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Cellular and Molecular Neurobiology

, Volume 32, Issue 1, pp 41–48 | Cite as

Unique Induction of CA1 LTP Components After Intake of Theanine, an Amino Acid in Tea Leaves and its Effect on Stress Response

  • Atsushi Takeda
  • Haruna Tamano
  • Miki Suzuki
  • Kazuhiro Sakamoto
  • Naoto Oku
  • Hidehiko Yokogoshi
Original Research

Abstract

Theanine, γ-glutamylethylamide, is one of the major amino acid components in green tea. This study was undertaken to evaluate the effect of theanine intake on long-term potentiation (LTP) induction at hippocampal CA1 synapses and exposure to acute stress. Young rats were fed water containing 0.3% theanine after birth. Key findings: Serum corticosterone level was markedly decreased by theanine intake. Because this decrease can modify synaptic plasticity, the effect of theanine intake was examined focused on CA1 LTP induction. CA1 LTP induced by a 100-Hz tetanus for 1 s was almost the same extent in hippocampal slices from theanine-administered rats, whereas that induced by a 200-Hz tetanus for 1 s was significantly attenuated. 2-Amino-5-phosphonovalerate (APV), an N-methyl-d-aspartate (NMDA) receptor antagonist, significantly attenuated CA1 LTP induced by a 200-Hz tetanus in the control rats, but not in theanine-administered rats. Interestingly, APV completely blocked CA1 LTP induced by a 100-Hz tetanus in the control rats, while scarcely blocking it in theanine-administered rats. These results indicate that theanine intake reduces NMDA receptor-dependent CA1 LTP, while increasing NMDA receptor-independent CA1 LTP. Furthermore, neither 100-Hz tetanus-induced LTP nor 200-Hz tetanus-induced LTP was attenuated in theanine-administered rats after exposure to tail suspension stress, suggesting that the lack of NMDA receptor-dependent CA1 LTP by theanine intake is involved in ameliorating the attenuation of CA1 LTP after tail suspension. This study is the first to indicate that theanine intake modifies the mechanism of CA1 LTP induction.

