Seasonal acclimatization of brain lipidome in a eurythermal fish (Carassius carassius) is mainly determined by temperature

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 294, Issue 5, 2008, Pages

  Käkelä, Reijo ^a   Mattila, Minja ^b   Hermansson, Martin ^a   Haimi, Perttu ^a   Uphoff, Andreas ^a   Paajanen, Vesa ^b   Somerharju, Pentti ^a   Vornanen, Matti ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Docosahexaenoic acid; Mass spectrometry; Phosphatidylethanolamine; Phosphatidylserine; Polyunsaturated fatty acid

Indexed keywords

GLYCEROPHOSPHOLIPID; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; SPHINGOLIPID; FATTY ACID; PHOSPHATIDYLCHOLINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARASSIUS CARASSIUS; CONTROLLED STUDY; CYPRINIFORMES; LIPID BRAIN LEVEL; LIPID COMPOSITION; MASS SPECTROMETRY; NERVE CELL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; SEASONAL VARIATION; TEMPERATURE ACCLIMATIZATION; TEMPERATURE DEPENDENCE; ACCLIMATIZATION; ANIMAL; BRAIN LEVEL; CARP; EXPERIMENTAL ANIMAL; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MEMBRANE FUSION; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SEASON; TEMPERATURE; THERMOREGULATION; WILD ANIMAL;

ACCLIMATIZATION; ANIMALS; ANIMALS, LABORATORY; ANIMALS, WILD; BODY TEMPERATURE REGULATION; BRAIN CHEMISTRY; CARPS; CHROMATOGRAPHY, LIQUID; FATTY ACIDS; LIPID METABOLISM; MASS SPECTROMETRY; MEMBRANE FUSION; OXIDATION-REDUCTION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLSERINES; SEASONS; TEMPERATURE;

EID: 45549084330     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00883.2007     Document Type: Article

References (97)

1. Allen JA, Halverson-Tamboli RA, Rasenik MM. Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8: 128-140, 2007.
2. Anderson RGW, Jacobsen K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296: 1821-1825, 2002.
3. Armstrong VT, Brzustowicz MR, Wassall SR, Jenski LJ, Stillwell W. Rapid flip-flop in polyunsaturated (docosahexaenoate) phospholipid membranes. Arch Biochem Biophys 414: 74-82, 2003.
4. Bartlett EM, Lewis DH. Spectrophotometric determination of phosphate esters in the presence and absence of orthophosphate. Anal Biochem 36: 159-167, 1970.
5. Bell MV, Tocher DR. Molecular species composition of the major phospholipids in brain and retina from rainbow trout (Salmo gairdneri). Biochem J 264: 909-915, 1989.
6. Bell MV, Dick JR, Buda C. Molecular speciation of fish sperm phospholipids: large amounts of dipolyunsaturated phosphatidylserine. Lipids 32: 1085-1091, 1997.
7. Blank ML, Smith ZL, Lee YJ, Snyder F. Effects of eicosapentaenoic and docosahexaenoic acid supplements on phospholipid composition and plasmalogen biosynthesis in P388D1 cells. Arch Biochem Biophys 269: 603-611, 1989.
8. Brooks S, Clark GT, Wright SM, Trueman RJ, Postle AD, Cossins AR, Maclean NM. Electrospray ionization mass spectrometric analysis of lipid restructuring in the carp (Cyprinus carpio L.) during cold acclimation. J Exp Biol 205: 3989-3997, 2002.
9. Brosche T, Platt D. The biological significance of plasmalogens in defense against oxidative damage. Exp Gerontol 33: 363-369, 1998.
10. Brügger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD. Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionisation tandem mass spectrometry. Proc Natl Acad Sci USA 94: 2339-2344, 1997.
11. Brzustowicz MR, Cherezov V, Zerouga M, Caffrey M, Stillwell W, Wassall SR. Controlling membrane cholesterol content. A role for polyunsaturated (docosahexaenoate) phospholipids. Biochemistry 41: 12509-12519, 2002.
