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Review
. 2009 Mar;88(3):212-8.
doi: 10.1177/0022034508330212.

Transient receptor potential (TRP) channels and taste sensation

Y Ishimaru  1 , H Matsunami
Affiliations
Review

Transient receptor potential (TRP) channels and taste sensation

Y Ishimaru et al. J Dent Res. 2009 Mar.

Abstract

Humans have 5 basic taste sensations: sweet, bitter, sour, salty, and umami (taste of 1-amino acids). Among 33 genes related to transient receptor potential (TRP) channels, 3--including TRP-melastatin 5 (TRPM5), polycystic kidney disease-1-like 3 (PKD1L3), and polycystic kidney disease-2-like 1 (PKD2L1)--are specifically and abundantly expressed in taste receptor cells. TRP-melastatin 5 is co-expressed with taste receptors T1Rs and T2Rs, and functions as a common downstream component in sweet, bitter, and umami taste signal transduction. In contrast, polycystic kidney disease-1-like 3 and polycystic kidney disease-2-like 1 are co-expressed in distinct subsets of taste receptor cells not expressing TRP-melastatin 5. In the heterologous expression system, cells expressing both polycystic kidney disease-1-like 3 and polycystic kidney disease-2-like 1 responded to sour stimuli, showing a unique "off-response" property. Genetic ablation of poly-cystic kidney disease-2-like 1-expressing cells resulted in elimination of gustatory nerve response to sour stimuli, indicating that cells expressing polycystic kidney disease-2-like 1 function as sour taste detectors. These results suggest that polycystic kidney disease-1-like 3/polycystic kidney disease-2-like 1 may play a significant role, possibly as taste receptors, in sour taste sensation.

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Figures

Figure 1.
Figure 1.
Signal transduction molecules involved in 5 taste qualities. Sweet, umami, and bitter compounds are detected by 2 distinct families of G-protein-coupled receptors (GPCRs), T1Rs and T2Rs, expressed in type II taste cells. These signals are relayed via the common downstream components, including G-proteins, PLC-b2, IP3R3. and TRPM5, resulting in ATP release. In contrast, sour compounds are potentially detected by PKD1L3/PKD2L1 heteromers expressed in type III taste cells. Type III cells are supposed to transmit the gustatory information by the neurotransmitter, serotonin.
Figure 2.
Figure 2.
Schematic drawing illustrating conformational structures of TRPM5, PKD1L3, and PKD2L1. TRPM5 is predicted to have 6 transmembrane domains and to assemble as tetramers, containing 4 MHRs in the intracellular N-terminal region, and a TRP-motif and a putative coiled-coil domain in the intracellular C-terminal region. Mouse PKD1L3 is predicted to have 11 transmembrane domains, and contains an N-terminal CLD, 29 S/P-rich repeats, a GPS, and a PLAT/LH2 domain. Note that human PKD1L3 does not contain S/P-rich repeats, even in its genomic sequences. PKD2L1 is predicted to have 6 transmembrane domains and contains a putative Ca2+ binding EF hand motif and predicted coiled-coil domain in its C-terminal cytoplasmic tail. MHR, TRPM homology region; CLD, C-type lectin domain; S/P-rich repeats, serine/proline-rich repeats; GPS, G-protein-coupled receptor proteolytic site; PLAT, polycystin-1-lipoxygenase-alpha toxin; LH2, lipoxygenase homology 2; ER, endoplasmic recticulum retention signal; EF hand, calcium-binding domain. Portions of this Figure were modified from Fig.1 in Delmas et al. (2004).
Figure 3.
Figure 3.
Several models of sour taste detection. (A) When expressed in HEK293T cells, the PKD1L3/PKD2L1 channel showed a unique “off-response” property, meaning that this channel is gated open only after the removal of an acid stimulus, although initial acid exposure is essential. It is possible that our heterologous expression system may be lacking additional receptor components that may confer different properties onto the PKD1L3/PKD2L1 channel complex. (B) Other putative sour taste receptors and mechanisms other than taste buds, including somatosensation, may also play some roles in sour transduction.
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