Neurobiology of Aging
Volume 28, Issue 8 , Pages 1179-1186 , August 2007

Arachidonic acid preserves hippocampal neuron membrane fluidity in senescent rats

  • Taisuke Fukaya

      Affiliations

    • Graduate School of High-Technology for Human Welfare, Tokai University, Numazu 410-0321, Shizuoka, Japan
  • ,
  • Takumi Gondaira

      Affiliations

    • School of High-Technology for Human Welfare, Tokai University, Numazu 410-0321, Shizuoka, Japan
  • ,
  • Yasuto Kashiyae

      Affiliations

    • School of High-Technology for Human Welfare, Tokai University, Numazu 410-0321, Shizuoka, Japan
  • ,
  • Susumu Kotani

      Affiliations

    • Department of Pharmacology, School of Medicine, Kanazawa University, Kanazawa 920-8640, Ishikawa, Japan
  • ,
  • Yoshiyuki Ishikura

      Affiliations

    • Institute of Health Care Science, SUNTORY Ltd. Shimamoto 618-8503, Osaka, Japan
  • ,
  • Shigeaki Fujikawa

      Affiliations

    • Institute of Health Care Science, SUNTORY Ltd. Shimamoto 618-8503, Osaka, Japan
  • ,
  • Yoshinobu Kiso

      Affiliations

    • Institute of Health Care Science, SUNTORY Ltd. Shimamoto 618-8503, Osaka, Japan
  • ,
  • Manabu Sakakibara

      Affiliations

    • School of High-Technology for Human Welfare, Tokai University, Numazu 410-0321, Shizuoka, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 55 968 1111; fax: +81 55 968 1156.

Received 7 December 2005 ,Revised 29 March 2006 ,Accepted 22 May 2006.