12. Buda C, Dey I, Balogh N, Horvath LI, Maderspach K, Juhasz M, Yeo YK, Farkas T. Structural order of membranes and composition of phospholipids in fish brain cells during thermal acclimatization. Proc Natl Acad Sci USA 91: 8234-8238, 1994.
13. Chang MC, Roots BI. The effects of temperature- and oxygen-acclimation on phospholipids of goldfish (Carassius auratus L.) brain microsomes. Neurochem Res 10: 355-375, 1985.
14. Ekroos K, Chernushevich IV, Simons K, Shevchenko A. Quantitative profiling of phospholipids by multiple precursor ion scanning on a hybrid quadrupole time-of-flight mass spectrometer. Anal Chem 74: 941-949, 2002.
15. Emoto K, Kobayashi T, Yamaji A, Aizawa H, Yahara I, Inoue K, Umeda M. Redistribution of phosphatidylethanolamine at the cleavage furrow of dividing cells during cytokinesis. Proc Natl Acad Sci USA 93: 12867-12872, 1996.
16. Farkas T, Kitajka K, Fodor E, Csengeri I, Lahdes E, Yeo YK, Krasznai Z, Halver JE. Docosahexaenoic acid-containing phospholipid molecular species in brains of vertebrates. Proc Natl Acad Sci USA 97: 6362-6366, 2000.
17. Folch JM, Lees M, Sloane-Stanley GH. A simple method for the isolation and purification of total lipides from animal tissue. J Biol Chem 226: 497-509, 1957.
18. Gamble W, Vaughan M, Kruth HS, Avigan J. Procedure for the determination of free and total cholesterol in micro- and nanogram amounts for studies with cultured cells. J Lipid Res 19: 1068-1070, 1978.
19. Gaposchkin DP, Zoeller RA. Plasmalogen status influences docosahexaenoic acid levels in a macrophage cell line: insight using ether lipid-deficient variants. J Lipid Res 40: 495-503, 1999.
20. Garner AE, Smith DA, Hooper NM. Sphingomyelin chain length influences the distribution of GPI-anchored proteins in rafts in supported lipid bilayers. Mol Membr Biol 24: 233-242, 2007.
21. Gerbi A, Maixent JM, Barbey O, Jamme I, Pierlovisi M, Coste T, Pieroni G, Nouvelot A, Vague P, Raccah D. Alterations of Na,K-ATPase isoenzymes in the rat diabetic neuropathy: protective effect of dietary supplementation with n-3 fatty acids. J Neurochem 71: 732-740, 1998.
22. Giorgione J, Epand RM, Buda C, Farkas T. Role of phospholipids containing docosahexaenoyl chains in modulating the activity of protein kinase C. Proc Natl Acad Sci USA 92: 9767-9770, 1995.
23. Glomset JA. Role of docosahexaenoic acid in neuronal plasma membranes. Sci STKE 321: pe6, 2006.
24. Goldfine H. Bacterial membranes and lipid packing theory. J Lipid Res 25: 1501-1507, 1984.
25. Grossfield A, Feller SE, Pitman MC. A role for direct interactions in the modulation of rhodopsin by ω-3 polyunsaturated lipids. Proc Natl Acad Sci USA 103: 4888-4893, 2006.
26. Guschina IA, Harwood JL. Mechanisms of temperature adaptation in poikilotherms. FEBS Lett 580: 5477-5483, 2006.
27. Haimi P, Uphoff A, Hermansson M, Somerharju P. Software tools for analysis of mass spectrometric lipidome data. Anal Chem 78: 8324-8331, 2006.
28. Hamano H, Nabekura J, Nishikawa M, Ogawa T. Docosahexaenoic acid reduces GABA response in substantia nigra neuron of rat. J Neurophysiol 75: 1264-1270, 1996.