Keywords

Theanine Green tea LTP Hippocampus NMDA receptor Stress 

References

  1. Abreu LN, Lafer B, Baca-Garcia E, Oquendo MA (2009) Suicidal ideation and suicide attempts in bipolar disorder type I: an update for the clinician. Rev Bras Psiquiatr 31:271–280PubMedCrossRefGoogle Scholar
  2. Asrar S, Zhou Z, Ren W, Jia Z (2009) Ca(2+) permeable AMPA receptor induced long-term potentiation requires PI3/MAP kinases but not Ca/CaM-dependent kinase II. PLoS One 4:e4339PubMedCrossRefGoogle Scholar
  3. Bolling BW, Chen CY, Blumberg JB (2009) Tea and health: preventive and therapeutic usefulness in the elderly? Curr Opin Clin Nutr Metab Care 12:42–48PubMedCrossRefGoogle Scholar
  4. Borroni AM, Fichtenholtz H, Woodside BL, Teyler TJ (2000) Role of voltage-dependent calcium channel long-term potentiation (LTP) and NMDA LTP in spatial memory. J Neurosci 20:9272–9276PubMedGoogle Scholar
  5. Cho HS, Kim S, Lee SY, Park JA, Kim SJ, Chun HS (2008) Protective effect of the green tea component, l-theanine on environmental toxins-induced neuronal cell death. Neurotoxicology 29:656–662PubMedCrossRefGoogle Scholar
  6. Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381PubMedCrossRefGoogle Scholar
  7. Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. J Am Med Assoc 267:1244–1252CrossRefGoogle Scholar
  8. Di X, Yan J, Zhao Y, Zhang J, Shi Z, Chang Y, Zhao B (2010) l-theanine protects the APP (Swedish mutation) transgenic SH-SY5Y cell against glutamate-induced excitotoxicity via inhibition of the NMDA receptor pathway. Neuroscience 168:778–786PubMedCrossRefGoogle Scholar
  9. Egashira N, Hayakawa K, Mishima K, Kimura H, Iwasaki K, Fujiwara M (2004) Neuroprotective effect of gamma-glutamylethylamide (theanine) on cerebral infarction in mice. Neurosci Lett 363:58–61PubMedCrossRefGoogle Scholar
  10. Einöther SJ, Martens VE, Rycroft JA, De Bruin EA (2010) l-theanine and caffeine improve task switching but not intersensory attention or subjective alertness. Appetite 54:406–409PubMedCrossRefGoogle Scholar
  11. Garcia R (2001) Stress, hippocampal plasticity, and spatial learning. Synapse 40:180–183PubMedCrossRefGoogle Scholar
  12. Gonzalez de Mejia E, Ramirez-Mares MV, Puangpraphant S (2009) Bioactive components of tea: cancer, inflammation and behavior. Brain Behav Immun 23:721–732CrossRefGoogle Scholar
  13. Graham HN (1992) Green tea composition, consumption, and polyphenol chemistry. Prev Med 21:334–350PubMedCrossRefGoogle Scholar
  14. Grover LM, Teyler TJ (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347:477–479PubMedCrossRefGoogle Scholar
  15. Haskell CF, Kennedy DO, Milne AL, Wesnes KA, Scholey AB (2008) The effects of l-theanine, caffeine and their combination on cognition and mood. Biol Psychol 77:113–122PubMedCrossRefGoogle Scholar
  16. Howland JG, Wang YT (2008) Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 169:145–158PubMedCrossRefGoogle Scholar
  17. Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134PubMedCrossRefGoogle Scholar
  18. Joëls M, Krugers HL (2007) LTP after stress: up or down? Neural Plast 2007:93202PubMedCrossRefGoogle Scholar
  19. Kakuda T (2011) Neuroprotective effects of theanine and its preventive effects on cognitive dysfunction. Pharmacol Res 64:162–168Google Scholar
  20. Kakuda T, Nozawa A, Sugimoto A, Niino H (2002) Inhibition by theanine of binding of [3H]AMPA, [3H]kainate, and [3H]MDL 105, 519 to glutamate receptors. Biosci Biotechnol Biochem 66:2683–2686PubMedCrossRefGoogle Scholar
  21. Keller-Wood ME, Dallman MF (1984) Corticosteroid inhibition of ACTH secretion. Endocr Rev 5:1–24PubMedCrossRefGoogle Scholar
  22. Kelly SP, Gomez-Ramirez M, Montesi JL, Foxe JJ (2008) l-theanine and caffeine in combination affect human cognition as evidenced by oscillatory alpha-band activity and attention task performance. J Nutr 138:1572S–1577SPubMedGoogle Scholar
  23. Kim JJ, Yoon KS (1998) Stress: metaplastic effects in the hippocampus. Trends Neurosci 21:505–509PubMedCrossRefGoogle Scholar
  24. Kim JJ, Foy MR, Thompson RF (1996) Behavioral stress modifies hippocampal plasticity through N-methyl-d-aspartate receptor activation. Proc Natl Acad Sci USA 93:4750–4753PubMedCrossRefGoogle Scholar
  25. Kimura K, Ozeki M, Juneja LR, Ohira H (2007) l-Theanine reduces psychological and physiological stress responses. Biol Psychol 74:39–45PubMedCrossRefGoogle Scholar
  26. Kobayashi K, Nagato Y, Aoi N, Juneja LR, Kim M, Yamamoto T, Sugimoto S (1998) Effects of l-theanine on the release of α-brain waves in human volunteers. Nippon Nogeikagaku Kaishi 72:153–157CrossRefGoogle Scholar
  27. Linthorst AC, Reul JM (2008) Stress and the brain: solving the puzzle using microdialysis. Pharmacol Biochem Behav 90:163–173PubMedCrossRefGoogle Scholar
