Lipidomics reveals mitochondrial membrane remodeling associated with acute thermoregulation in a rodent with a wide thermoneutral zone

Lipids

Volumn 49, Issue 7, 2014, Pages 715-730

  Pan, Qian ^a,b   Li, Min ^c   Shi, Yao Long ^a,b   Liu, Huwei ^c   Speakman, John R ^d,e   Wang, De Hua ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c PEKING UNIVERSITY   (China)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

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

Indexed keywords

FATTY ACID; LIPIDOME; MEMBRANE PHOSPHOLIPID;

ANIMAL CELL; ARTICLE; BODY TEMPERATURE; BROWN ADIPOSE TISSUE; ENVIRONMENTAL TEMPERATURE; LIPIDOMICS; MERIONES UNGUICULATUS; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUSCLE; NONHUMAN; THERMOREGULATION; ANIMAL; GERBIL; LIPID METABOLISM; METABOLISM; METABOLOMICS; TEMPERATURE;

ANIMALS; BODY TEMPERATURE REGULATION; GERBILLINAE; LIPID METABOLISM; METABOLOMICS; MITOCHONDRIAL MEMBRANES; TEMPERATURE;

EID: 84903784901     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-014-3900-0     Document Type: Article

References (50)

1. Schmidt-Nielsen K (1990) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge
2. Robinson PF (1959) Metabolism of the gerbil, Meriones unguiculatus. Science 130:502-503
3. Gordon CJ (2012) Thermal physiology of laboratory mice: defining thermoneutrality. J Therm Biol 37:654-685
4. Cannon B, Nedergaard J (2011) Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214:242-253
5. Faerevik H, Markussen D, Oglaend GE, Reinertsen RE (2001) The thermoneutral zone when wearing aircrew protective clothing. J Therm Biol 26:419-425 (Pubitemid 32804468)
6. Szekely M, Mercer JB (1999) Thermosensitivity changes in cold-adapted rats. J Therm Biol 24:369-371 (Pubitemid 30063054)
7. Schwimmer H, Haim A (2009) Physiological adaptations of small mammals to desert ecosystems. Integr Zool 4:357-366
8. Li YG, Yan ZC, Wang DH (2010) Physiological and biochemical basis of basal metabolic rates in Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus). Comp Biochem Physiol A Mol Integr Physiol 157:204-211
9. Wang DH, Wang YS, Wang ZW (2000) Metabolism and thermoregulation in the Mongolian gerbil Meriones unguiculatus. Acta Theriol 45:183-192
10. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731-758 (Pubitemid 27328739)
11. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy-metabolism. Proton permeability of the inner membrane of liver-mitochondria is greater in a mammal than in a reptile. Biochem J 275:81-86
12. Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19-42
13. Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593-1599 (Pubitemid 40697607)
14. Haggerty C, Hoggard N, Brown DS, Clapham JC, Speakman JR (2008) Intra-specific variation in resting metabolic rate in MF1 mice is not associated with membrane lipid desaturation in the liver. Mech Ageing Dev 129:129-137
15. Stuart JA, Gillis TE, Ballantyne JS (1998) Remodeling of phospholipid fatty acids in mitochondrial membranes of estivating snails. Lipids 33:787-793 (Pubitemid 28388059)
16. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Bio 9:112-124 (Pubitemid 351158912)
17. Valencak TG, Ruf T (2011) Feeding into old age: long-term effects of dietary fatty acid supplementation on tissue composition and life span in mice. J of Comp Physiol B Biochem Syst Environ Physiol 181:289-298
18. Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta Biomembranes 1666:62-87
19. Valencak TG, Arnold W, Tataruch F, Ruf T (2003) High content of polyunsaturated fatty acids in muscle phospholipids of a fast runner, the European brown hare (Lepus europaeus). J Comp Physiol B Biochem Syst Environ Physiol 173:695-702 (Pubitemid 37502458)
20. Kiebish MA, Han XL, Cheng H, Chuang JH, Seyfried TN (2008) Brain mitochondrial lipid abnormalities in mice susceptible to spontaneous gliomas. Lipids 43:951-959
21. Toyoda T, Hiramatsu Y, Sasaki T, Nakaoka Y (2009) Thermosensitive response based on the membrane fluidity adaptation in Paramecium multimicronucleatum. J Exp Biol 212:2767-2772
