Lipidomics Reveals Mitochondrial Membrane Remodeling Associated with Acute Thermoregulation in a Rodent with a Wide Thermoneutral Zone

Qian Pan, Min Li, Yao-Long Shi, Huwei Liu, John R. Speakman, De-Hua Wang

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Mongolian gerbils (Meriones unguiculatus) have high physiological flexibility in response to acute temperature changes, and have the widest thermoneutral zone (TNZ, 26.5-38.9 A degrees C) reported among small mammals. At the upper critical temperature (T (uc), 38.9 A degrees C), body temperatures of gerbils were significantly increased (39-41 A degrees C) while metabolic rates were maintained at the basal level. In contrast, below the lower critical temperature (T (lc), 26.5 A degrees C), metabolism was elevated and body temperature stable. Rapid changes in mitochondrial membrane lipidome were hypothesized to play an important role during acute thermoregulation of gerbils. Taking advantage of a recent lipidomic technique, we examined changes in the membrane phospholipids environment and free fatty acids (FFA) production in mitochondria between 38 and 27 A degrees C (in the TNZ), and between 27 and 16 A degrees C (below the TNZ). At 38 A degrees C, acute heat stress elicited distinct remodeling in mitochondrial membrane lipidome which related to a potential decrease in mitochondrial respiration and membrane fluidity compared to 27 A degrees C. At 16 A degrees C, a sharply decreased unsaturation index and increased chain lengths were detected in mitochondrial FFA production both in muscle and brown adipose tissue. Our results suggest that mitochondrial membrane lipid remodeling may stabilize membrane function and activity of respiration related membrane protein to maintain a stable metabolic rate at T (uc), and improve heat production by decomposing less fluid fatty acid conjugates of membrane lipids under acute cold exposure. These data therefore imply an important role of membrane remodeling during acute thermoregulation in a non-hibernating endotherm.

Original languageEnglish
Pages (from-to)715-730
Number of pages16
JournalLipids
Volume49
Issue number7
Early online date7 May 2014
DOIs
Publication statusPublished - Jul 2014

Keywords

  • HPLC-ESI-MS
  • Lipidomics
  • Mongolian gerbils
  • Acute thermoregulation
  • Mitochondrial membrane lipid
  • Thermoneutral zone

Cite this

Lipidomics Reveals Mitochondrial Membrane Remodeling Associated with Acute Thermoregulation in a Rodent with a Wide Thermoneutral Zone. / Pan, Qian; Li, Min; Shi, Yao-Long; Liu, Huwei; Speakman, John R.; Wang, De-Hua.

In: Lipids, Vol. 49, No. 7, 07.2014, p. 715-730.

Research output: Contribution to journalArticle

Pan, Qian ; Li, Min ; Shi, Yao-Long ; Liu, Huwei ; Speakman, John R. ; Wang, De-Hua. / Lipidomics Reveals Mitochondrial Membrane Remodeling Associated with Acute Thermoregulation in a Rodent with a Wide Thermoneutral Zone. In: Lipids. 2014 ; Vol. 49, No. 7. pp. 715-730.
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abstract = "Mongolian gerbils (Meriones unguiculatus) have high physiological flexibility in response to acute temperature changes, and have the widest thermoneutral zone (TNZ, 26.5-38.9 A degrees C) reported among small mammals. At the upper critical temperature (T (uc), 38.9 A degrees C), body temperatures of gerbils were significantly increased (39-41 A degrees C) while metabolic rates were maintained at the basal level. In contrast, below the lower critical temperature (T (lc), 26.5 A degrees C), metabolism was elevated and body temperature stable. Rapid changes in mitochondrial membrane lipidome were hypothesized to play an important role during acute thermoregulation of gerbils. Taking advantage of a recent lipidomic technique, we examined changes in the membrane phospholipids environment and free fatty acids (FFA) production in mitochondria between 38 and 27 A degrees C (in the TNZ), and between 27 and 16 A degrees C (below the TNZ). At 38 A degrees C, acute heat stress elicited distinct remodeling in mitochondrial membrane lipidome which related to a potential decrease in mitochondrial respiration and membrane fluidity compared to 27 A degrees C. At 16 A degrees C, a sharply decreased unsaturation index and increased chain lengths were detected in mitochondrial FFA production both in muscle and brown adipose tissue. Our results suggest that mitochondrial membrane lipid remodeling may stabilize membrane function and activity of respiration related membrane protein to maintain a stable metabolic rate at T (uc), and improve heat production by decomposing less fluid fatty acid conjugates of membrane lipids under acute cold exposure. These data therefore imply an important role of membrane remodeling during acute thermoregulation in a non-hibernating endotherm.",
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note = "Acknowledgments Many thanks to the two anonymous reviewers for their comments and suggestions. We are grateful to all the members of Animal Physiological Ecology Group for their assistance and suggestions. Particularly we thank Dr. Qing-Sheng Chi for his help on metabolic rate determinations and Li Chen and Rui Wang for their valuable suggestions and help with chemical analysis of membrane lipids. This study was supported by the National Natural Scientific Foundation of China (No. 31272312, 31071930) to DHW.",
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AU - Speakman, John R.

