Synaptic inhibition and γ-aminobutyric acid in the mammalian central nervous system

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 89, Issue 4, 2013, Pages 139-156

  Obata, Kunihiko ^a  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Brain development; GABA; Gene targeting; Mental disorders; Neurotransmitter

Indexed keywords

INVERTEBRATA; MAMMALIA; VERTEBRATA;

EID: 84878362216     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.89.139     Document Type: Review

References (113)

1. Sherrington, C.S. (1906) The Integrative Action of the Nervous System. Yale Univ. Press, New Haven, CT, pp. 1-413.
2. Granit, R. (1967) Charles Scott Sherrington an Appraisal. Doubleday & Co., Garden City, NY, pp. 1-188.
3. Eccles, J.C. (1964) The Physiology of Synapses. Springer, Berlin, pp. 1-316.
4. Finger, S. (1994) Origins of Neuroscience. Oxford Univ. Press, New York, NY, p. 47.
5. Setchenov, I.M. (1863) ref1lexes of the Brain. (Russian pamphlet).
6. Pavlov, I.P. (1927) Conditioned ref1lexes (translated by Anrep, G.V.). Dover Publications, Mineola, NY, pp. 1-430.
7. Katz, B. (1966) Nerve, Muscle, and Synapse. McGraw-Hill, New York, NY, pp. 1-193.
8. Brock, T.D. (1988) Robert Koch-a Life in Medicine and Bacteriology. Science Tech. Publishers & Springer-Verlag, Berlin.
9. Cooper, J.R., Bloom, F.E. and Roth, R.H. (1996) The Biochemical Basis of Neuropharmacology. Seventh Edition. Oxford Univ. Press, New York, NY, pp. 4-5, pp. 171-190.
10. Obata, K. (1977) Biochemistry and physiology of amino acid transmitters. In Handbook of Physiology- The Nervous System I (eds. Kandel, E.R. et al.). The Amer. Physiol. Soc., Bethesda, MD, pp. 625-650.
11. Loewi, O. (1921) Über humorale Übertragbarkeit der Herznervenwirkung. I Mitteilung. Pflugers Arch. Ges. Physiol. 189, 239-242.
12. Ackermann, D. (1910) Über ein neues, auf bakteriellem Wege gewinnbares Aporrhegma. Z. Physiol. Chem. 69, 273-281.
13. Okunuki, K. (1937) Über ein neues Enzym Glutaminocarboxylase. Bot. Mag. 51, 270-278.
14. Awapara, J., Landua, A.J., Fuerst, R. and Seale, B. (1950) Free γ-aminobutyric acid in brain. J. Biol. Chem. 187, 35-39.
15. Roberts, E. and Frankel, S. (1950) γ-Aminobutyric acid in brain: its formation from glutamic acid. J. Biol. Chem. 187, 55-63.
16. Roberts, E., Chase, T.N. and Tower, D.B. (eds.) (1976) GABA in Nervous System Function. Raven Press, New York, NY, pp. 1-554.
17. Martin, D.L. and Olsen, R.W. (eds.) (2000) GABA in the Nervous System The View at Fifty Years. Lippincott Williams & Wilkins, Philadelphia, PA, pp. 1-510.
18. Hayashi, T. and Nagai, K. (1956) Action of B-amino acids on the motor cortex of higher animals, especially γ-amino-O-oxybutyric acid on the real inhibitory principle in brain. Abstr. XX Int. Physiol. Congr. p. 410.
19. Hayashi, T. (1956) Chemical Physiology of Excitation in Muscle and Nerve. Nakayama Shoten, Tokyo, pp. 1-166.
20. Iwama, K. and Jasper, H.H. (1957) The action of gamma-aminobutyric acid upon cortical electrical activity in the cat. J. Physiol. 138, 365-380.
21. Curtis, D.R., Phillis, J.W. and Watkins, J.C. (1959) The depression of spinal neurones by γ-amino-nbutyric acid and O-alanine. J. Physiol. 146, 185- 203.
