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The Journal of Neuroscience, October 22, 2008, 28(43):10852-10863; doi:10.1523/JNEUROSCI.0894-08.2008

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Cellular/Molecular
Glutamate Transporter-Mediated Glutamate Secretion in the Mammalian Pineal Gland

Mean-Hwan Kim,1 Shunsuke Uehara,2 Akiko Muroyama,2 Bertil Hille,3 Yoshinori Moriyama,2 and Duk-Su Koh1,3

1Department of Physics, Pohang University of Science and Technology, Kyungbuk 790-784, Republic of Korea, 2Department of Biochemistry, Faculty of Pharmaceutical Sciences, Okayama University, Okayama 700-8530, Japan, and 3Department of Physiology and Biophysics, University of Washington, Seattle, Washington 98195-7290

Correspondence should be addressed to Dr. Duk-Su Koh, Department of Physiology and Biophysics, University of Washington, Box 357290, Health Sciences Building, Seattle, WA 98195-7290. Email: koh{at}u.washington.edu

Glutamate transporters are expressed throughout the CNS where their major role is to clear released glutamate from presynaptic terminals. Here, we report a novel function of the transporter in rat pinealocytes. This electrogenic transporter conducted inward current in response to L-glutamate and L- or D-aspartate and depolarized the membrane in patch-clamp experiments. Ca2+ imaging demonstrated that the transporter-mediated depolarization induced a significant Ca2+ influx through voltage-gated Ca2+ channels. The Ca2+ rise finally evoked glutamate exocytosis as detected by carbon-fiber amperometry and by HPLC. In pineal slices with densely packed pinealocytes, glutamate released from the cells effectively activated glutamate transporters in neighboring cells. The Ca2+ signal generated by KCl depolarization or acetylcholine propagated through several cell layers by virtue of the regenerative "glutamate-induced glutamate release." Therefore, we suggest that glutamate transporters mediate synchronized elevation of L-glutamate and thereby efficiently downregulate melatonin secretion via previously identified inhibitory metabotropic glutamate receptors in the pineal gland.

Key words: glutamate transporters; depolarization; calcium; secretion; patch clamp; pineal

Received June 12, 2008; accepted Aug. 29, 2008.

Correspondence should be addressed to Dr. Duk-Su Koh, Department of Physiology and Biophysics, University of Washington, Box 357290, Health Sciences Building, Seattle, WA 98195-7290. Email: koh{at}u.washington.edu






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