AU - Wang, De-Hua

N1 - Acknowledgments Many thanks to the two anonymous reviewers for their comments and suggestions. We are grateful to all the members of Animal Physiological Ecology Group for their assistance and suggestions. Particularly we thank Dr. Qing-Sheng Chi for his help on metabolic rate determinations and Li Chen and Rui Wang for their valuable suggestions and help with chemical analysis of membrane lipids. This study was supported by the National Natural Scientific Foundation of China (No. 31272312, 31071930) to DHW.

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N2 - Mongolian gerbils (Meriones unguiculatus) have high physiological flexibility in response to acute temperature changes, and have the widest thermoneutral zone (TNZ, 26.5-38.9 A degrees C) reported among small mammals. At the upper critical temperature (T (uc), 38.9 A degrees C), body temperatures of gerbils were significantly increased (39-41 A degrees C) while metabolic rates were maintained at the basal level. In contrast, below the lower critical temperature (T (lc), 26.5 A degrees C), metabolism was elevated and body temperature stable. Rapid changes in mitochondrial membrane lipidome were hypothesized to play an important role during acute thermoregulation of gerbils. Taking advantage of a recent lipidomic technique, we examined changes in the membrane phospholipids environment and free fatty acids (FFA) production in mitochondria between 38 and 27 A degrees C (in the TNZ), and between 27 and 16 A degrees C (below the TNZ). At 38 A degrees C, acute heat stress elicited distinct remodeling in mitochondrial membrane lipidome which related to a potential decrease in mitochondrial respiration and membrane fluidity compared to 27 A degrees C. At 16 A degrees C, a sharply decreased unsaturation index and increased chain lengths were detected in mitochondrial FFA production both in muscle and brown adipose tissue. Our results suggest that mitochondrial membrane lipid remodeling may stabilize membrane function and activity of respiration related membrane protein to maintain a stable metabolic rate at T (uc), and improve heat production by decomposing less fluid fatty acid conjugates of membrane lipids under acute cold exposure. These data therefore imply an important role of membrane remodeling during acute thermoregulation in a non-hibernating endotherm.

AB - Mongolian gerbils (Meriones unguiculatus) have high physiological flexibility in response to acute temperature changes, and have the widest thermoneutral zone (TNZ, 26.5-38.9 A degrees C) reported among small mammals. At the upper critical temperature (T (uc), 38.9 A degrees C), body temperatures of gerbils were significantly increased (39-41 A degrees C) while metabolic rates were maintained at the basal level. In contrast, below the lower critical temperature (T (lc), 26.5 A degrees C), metabolism was elevated and body temperature stable. Rapid changes in mitochondrial membrane lipidome were hypothesized to play an important role during acute thermoregulation of gerbils. Taking advantage of a recent lipidomic technique, we examined changes in the membrane phospholipids environment and free fatty acids (FFA) production in mitochondria between 38 and 27 A degrees C (in the TNZ), and between 27 and 16 A degrees C (below the TNZ). At 38 A degrees C, acute heat stress elicited distinct remodeling in mitochondrial membrane lipidome which related to a potential decrease in mitochondrial respiration and membrane fluidity compared to 27 A degrees C. At 16 A degrees C, a sharply decreased unsaturation index and increased chain lengths were detected in mitochondrial FFA production both in muscle and brown adipose tissue. Our results suggest that mitochondrial membrane lipid remodeling may stabilize membrane function and activity of respiration related membrane protein to maintain a stable metabolic rate at T (uc), and improve heat production by decomposing less fluid fatty acid conjugates of membrane lipids under acute cold exposure. These data therefore imply an important role of membrane remodeling during acute thermoregulation in a non-hibernating endotherm.

KW - HPLC-ESI-MS

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KW - Mongolian gerbils

KW - Acute thermoregulation

KW - Mitochondrial membrane lipid

KW - Thermoneutral zone

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DO - 10.1007/s11745-014-3900-0

M3 - Article

VL - 49

SP - 715

EP - 730

JO - Lipids

JF - Lipids

SN - 0024-4201

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