22. Florey, E. (1954) An inhibitory and excitatory factor of mammalian central nervous system and their action on a single sensory neurone. Arch. Int. Physiol. 62, 33-53.
23. Bazemore, A.W., Elliott, K.A.C. and Florey, E. (1957) Isolation of Factor I. J. Neurochem. 1, 334-339.
24. Jasper, H.H. (1984) The saga of K.A.C. Elliott and GABA. Neurochem. Res. 9, 447-458.
25. Kuffler, S.W. and Edwards, C. (1958) Mechanism of gamma aminobutyric acid (GABA) action and its relation to synaptic inhibition. J. Neurophysiol. 21, 589-610.
26. Hagiwara, S., Kusano, K. and Saito, S. (1960) Membrane changes in crayfish stretch receptor neuron during synaptic inhibition and under action of gamma-aminobutyric acid. J. Neurophysiol. 23, 505-515.
27. Takeuchi, A. and Takeuchi, N. (1965) Localized action of gamma-aminobutyric acid on the crayfish muscle. J. Physiol. 177, 225-238.
28. Kravitz, E.A. (2004) Edward A. Kravitz. In The History of Neuroscience in Autobiography, Vol. 4 (ed. Squire, L.R.). Academic Press, London, pp. 346-408.
29. Ito, M., Hongo, T., Yoshida, M., Okada, Y. and Obata, K. (1964) Antidromic and trans-synaptic activation of Deiters' neurones induced from the spinal cord. Jpn. J. Physiol. 14, 638-658.
30. Tsukahara, N., Toyama, K. and Kosaka, K. (1964) Intracellularly recorded responses of red nucleus neurones during antidromic and orthodromic activation. Experientia 20, 632-633.
31. Ito, M. and Yoshida, M. (1964) The cerebellarevoked monosynaptic inhibition of Deiters' neurones. Experientia 20, 515-516.
32. Ito, M., Yoshida, M. and Obata, K. (1964) Monosynaptic inhibition of the intracerebellar nuclei induced from the cerebellar cortex. Experientia 20, 575-576.
33. Obata, K. (1965) Pharmacological study on postsynaptic inhibition of Deiters' neurons. Abstr. XXIII Int. Congr. Physiol. Sci. Tokyo, 958.
34. Obata, K., Ito, M., Ochi, R. and Sato, N. (1967) Pharmacological properties of the postsynaptic inhibition by Purkinje cell axons and the action of γ-aminobutyric acid on Deiters neurons. Exp. Brain Res. 4, 43-57.
35. Krnjevic, K. and Schwartz, S. (1966) Cortical inhibition and GABA. Fed. Proc. 25, 27.
36. Curtis, D.R. and Crawford, J.M. (1969) Central synaptic transmission-microelectrophoretic studies. Annu. Rev. Pharmacol. 9, 209-240.
37. Barnard, E.A., Bilbe, G., Houamed, K., Moss, S.J., Van Renterghem, C. and Smart, T.G. (1987) Functional expression in the Xenopus oocyte of neurotransmitter receptors: further characterisation of the implanted GABA receptor. Neuropharmacology 26, 837-844.
38. Barnard, E.A., Skolnick, P., Olsen, R.W., Mohler, H., Sieghart, W., Biggio, G., Braestrup, C., Bateson, A.N. and Langer, S.Z. (1998) Subtypes of γ-aminobutyric acidA receptors: classification of the basis of subunit structure and receptor function. Pharmacol. Rev. 50, 291-313.
39. Yamamoto, C. and McIlwain, H. (1966) Electrical activities in thin sections from the mammalian brain maintained in chemically-defined media in vitro. J. Neurochem. 13, 1333-1343.
40. Kravitz, E.A., Kuffler, S.W. and Potter, D.D. (1963) Gamma-aminobutyric acid and other blocking compounds in crustacea. III. Their relative concentrations in separated motor and inhibitory axons. J. Neurophysiol. 26, 739-751.
41. Scott, E.M. and Jacoby, W.B. (1959) Soluble γ-aminobutyric-glutamic transaminase from Pseudomonas fluorescens. J. Biol. Chem. 234, 932- 936.