29. Han X, Gross RW. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom Rev 24: 367-412, 2005.
30. Hannun YA, Loomis CR, Bell RM. Protein kinase C activation in mixed micelles. J Biol Chem 261: 7184-7190, 1986.
31. Hazel JR. Effects of temperature on the structure and metabolism of cell membranes in fish. Am J Physiol Regul Integr Comp Physiol 246: R460-R470, 1984.
32. Hazel JR. Adaptation to temperature: phospholipid synthesis in hepatocytes of rainbow trout. Am J Physiol Regul Integr Comp Physiol 258: R1495-R1501, 1990.
33. Hazel JR. Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19-42, 1995.
34. Hazel JR, Carpenter R. Rapid changes in the phospholipid composition of gill membranes during thermal acclimation of the rainbow trout, Salmo gairdneri. J Comp Physiol [B] 155: 597-602, 1985.
35. Hazel JR, Landrey SR. Time course of thermal adaptation in plasma membranes of trout kidney. I. Headgroup composition. Am J Physiol Regul Integr Comp Physiol 255: R622-R627, 1988.
36. Hazel JR, Landrey SR. Time course of thermal adaptation in plasma membranes of trout kidney. II. Molecular species composition. Am J Physiol Regul Integr Comp Physiol 255: R628-R634, 1988.
37. Hendriks T, Klompmakers AA, Daemen FJM, Bonting SL. Biochemical aspects of the visual process. XXXII. Movement of sodium ions through bilayers composed of retinal and rod outer segment lipids. Biochim Biophys Acta 433: 271-281, 1976.
38. Hermansson M, Uphoff A, Käkelä R, Somerharju P. Quantitative analysis of complex lipidomes by liquid chromatography/mass spectrometry. Anal Chem 77: 2166-2175, 2005.
39. Horoszewicz L. Lethal and "disturbing" temperatures in some fish species from lakes with normal and artificially elevated temperature. J Fish Biol 5: 165-181, 1973.
40. Hsieh SL, Kuo CM. Stearoyl-CoA desaturase expression and fatty acid composition in milkfish (Chanos chanos) and grass carp (Ctenopharyngodon idella) during cold acclimation. Comp Biochem Physiol B 141: 95-101, 2005.
41. Hsu FF, Bohrer A, Turk J. Electrospray ionization tandem mass spectrometric analysis of sulfatide. Determination of fragmentation patterns and characterization of molecular species expressed in brain and in pancreatic islets. Biochim Biophys Acta 1392: 202-216, 1998.
42. 2H NMR and molecular dynamics simulations. J Am Chem Soc 124: 298-309, 2002.
43. 17O NMR. Biophys J 73: 855-864, 1997.
44. Ikezawa H. Glycosylphosphatidylinositol-anchored proteins. Biol Pharm Bull 25: 409-417, 2002.
45. Käkelä R, Somerharju P, Tyynelä J. Analysis of phospholipid molecular species in brains from patients with infantile and juvenile neuronalceroid lipofuscinosis using liquid chromatography-electrospray ionization mass spectrometry. J Neurochem 84: 1051-1065, 2003.
46. Käkelä R, Käkelä A, Kahle S, Becker PH, Kelly A, Furness RW. Fatty acid signatures in plasma of captive herring gulls as indicators of demersal or pelagic fish diet. Mar Ecol Progr Ser 293: 191-200, 2005.
47. Kang JX, Leaf A. Prevention of fatal cardiac arrhythmias by polyunsaturated fatty acids. Am J Clin Nutr 71: 202S-207S, 2000.
48. Koenig BW, Strey HH, Gawrish K. Membrane lateral compressibility determined by NMR and x-ray diffraction: effect of acyl chain polyunsaturation. Biophys J 73: 1954-1966, 1997.
49. Kraffe E, Marty Y, Guderley H. Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhyncus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210: 149-165, 2007.
50. Kusumi A, Suzuki K. Towards understanding the dynamics of membrane-raft-based molecular interactions. Biochim Biophys Acta 1746: 234-251, 2005.
