolites were identified as responsive to heat stress and could be related to known physiological and biochemical responses. The time course of the recovery of metabolite homeostasis mirrored general changes in gene expression, showing that recovery follows the same temporal pattern at these two biological levels. Finally, our data show that heat hardening permits a quicker return to homeostasis, rather than a reduction of the acute metabolic perturbation and that the reestablishment of homeostasis is important for obtaining maximal heat-hardening effect. The results display the power of NMR metabolomic profiling for characterization of the instantaneous physiological condition, enabling direct visualization of the perturbation of and return to homeostasis.

U2 - 10.1152/ajpregu.00867.2005

DO - 10.1152/ajpregu.00867.2005

M3 - Journal article

VL - 291

SP - R205-12

JO - American Journal of Physiology: Regulatory, Integrative and Comparative Physiology

JF - American Journal of Physiology: Regulatory, Integrative and Comparative Physiology

SN - 0363-6119

IS - 1

ER -