42. Obata, K. (1969) Gamma-aminobutyric acid in Purkinje cells and motoneurones. Experientia 25, 1283.
43. Lowry, O.H., Passonneau, J.V., Schulz, D.Z. and Rock, M.K. (1961) The measurement of enzymatic cycling. J. Biol. Chem. 236, 2746-2755.
44. Otsuka, M., Kravitz, E.A. and Potter, D.D. (1967) Physiological and chemical architecture of a lobster ganglion with particular ref1erence to gamma-aminobutyrate and glutamate. J. Neurophysiol. 30, 725-752.
45. Otsuka, M., Iversen, L.L., Hall, Z.W. and Kravitz, E.A. (1966) Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc. Natl. Acad. Sci. U.S.A. 56, 1110-1115.
46. Obata, K., Otsuka, M. and Tanaka, Y. (1970) Determination of gamma-aminobutyric acid in single nerve cells of cat central nervous system. J. Neurochem. 17, 697-698.
47. Otsuka, M., Obata, K., Miyata, Y. and Tanaka, Y. (1971) Measurement of γ-aminobutyric acid in isolated nerve cells of cat central nervous system. J. Neurochem. 18, 287-295.
48. Okada, Y. and Shimada, C. (1976) Gamma-aminobutyric acid (GABA) concentration in a single neuron-localization of GABA in Deiters' neuron. Brain Res. 107, 658-662.
49. Obata, K. and Takeda, K. (1969) Release of gamma γ-aminobutyric acid into the fourth ventricle induced by stimulation of the cat's cerebellum. J. Neurochem. 16, 1043-1047.
50. Obata, K. (1976) Release of GABA into the fourth ventricle. In GABA in Nervous System Function (eds. Roberts, E., Chase, T.N. and Tower, D.B.). Raven Press, New York, NY, pp. 251-254.
51. Obata, K. (1976) Association of GABA with cerebellar Purkinje Cells: single cell analysis. In GABA in Nervous System Function (eds. Roberts, E., Chase, T.N. and Tower, D.B.). Raven Press, New York, NY, pp. 217-222.
52. Obata, K. (1972) Acetylcholine and gamma-aminbutyric acid action on tissue-cultured cells from sympathetic ganglion, dorsal-root ganglion and diaphragm muscle. Fed. Proc. 31 (2), 231.
53. Obata, K. (1974) Transmitter sensitivities of some nerve and muscle cells. Brain Res. 73, 71-88.
54. Obata, K., Oide, M. and Tanaka, H. (1978) Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res. 144, 179-184.
55. Ben-Ari, Y., Gaiarsa, J-L., Tyzio, R. and Khazipov, R. (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284.
56. Rivera, C., Voipio, J., Payne, J.A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., Pirvola, U., Saarma, M. and Kaila, K. (1999) The KD/Cl! co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255.
57. Yamada, J., Okabe, A., Toyoda, H., Kilb, W., Luhmann, H.J. and Fukuda, A. (2004) Cl! uptake promoting depolarizing GABA actions in inmature rat neocortical neurons is mediated by NKCC1. J. Physiol. 557 (3), 829-841.
58. Ben-Ari, Y., Khazipov, R., Leinekugel, X., Caillars, O. and Gaiarsa, J.L. (1997) GABAA, NMDA and ANMPA receptors: a developmentally regulated "ménage a trois". Trends Neurosci. 20, 523-529.
59. Wagner, S., Castel, M., Gainer, H. and Yarom, Y. (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387, 598-603.
60. Choi, H.J., Lee, C.J., Schroeder, A., Kim, Y.S., Jung, S.H., Kim, J.S., Kim, D.Y., Son, E.J., Han, H.C. and Hong, S.K. (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J. Neurosci. 28, 5450-5459.
61. Bu, D.-F., Erlander, M.G., Hitz, B.C., Tillakaratne, N.J.K., Kaufman, D.L., Wagner-McPherson, C.B., Evan, G.A. and Tobin, A.J. (1992) Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene. Proc. Natl. Acad. Sci. U.S.A. 89, 2115- 2119.