51. Lee AG. How lipids and proteins interact in a membrane: a molecular approach. Mol Biosyst 1: 203-212, 2005.
52. Li F, Chen H, Anderson RE. Biosynthesis of docosahexaenoate- containing glycerolipid molecular species in the retina. J Mol Neurosci 16: 205-221, 2001.
53. Li Q, Wang M, Tan L, Wang C, Ma J, Li N, Li Y, Xu G, Li J. Docosahexaenoic acid changes lipid composition and interleukin-2 receptor signaling in membrane rafts. J Lipid Res 46: 1904-1913, 2005.
54. Logue JA, De Vries AL, Fodor E, Cossins AR. Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203: 2105-2115, 2000.
55. Lohner K. Is the high propensity of ethanolamine plasmalogens to form non-lamellar lipid structures manifested in the properties of biomembranes? Chem Phys Lipids 81: 167-184, 1996.
56. Lushchak VI, Bagnyukova TV. Temperature increase results in oxidative stress in goldfish tissues. 1. Indices of oxidative stress. Comp Biochem Physiol C 143: 30-35, 2006.
57. Lushchak VI, Bagnyukova TV. Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comp Biochem Physiol C 143: 36-41, 2006.
58. Ma DWL, Seo J, Switzer KC, Fan YY, McMurray DN, Lupton JR, Chapkin RS. n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J Nutr Biochem 15: 700-706, 2004.
59. Marius P, Alvis SJ, East JM, Lee AG. The interfacial lipid binding site on the potassium channel KcsA is specific for anionic phospholipids. Biophys J 89: 4081-4089, 2005.
60. Mills K, Eaton S, Ledger V, Young E, Winchester B. The synthesis of internal standards for the quantitative determination of sphingolipids by tandem mass spectrometry. Rapid Commun Mass Spectrom 19: 1739-1748, 2005.
61. Mitchell DC, Niu SL, Litman BJ. DHA-rich phospholipids optimize G-protein-coupled signaling. J Pediatr 143: S80-S86, 2003.
62. Naoi M, Lee YC, Roseman S. Rapid and sensitive determination of sphingosine bases and sphingolipid with fluorescamine. Anal Biochem 58: 571-577, 1974.
63. Nilsson GE. Surviving anoxia with the brain turned on. News Physiol Sci 16: 217-221, 2001.
64. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9: 484-496, 1995.
65. Ntambi JM. Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. J Lipid Res 40: 1549-1558, 1999.
66. Piironen J, Holopainen IJ. A note on seasonality in anoxia tolerance of crucian carp (Carassius carassius L.) in the laboratory. Ann Zool Fenn 23: 335-338, 1986.
67. Poling JS, Karanian JW, Salem N Jr, Vicini S. Time- and voltage-dependent block of delayed rectifier potassium channels by docosahexaenoic acid. Mol Pharmacol 47: 381-390, 1995.
68. Polozova A, Litman BJ. Cholesterol dependent recruitment of di22:6-PC by a G protein-coupled receptor into lateral domains. Biophys J 79: 2632-2643, 2000.
69. + channel RCK domain with charged membrane surfaces. Biochemistry 44: 62-71, 2005.
70. Ramstedt B, Slotte JP. Membrane properties of sphingomyelins. FEBS Lett 531: 33-37, 2002.
71. Robertson JC, Hazel JR. Cholesterol content of trout plasma membranes varies with acclimation temperature. Am J Physiol Regul Integr Comp Physiol 269: R1113-R1119, 1995.
72. Saiz L, Klein ML. Structural properties of a highly polyunsaturated lipid bilayer from molecular dynamics simulations. Biophys J 81: 204-216, 2001.
73. Salem N Jr, Niebylski CD. The nervous system has an absolute molecular species requirement for proper function. Mol Membr Biol 12: 131-134, 1995.
