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The Journal of Neuroscience, April 12, 2006, 26(15):3971-3980; doi:10.1523/JNEUROSCI.0515-06.2006

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Cellular/Molecular
Separate Populations of Receptor Cells and Presynaptic Cells in Mouse Taste Buds

Richard A. DeFazio,^1 * Gennady Dvoryanchikov,^1 * Yutaka Maruyama,¹ Joung Woul Kim,¹ Elizabeth Pereira,¹ Stephen D. Roper,^1,2 and Nirupa Chaudhari^1,2

¹Department of Physiology and Biophysics and ²Program in Neurosciences, University of Miami Miller School of Medicine, Miami, Florida 33136

Correspondence should be addressed to Dr. Nirupa Chaudhari, Department of Physiology and Biophysics, University of Miami Miller School of Medicine, 1600 NW 10th Avenue, Rosenstiel Medical Sciences Building 4040, Miami, FL 33136. Email: nchaudhari{at}miami.edu

Taste buds are aggregates of 50–100 cells, only a fraction of which express genes for taste receptors and intracellular signaling proteins. We combined functional calcium imaging with single-cell molecular profiling to demonstrate the existence of two distinct cell types in mouse taste buds. Calcium imaging revealed that isolated taste cells responded with a transient elevation of cytoplasmic Ca²⁺ to either tastants or depolarization with KCl, but never both. Using single-cell reverse transcription (RT)-PCR, we show that individual taste cells express either phospholipase C 2 (PLC2) (an essential taste transduction effector) or synaptosomal-associated protein 25 (SNAP25) (a key component of calcium-triggered transmitter exocytosis). The two functional classes revealed by calcium imaging mapped onto the two gene expression classes determined by single-cell RT-PCR. Specifically, cells responding to tastants expressed PLC2, whereas cells responding to KCl depolarization expressed SNAP25. We demonstrate this by two methods: first, through sequential calcium imaging and single-cell RT-PCR; second, by performing calcium imaging on taste buds in slices from transgenic mice in which PLC2-expressing taste cells are labeled with green fluorescent protein. To evaluate the significance of the SNAP25-expressing cells, we used RNA amplification from single cells, followed by RT-PCR. We show that SNAP25-positive cells also express typical presynaptic proteins, including a voltage-gated calcium channel (1A), neural cell adhesion molecule, synapsin-II, and the neurotransmitter-synthesizing enzymes glutamic acid decarboxylase and aromatic amino acid decarboxylase. No synaptic markers were detected in PLC2 cells by either amplified RNA profiling or by immunocytochemistry. These data demonstrate the existence of at least two molecularly distinct functional classes of taste cells: receptor cells and synapse-forming cells.

Key words: taste bud; cell type; afferent synapse; PLC2; SNAP25; response

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Received Nov. 12, 2005; revised March 2, 2006; accepted March 2, 2006.

Correspondence should be addressed to Dr. Nirupa Chaudhari, Department of Physiology and Biophysics, University of Miami Miller School of Medicine, 1600 NW 10th Avenue, Rosenstiel Medical Sciences Building 4040, Miami, FL 33136. Email: nchaudhari{at}miami.edu

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