References 

  1. Barcelo-Coblijn G, Hogyes E, Kitajka K, Puskas LG, Zvara A, Hackler L, et al. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proc Natl Acad Sci USA. 2003;100:11321–11326
  2. Bousserouel S, Brouillet A, Bereziat G, Raymondjean M, Andreani M. Different effects of n−6 and n−3 polyunsaturated fatty acids on the activation of rat smooth muscle cells by interleukin-1 beta. J Lipid Res. 2003;44:601–611
  3. Bousserouel S, Raymondjean M, Brouillet A, Bereziat G, Andreani M. Modulation of cyclin D1 and early growth response factor-1 gene expression in interleukin-1beta-treated rat smooth muscle cells by n−6 and n−3 polyunsaturated fatty acids. Eur J Biochem. 2004;271:4462–4473
  4. Calder PC. Dietary modification of inflammation with lipids. Proc Nutr Soc. 2002;61:345–358
  5. Cotrina ML, Gao Q, Lin JH, Nedergaard M. Expression and function of astrocytic gap junctions in aging. Brain Res. 2001;901:55–61
  6. Dumuis A, Sebben M, Haynes L, Pin JP, Bockaert J. NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature. 1988;336:68–70
  7. Edidin M, Zuniga MC, Sheetz MP. Truncation mutants define and locate cytoplasmic barriers to lateral mobility of membrane glycoproteins. Proc Natl Acad Sci USA. 1994;91:3378–3382
  8. Foster TC. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Brain Res Rev. 1999;30:236–249
  9. Fujita S, Ikegaya Y, Nishikawa M, Nishiyama N, Matsuki N. Docosahexaenoic acid improves long-term potentiation attenuated by phospholipase A(2) inhibitor in rat hippocampal slices. Br J Pharmacol. 2001;132:1417–1422
  10. Ghosh PK, Vasanji A, Murugesan G, Eppell SJ, Graham LM, Fox PL. Membrane microviscosity regulates endothelial cell motility. Nat Cell Biol. 2002;4:894–900
  11. Greiner RS, Moriguchi T, Hutton A, Slotnick BM, Salem N. Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids. 1999;34(Suppl):S239–S243
  12. Hagve TA, Woldseth B, Brox J, Narce M, Poisson JP. Membrane fluidity and fatty acid metabolism in kidney cells from rats fed purified eicosapentaenoic acid or purified docosahexaenoic acid. Scand J Clin Lab Invest. 1998;58:187–194
  13. Hashimoto M, Shahdat MH, Shimada T, Yamasaki H, Fujii Y, Ishibashi Y, et al. Relationship between age-related increases in rat liver lipid peroxidation and bile canalicular plasma membrane fluidity. Exp Gerontol. 2001;37:89–97
  14. Horrocks LA, Farooqui AA. Docosahexaenoic acid in the diet: its importance in maintenance and restoration of neural membrane function. Prostaglandins Leukot Essent Fatty Acids. 2004;70:361–372
  15. Horrocks LA, Yeo YK. Health benefits of docosahexaenoic acid (DHA). Pharmacol Res. 1999;40:211–225
  16. Kenworthy AK, Nichols BJ, Remmert CL, Hendrix GM, Kumar M, Zimmerberg J, et al. Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol. 2004;165:735–746
  17. Kessler AR, Yehuda S. Learning-induced changes in brain membrane cholesterol and fluidity: implications for brain aging. Int J Neurosci. 1985;28:73–82
  18. Kitani K, Kanai S, Carrillo MC, Ivy GO. (-)Deprenyl increases the life span as well as activities of superoxide dismutase and catalase but not of glutathione peroxidase in selective brain regions in Fischer rats. Ann NY Acad Sci. 1994;717:60–71
  19. Kotani S, Nakazawa H, Tokimasa T, Akimoto K, Kawashima H, Toyoda-Ono Y, et al. Synaptic plasticity preserved with arachidonic acid diet in aged rats. Neurosci Res. 2003;46:453–461
  20. Leifert WR, Jahangiri A, McMurchie EJ. Membrane fluidity changes are associated with the antiarrhythmic effects of docosahexaenoic acid in adult rat cardiomyocytes. J Nutr Biochem. 2000;11:38–44
  21. Lippincott-Schwartz J, Presley JF, Zaal KJ, Hirschberg K, Miller CD, Ellenberg J. Monitoring the dynamics and mobility of membrane proteins tagged with green fluorescent protein. Methods Cell Biol. 1999;58:261–281
  22. Lippincott-Schwartz J, Snapp E, Kenworthy A. Studying protein dynamics in living cells. Nat Rev Mol Cell Biol. 2001;2:444–456
  23. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001;29:243–254
  24. Lynch MA. Age-related impairment in long-term potentiation in hippocampus: a role for the cytokine, interleukin-1 beta?. Prog Neurobiol. 1998;56:571–589
  25. Lynch MA, Voss KL. Membrane arachidonic acid concentration correlates with age and induction of long-term potentiation in the dentate gyrus in the rat. Eur J Neurosci. 1994;6:1008–1014
  26. Malle E, Sattler W, Prenner E, Leis HJ, Hermetter A, Gries A, et al. Effects of dietary fish oil supplementation on platelet aggregability and platelet membrane fluidity in normolipemic subjects with and without high plasma Lp(a) concentrations. Atherosclerosis. 1991;88:193–201
  27. Martin DS, Spencer P, Horrobin DF, Lynch MA. Long-term potentiation in aged rats is restored when the age-related decrease in polyunsaturated fatty acid concentration is reversed. Prostaglandins Leukot Essent Fatty Acids. 2002;67:121–130
  28. McGahon B, Lynch MA. A study of the synergism between metabotropic glutamate receptor activation and arachidonic acid in the rat hippocampus. Neuroreport. 1994;5:2353–2357
  29. Moriguchi T, Greiner RS, Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem. 2000;75:2563–2573
  30. Muccioli G, Raso GM, Ghe C, Di Carlo R. Effect of l-alpha glycerylphosphorylcholine on muscarinic receptors and membrane microviscosity of aged rat brain. Prog Neuropsychopharmacol Biol Psychiatry. 1996;20:323–339
  31. Muccioli G, Scordamaglia A, Bertacco S, Di Carlo R. Effect of S-adenosyl-l-methionine on brain muscarinic receptors of aged rats. Eur J Pharmacol. 1992;227:293–299
  32. Murray CA, Lynch MA. Dietary supplementation with vitamin E reverses the age-related deficit in long term potentiation in dentate gyrus. J Biol Chem. 1998;273:12161–12168
  33. Narayanan BA, Narayanan NK, Reddy BS. Docosahexaenoic acid regulated genes and transcription factors inducing apoptosis in human colon cancer cells. Int J Oncol. 2001;19:1255–1262
  34. Okaichi Y, Ishikura Y, Akimoto K, Kawashima H, Toyoda-Ono Y, Kiso Y, et al. Arachidonic acid improves aged rats’ spatial cognition. Physiol Behav. 2005;84:617–623
  35. SanGiovanni JP, Chew EY. The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res. 2005;24:87–138
  36. Scheuer K, Rostock A, Bartsch R, Muller WE. Piracetam improves cognitive performance by restoring neurochemical deficits of the aged rat brain. Pharmacopsychiatry. 1999;32(Suppl 1):10–16
  37. Simopoulos AP, Leaf A, Salem N. Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. Issfal Newslett. 1999;6:14–16
  38. Singer SJ, Nicolson GL. The fluid mosaic model of the structure of cell membranes. Science. 1972;175:720–731
  39. Sneddon AA, Wu HC, Farquharson A, Grant I, Arthur JR, Rotondo D, et al. Regulation of selenoprotein GPx4 expression and activity in human endothelial cells by fatty acids, cytokines and antioxidants. Atherosclerosis. 2003;171:57–65
  40. Soderberg M, Edlund C, Kristensson K, Dallner G. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids. 1991;26:421–425
  41. Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids. 2003;126:1–27
  42. Tapiero H, Ba GN, Couvreur P, Tew KD. Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies. Biomed Pharmacother. 2002;56:215–222
  43. Tillman TS, Cascio M. Effects of membrane lipids on ion channel structure and function. Cell Biochem Biophys. 2003;38:161–190
  44. Vereb G, Szollosi J, Matko J, Nagy P, Farkas T, Vigh L, et al. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc Natl Acad Sci USA. 2003;100:8053–8058
  45. Yehuda S, Rabinovitz S, Carasso RL, Mostofsky DI. The role of polyunsaturated fatty acids in restoring the aging neuronal membrane. Neurobiol Aging. 2002;23:843–853
  46. Yu C, Zuo P, Song C. Study of experimental hypoparathyroidism in rats. III. Fluidity changes in brain synaptolemma. Chin Med Sci J. 1992;7:213–215
  47. Zanotti A, Valzelli L, Toffano G. Chronic phosphatidylserine treatment improves spatial memory and passive avoidance in aged rats. Psychopharmacology (Berl). 1989;99:316–321
  48. Zs-Nagy I. The membrane hypothesis of aging: its relevance to recent progress in genetic research. J Mol Med. 1997;75:703–714

PII: S0197-4580(06)00182-5

doi: 10.1016/j.neurobiolaging.2006.05.023

Neurobiology of Aging
Volume 28, Issue 8 , Pages 1179-1186 , August 2007