74. Samsonov AV, Mihalyov I, Cohen FS. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys J 81: 1486-1500, 2001.
75. Shaikh SR, Dumaual AC, Castillo A, LoCascio D, Siddiqui RA, Stillwell W, Wassall SR. Oleic and docosahexaenoic acid differentially phase separate from lipid raft molecules: a comparative NMR, DSC, AFM, and detergent extraction study. Biophys J 87: 1752-1766, 2004.
76. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 387: 569-572, 1997.
77. Sinensky M. Homeoviscous adaptation-a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71: 522-525, 1974.
78. Smaby JM, Momsen MM, Brockman HL, Brown RE. Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol. Biophys J 73: 1492-1505, 1997.
79. Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 126: 1-27, 2003.
80. Stillwell W, Jenski LJ, Crump FT, Ehringer W. Effect of docosahexaenoic acid on mouse mitochondrial membrane properties. Lipids 32: 497-506, 1997.
81. Sullards MC, Merrill AH Jr. Analysis of sphingosine1-phosphate, ceramides, and other bioactive sphingolipids by highperformance liquid chromatography-tandem mass spectrometry. Sci STKE 67: PL1, 2001.
82. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Mü ller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmü ller H, Heuser J, Wieland F, Jahn R. Molecular anatomy of a trafficking organelle. Cell 127: 831-846, 2006.
83. Treen M, Uauy RD, Jameson DM, Thomas VL, Hoffman DR. Effect of docosahexaenoic acid on membrane fluidity and function in intact cultured Y-79 retinoblastoma cells. Arch Biochem Biophys 294: 564-570, 1992.
84. Turner N, Else PL, Hulbert AJ. Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease sates and metabolism. Naturwissenschaften 90: 521-523, 2003.
85. Van den Brink-van der Laan E, Killian JA, de Kruijff B. Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim Biophys Acta 1666: 275-288, 2004.
86. Van Echten-Deckert G, Herget T. Sphingolipid metabolism in neural cells. Biochim Biophys Acta 1758: 1978-1994, 2006.
87. Virtanen JA, Cheng KH, Somerharju P. Phospholipid composition of the mammalian red cell membrane can be rationalized by a superlattice model. Proc Natl Acad Sci USA 95: 4964-4969, 1998.
88. +-ATPase activity in the brain of crucian carp. Am J Physiol Regul Integr Comp Physiol 291: R1482-R1489, 2006.
89. Vreugdenhil M, Bruehl C, Voskuyl RA, Kang JX, Leaf A, Wadman WJ. Polyunsaturated fatty acids modulate sodium and calcium currents in CA1 neurons. Proc Natl Acad Sci USA 93: 12559-12563, 1996.
90. Wang X, Bogdanov M, Dowhan W. Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J 21: 5673-5681, 2002.
91. Wenk MR, De Camilli P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc Natl Acad Sci USA 98: 5619-5624, 2004.
92. Williams EE, Hazel JR. Thermal adaptation in fish membranes: temporal resolution of adaptive mechanisms. In: Temperature Adaptation of Biological Membranes, edited by Cossins AR. London: Portland Press, 1994, p. 91-106.
93. Williams EE, Jenski LJ, Stillwell W. Docosahexaenoic acid (DHA) alters the structure and composition of membranous vesicles exfoliated from the surface of a murine leukemia cell line. Biochim Biophys Acta 1371: 351-362, 1998.
94. Zachowski A. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J 294: 1-14, 1993.
95. Zehmer JK, Hazel JR. Plasma membrane rafts of rainbow trout are subject to thermal acclimation. J Exp Biol 206: 1657-1667, 2003.
96. Zehmer JK, Hazel JR. Thermally induced changes in lipid composition of raft and non-raft regions of hepatocyte plasma membranes of rainbow trout. J Exp Biol 208: 4283-4290, 2005.
97. Zerouga M, Jenski LJ, Stillwell W. Comparison of phosphatidylcholines containing one or two docosahexaenoic acyl chains on properties of phospholipid monolayers and bilayers. Biochim Biophys Acta 1236: 266-272, 1995.