62. Kobayashi, Y., Kaufman, D.L. and Tobin, A.J. (1987) Glutamic acid decarboxylase cDNA: nucleotide sequence encoding an enzymatically active fusion protein. J. Neurosci. 7, 2768-2772.
63. Silva, A.J., Payler, R., Wehner, J.M. and Tonegawa, S. (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 206-211.
64. Grant, S.G., O'Dell, T.J., Karl, K.A., Stein, P.L., Soriano, P. and Kandel, E.R. (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258, 1903-1910.
65. Asada, H., Kawamura, Y., Maruyama, K., Kume, H., Ding, R.-G., Ji, F.Y., Kanbara, N., Kuzume, H., Sanbo, M., Yagi, T. and Obata, K. (1996) Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brain but are susceptible to seizures. Biochem. Biophys. Res. Commun. 229, 891-895.
66. Asada, H., Kawamura, Y., Maruyama, K., Kume, H., Ding, R.-G., Kanbara, N., Kuzume, H., Sanbo, M., Yagi, T. and Obata, K. (1997) Cleft palate and decreased γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. U.S.A. 94, 6496-6499.
67. Obata, K., Fukuda, T., Konishi, S., Ji, F.-Y., Mitoma, H. and Kosaka, T. (1999) Synaptic localization of the 67,000 mol. wt isoform of glutamate decarboxylase and transmitter function of GABA in the mouse cerebellum lacking the 65,000 mol. wt isoform. Neuroscience 93, 1475- 1482.
68. Stork, O., Ji, F.-Y., Kaneko, K., Stork, S., Yoshinobu, Y., Moriya, T., Shibata, S. and Obata, K. (2000) Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res. 865, 45-58.
69. Stork, O., Yamanaka, H., Stork, S., Kume, N. and Obata, K. (2003) Altered conditioned fear behavior in glutamate decarboxylase 65 null mutant mice. Genes Brain Behav. 2, 65-70.
70. Esclapez, M., Tillakaratne, N.J.K., Feldblum, S., Patel, N. and Tobin, A. (1994) Comparative localization of two isoforms of glutamic acid decarboxylase and their mRNA in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14, 1834-1855.
71. Kuwana, S., Okada, Y., Sugawara, Y., Tsunekawa, N. and Obata, K. (2003) Disturbance of neural respiratory control in neonatal mice lacking GABA synthesizing enzyme 67-kDa isoform of glutamic acid decarboxylase. Neuroscience 120, 861-870.
72. Tsunekawa, N., Arata, A. and Obata, K. (2005) Development of spontaneous mouth/tongue movement and related neural activity, and their repression in fetal mice lacking glutamate decarboxylase 67. Eur. J. Neurosci. 21, 173-178.
73. Suzue, T. and Shinoda, Y. (1999) Highly reproducible spatiotemporal patterns of mammalian embryonic movements at the developmental stage of the earliest spontaneous motility. Eur. J. Neurosci. 11, 2697-2710.
74. Ji, F. and Obata, K. (1999) Development of the GABA system in organotypic culture of hippocampal and cerebellar slices from a 67-kDa isoform of glutamic acid decarboxylase (GAD67)-deficient mice. Neurosci. Res. 33, 233-237.
75. Ji, F., Kanbara, N. and Obata, K. (1999) GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms of glutamic acid decarboxylase. Neurosci. Res. 33, 187-194.
76. Fujii, M., Arata, A., Kanbara-Kume, N., Saito, K., Yanagawa, Y. and Obata, K. (2007) Respiratory activity in brainstem of fetal mice lacking glutamate decarboxylase 65/67 and vesicular GABA transporter. Neuroscience 146, 1044-1052.
77. Owens, D.F. and Kriegstein, A.R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727.
78. Saito, K., Kakizaki, T., Hayashi, R., Nishimaru, H., Furukawa, T., Nakazato, Y., Takamori, S., Ebihara, S., Uematsu, M., Mishina, M., Miyazaki, J., Yokoyama, M., Konishi, K., Inoue, K., Fukuda, A., Fukumoto, M., Nakamura, K., Obata, K. and Yanagawa, Y. (2010) The physiological roles of vesicular GABA transporter during embryonic development: a study using knockout mice. Mol. Brain 3, 40.