22. Williams E, Somero G (1996) Seasonal-, tidal-cycle- and microhabitat-related variation in membrane order of phospholipid vesicles from gills of the intertidal mussel Mytilus californianus. J Exp Biol 199:1587-1596 (Pubitemid 26272449)
23. Armstrong C, Thomas RH, Price ER, Guglielmo CG, Staples JF (2011) Remodeling mitochondrial membranes during arousal from hibernation. Physiol Biochem Zool 84:438-449
24. Nie H, Liu R, Yang Y, Bai Y, Guan Y, Qian D, Wang T, Liu H (2010) Lipid profiling of rat peritoneal surface layers by online normal- and reversed-phase 2D LC QToF-MS. J Lipid Res 51:2833-2844
25. Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Bba Mol Cell Biol L 1486:1-17 (Pubitemid 30336788)
26. Hishikawa D, Shindou H, Kobayashi S, Nakanishi H, Taguchi R, Shimizu T (2008) Discovery essential of a lysophospholipid acyltransferase family for membrane asymmetry and diversity. P Natl Acad Sci USA 105:2830-2835 (Pubitemid 351723629)
27. Hulbert AJ (2007) Membrane fatty acids as pacemakers of animal metabolism. Lipids 42:811-819
28. Selman C, Korhonen TK, Bunger L, Hill WG, Speakman JR (2001) Thermoregulatory responses of two mouse Mus musculus strains selectively bred for high and low food intake. J Comp Physiol B Biochem Syst Environ Physiol 171:661-668 (Pubitemid 33145840)
29. Raichlen DA, Gordon AD, Muchlinski MN, Snodgrass JJ (2010) Causes and significance of variation in mammalian basal metabolism. J Comp Physiol B 180:301-311
30. Chi QS, Wang DH (2011) Thermal physiology and energetics in male desert hamsters (Phodopus roborovskii) during cold acclimation. J Comp Physiol B Biochem Syst Environ Physiol 181:91-103
31. Arch J, Hislop D, Wang S, Speakman J (2006) Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J obes 30:1322-1331 (Pubitemid 44306513)
32. Zhao ZJ, Wang DH (2005) Short photoperiod enhances thermogenic capacity in Brandt's voles. Physiol Behav 85:143-149
33. Andrade FH, Garcia-Cazarin ML, Gamboa JL (2011) Rat diaphragm mitochondria have lower intrinsic respiratory rates than mitochondria in limb muscles. Am J Physiol Reg I 300:R1311-R1315
34. Scorrano L, Frezza C, Cipolat S (2007) Organelle isolation: functional mitochondria from mouse liver, muscle and cultured filroblasts. Nat Protoc 2:287-295 (Pubitemid 47040043)
35. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
36. Estabrook RW (1967) Mitochondrial respiratory control and the polarographic measurement of ADP: O ratios. Meths Enzymol 10:41-47
37. Li XS, Wang DH (2005) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt's voles (Microtus brandti). Horm Behav 48:321-328
38. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
39. Ocloo A, Shabalina IG, Nedergaard J, Brand MD (2007) Cold-induced alterations of phospholipid fatty acyl composition in brown adipose tissue mitochondria are independent of uncoupling protein-1. Am J Physiol Reg I 293:R1086-R1093 (Pubitemid 47358928)
40. Kang JX, Wang J (2005) A simplified method for analysis of polyunsaturated fatty acids. BMC Biochem 6:5
41. Weir JBD (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109:1-9
42. Ferrannini E (1988) The theoretical bases of indirect calorimetry: a review. Metab Clin Exp 37:287-301
43. Speakman JR (2000) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:177-297
44. Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199-232
45. Lands WE (1958) Metabolism of glycerolipids; a comparison of lecithin and triglyceride synthesis. J Biol Chem 231:883-888
46. Kang JX, Liu A (2013) The role of the tissue omega-6/omega-3 fatty acid ratio in regulating tumor angiogenesis. Cancer Metastasis Rev 32:201-210
47. Hulbert AJ (2003) Life, death and membrane bilayers. J Exp Biol 206:2303-2311
48. Valencak TG, Ruf T (2013) Phospholipid composition and longevity: lessons from Ames dwarf mice. Age 35:2303-2313
49. Paradies G, Paradies V, De Benedictis V, Ruggiero FM, Petrosillo G (2014) Functional role of cardiolipin in mitochondrial bioenergetics. Biochim Biophys Acta 1837:408-417
50. Litman BJ, Mitchell DC (1996) A role for phospholipid polyunsaturation in modulating membrane protein function. Lipids 31:S193-S197