  28. Mann JJ, Apter A, Bertolote J, Beautrais A, Currier D, Haas A, Hegerl U, Lonnqvist J, Malone K, Marusic A, Mehlum L, Patton G, Phillips M, Rutz W, Rihmer Z, Schmidtke A, Shaffer D, Silverman M, Takahashi Y, Varnik A, Wasserman D, Yip P, Hendin H (2005) Suicide prevention strategies: a systematic review. JAMA 294:2064–2074PubMedCrossRefGoogle Scholar
  29. McEwen BS (1999) Stress and hippocampal plasticity. Ann Rev Neurosci 22:105–122PubMedCrossRefGoogle Scholar
  30. McKay DL, Blumberg HR (2002) The role of tea in human health: an update. J Am Coll Nutr 21:1–13PubMedGoogle Scholar
  31. Nathan PJ, Lu K, Gray M, Oliver C (2006) The neuropharmacology of l-theanine(N-ethyl-l-glutamine): a possible neuroprotective and cognitive enhancing agent. J Herb Pharmacother 6:21–30PubMedGoogle Scholar
  32. Shankar S, Teyler TJ, Robbins N (1998) Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 79:334–341PubMedGoogle Scholar
  33. Shimbo M, Nakamura K, Shi HJ, Kizuki M, Seino K, Inose T, Takano T (2005) Green tea consumption in everyday life and mental health. Public Health Nutr 8:1300–1306PubMedCrossRefGoogle Scholar
  34. Smriga M, Saito H, Nishiyama N (1996) Hippocampal long- and short-term potentiation is modulated by adrenalectomy and corticosterone. Neuroendocrinology 64:35–41PubMedCrossRefGoogle Scholar
  35. Takeda A, Tamano H (2009) Insight into zinc signaling from dietary zinc deficiency. Brain Res Rev 62:33–34PubMedCrossRefGoogle Scholar
  36. Takeda A, Tamano H (2010) Zinc signaling through glucocorticoid and glutamate signaling in stressful circumstances. J Neurosci Res 88:3002–3010PubMedCrossRefGoogle Scholar
  37. Takeda A, Tamano H, Kan F, Itoh H, Oku N (2007) Anxiety-like behavior of young rats after 2-week zinc deprivation. Behav Brain Res 177:1–6PubMedCrossRefGoogle Scholar
  38. Takeda A, Sakamoto K, Tamano H, Fukura K, Inui N, Suh SW, Won SJ, Yokogoshi H (2011) Facilitated neurogenesis in the developing hippocampus after intake of theanine, an amino acid in tea leaves, and object recognition memory. Cell Mol Neurobiol (in press)Google Scholar
  39. Terashima T, Takido J, Yokogoshi H (1999) Time-dependent changes of amino acids in the serum, liver, brain and urine of rats administered with theanine. Biosci Biotechnol Biochem 63:615–618PubMedCrossRefGoogle Scholar
  40. Unno T, Suzuki Y, Kakuda T, Hayakawa T, Tsuge H (1999) Metabolism of theanine, gamma-glutamylethylamide, in rats. J Agric Food Chem 47:1593–1596PubMedCrossRefGoogle Scholar
  41. Wiegert O, Pu Z, Shor S, Joëls M, Krugers H (2005) Glucocorticoid receptor activation selectively hampers N-methyl-D-aspartate receptor dependent hippocampal synaptic plasticity in vitro. Neuroscience 135:403–411PubMedCrossRefGoogle Scholar
  42. Wong TP, Howland JG, Robillard JM, Ge Y, Yu W, Titterness AK, Brebner K, Liu L, Weinberg J, Christie BR, Phillips AG, Wang YT (2007) Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc Natl Acad Sci USA 104:11471–11476PubMedCrossRefGoogle Scholar
  43. Woodside BL, Borroni AM, Hammonds MD, Teyler TJ (2004) NMDA receptors and voltage-dependent calcium channels mediate different aspects of acquisition and retention of a spatial memory task. Neurobiol Learn Mem 81:105–114PubMedCrossRefGoogle Scholar
  44. Yamada T, Terashima T, Wada K, Ueda S, Ito M, Okubo T, Juneja LR, Yokogoshi H (2007) Theanine, r-glutamylethylamide, increases neurotransmission concentrations and neurotrophin mRNA levels in the brain during lactation. Life Sci 81:1247–1255PubMedCrossRefGoogle Scholar
  45. Yamada T, Terashima T, Honma H, Nagata S, Okubo T, Juneja LR, Yokogoshi H (2008) Effects of theanine, a unique amino acid in tea leaves, on memory in a rat behavioral test. Biosci Biotechnol Biochem 72:1356–1359PubMedCrossRefGoogle Scholar
  46. Yokogoshi H, Terashima T (2000) Effect of theanine, r-glutamylethylamide, on brain monoamines, striatal dopamine release and some kinds of behavior in rats. Nutrition 16:776–777PubMedCrossRefGoogle Scholar
  47. Yokogoshi H, Kobayashi M, Mochizuki M, Terashima T (1998) Effect of theanine, r-glutamylethylamide, on brain monoamines and striatal dopamine release in conscious rats. Neurochem Res 23:667–673PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Atsushi Takeda
    • 1
  • Haruna Tamano
    • 1
  • Miki Suzuki
    • 1
  • Kazuhiro Sakamoto
    • 2
  • Naoto Oku
    • 1
  • Hidehiko Yokogoshi
    • 2
  1. 1.Graduate School of Pharmaceutical SciencesUniversity of Shizuoka, Global COEShizuokaJapan
  2. 2.Graduate School of Nutritional and Environmental SciencesUniversity of Shizuoka, Global COEShizuokaJapan

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