79. Obata, K., Hirono, M., Kume, N., Kawaguchi, Y., Itohara, S. and Yanagawa, Y. (2008) GABA and synaptic inhibition of mouse cerebellum lacking glutamate decarboxylase 67. Biochem. Biophys. Res. Commun. 370, 429-433.
80. Hoshino, M., Nakamura, S., Mori, K., Kawauchi, T., Terao, M., Nishimura, Y.V., Fukuda, A., Fuse, T., Matsuo, N., Sone, M., Watanabe, M., Bito, H., Terashima, T., Wright, C.V., Kawaguchi, Y., Nakao, K. and Nabeshima, Y. (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuron fates in cerebellum. Neuron 47, 201-213.
81. Fogarty, M.J., Smallcombe, K.L., Yanagawa, Y., Obata, K., Bellingham, M.C. and Noakes, P.G. (2013) Genetic deficiency of GABA differentially regulates respiratory and non-respiratory motor neuron development. PLoS ONE 8, e56257.
82. Banks, G.B., Kannnjhan, R., Wiese, S., Kneussel, M., Wong, L.M., O'Sullivan, G., Sendtner, M., Bellingham, M.C., Betz, H. and Noakes, P.G. (2005) Glycinergic and GABAergic synaptic activity differentially regulate motoneuron survival and skeletal muscle innervation. J. Neurosci. 25, 1249-1259.
83. Kano, M. and Hashimoto, K. (2009) Synapse elimination in the central nervous system. Curr. Opin. Neurobiol. 19, 154-161.
84. Nakayama, H., Miyazaki, T., Kitamura, K., Hashimoto, K., Yanagawa, Y., Obata, K., Sakimura, K., Watanabe, M. and Kano, M. (2012) GABAergic inhibition regulated developmental synapse elimination in the cerebellum. Cell 74, 384-396.
85. Hubel, D.H. and Wiesel, T.N. (1970) The period of susceptibility to the physiological effects of unilateral eye closure. J. Physiol. 206, 419-436.
86. Hensch, T.K., Fagiolini, M., Mataga, N., Stryker, M.P., Baekkeskov, S. and Kash, S.F. (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504-1508.
87. Hensch, T.K. (2005) Critical period mechanisms in developing visual cortex. Curr. Top. Dev. Biol. 69, 215-237.
88. Southwell, D.G., Froemke, R.C., Alvarez-Buylla, A. and Strykwr, M.P. (2010) Cortical plasticity induced by inhibitory neuron transplantation. Science 327, 1145-1148.
89. Morishita, H., Miwa, J.M., Heintz, N. and Hensch,T.K. (2010) Lynx1, a cholinergic brake limits plasticity in adult visual cortex. Science 330, 1238-1240.
90. Ferguson, N.W. (1988) Palate development. Development 103 Supplement, 41-60.
91. Ding, R., Tsunekawa, N. and Obata, K. (2004) Cleft palate by picrotoxin or 3-MP and palatal shelf elevation in GABA-deficient mice. Neurotoxicol. Teratol. 26, 587-592.
92. Iseki, S., Ishii-Suzuki, M., Tsunekawa, N., Yamada, Y., Eto, K. and Obata, K. (2007) Experimental induction of palate shef elevation in glutamate decarboxylase 67-deficient mice with cleft palate due to vertically oriented paratal shelf. Birth Def. Res. (Part A) 79, 688-695.
93. Oh, W.-J., Westmoreland, J.J., Summers, R. and Condie, B.G. (2010) Cleft palate is caused by CNS dysfunction in Gad1 and Viaat knockout mice. PLoS ONE 5, e9758.
94. Culiat, C.T., Stubbs, L.J., Woychik, R.P., Russell, L.B., Johnson, D.K. and Rinchik, E.M. (1995) Deficiency of the beta 3 subunit of the type A gamma-aminobutyric acid receptor causes cleft palate in mice. Nat. Genet. 11, 344-346.
95. Rudolph, U. and Möhler, H. (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu. Rev. Pharmacol. Toxicol. 44, 475-498.
96. Kaneko, S., Okada, M., Iwasa, H., Yamakawa, K. and Hirose, S. (2002) Genetics of epilepsy: currents status and perspectives. Neurosci. Res. 44, 11-30.
97. George, A.L. (2004) Inherited channelopathies associated with epilepsy. Epilepsy Curr. 4, 65-70.
98. Galvan, A. and Wichmann, T. (2007) GABAergic circuits in the basal ganglia and movement disorders. Prog. Brain Res. 160, 287-312.
99. Chiken, S. and Nambu, A. (2013) High frequency pallidal stimulation disrupts information flow through the pallidum by GABAergic inhibition. J. Neurosci. 33, 2268-2280.
100. McLeod, M.C., Kobayashi, N.R., Sen, A., Baghbaderani, B.A., Sadi, D., Ulalia, R., Behie, L.A. and Mendez, I. (2012) Transplantation of GABAergic cells derived from bioreactorexpanded human neural precursor cells restores motor and cognitive behavioural deficits in a rodent model of Huntington's disease. Cell Transplant. 2012 Nov. 1 (Epub ahead of print).
101. Akbarian, S., Kim, J.J., Potkin, S.G., Hagman, J.O., Tafazzoli, A., Bunney, W.E. Jr. and Jones, E.G. (1995) Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in pref1rontal cortex of schizophrenics. Arch. Gen. Psychiatry 52, 258-266.
102. Lewis, D.A., Hashimoto, T. and Volk, D.W. (2005) Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324.
103. Volk, D.W., Matsubara, T., Li, S., Sengupta, E.J., Georgiev, D., Minabe, Y., Sampson, A., Hshimoto, T. and Lewis, D.A. (2012) Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia. Am. J. Psychiatry 169, 1082-1091.
104. Sternberg, P.W. and Horvitz, H.R. (1984) The genetic control of cell lineage during nematode development. Annu. Rev. Genet. 18, 489-524.
105. McIntire, S.L., Jorgensen, E., Kaplan, J. and Horvitz, H.R. (1993) The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337-341.
106. Kandel, E.R., Schwartz, J.H., Jessel, T.M., Siegelbaum, S.A. and Hudspeth, A.J. (eds.) (2013) Principles in Neural Science. Fifth Ed. McGraw Hill, New York, NY, pp. 1038-1050.
107. Kakee, A., Takanaga, H., Terasaki, T., Naito, M., Tsuruo, T. and Sugiyama, Y. (2001) Efflux of a suppressive neurotransmitter, GABA, across the blood-brain barrier. J. Neurochem. 79, 110-118.
108. Terasaki, T. and Ohtsuki, S. (2005) Brain-to-blood transporters for endogenous substrates and xenobiotics at the blood-brain barrier: an overview of biology and methodology. NeuroRx 2, 63-72.
109. Palanivelu, R., Brass, L., Edlund, A.F. and Preuss, D. (2003) Pollen tube growth and guidances regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47-59.
110. Ma, H. (2003) Plant reproduction: GABA gradient, guidance and growth. Curr. Biol. 13, R834-R836.
111. Yu, G., Liang, J., He, Z. and Sun, M. (2006) Quantum dot-mediated detection of γ-aminobutyric acid binding sites on the surface of living pollen protoplasts in tobacco. Chem. Biol. 13, 723-731.
112. Okuda, S., Tsutsui, H., Shiina, K., Sprunck, S., Takeuchi, H., Yui, R., Kasahara, R.D., Hamamura, Y., Mizukami, A., Susaki, D., Kawano, N., Sakakibara, T., Namiki, S., Itoh, K., Otsuka, K., Matsuzaki, M., Nozaki, H., Kuroiwa, T., Nakano, A., Kanaoka, M.M., Dresslhaus, T., Sasaki, N. and Higashiyama, T. (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357-361.
113. Okuda, S. and Higashiyama, T. (2010) Pollen tube guidance by attractant molecules: LUREs. Cell Struct. Funct. 35, 45-52.