Genome-Wide Analysis of Gene Expression in Primate Taste Buds Reveals Links to Diverse Processes

Peter Hevezi,Mark Zoller,Dalia Kalabat,Min Lu,Bryan D Moyer,Evan White,Bianca Laita,Albert Zlotnik,Hortensia Soto,Na Gao,Cherry Li,Shaoyang Anthony Yeh,Fernando Echeverri,Greg Gibson

doi:10.1371/journal.pone.0006395

Abstract

Efforts to unravel the mechanisms underlying taste sensation (gustation) have largely focused on rodents. Here we present the first comprehensive characterization of gene expression in primate taste buds. Our findings reveal unique new insights into the biology of taste buds. We generated a taste bud gene expression database using laser capture microdissection (LCM) procured fungiform (FG) and circumvallate (CV) taste buds from primates. We also used LCM to collect the top and bottom portions of CV taste buds. Affymetrix genome wide arrays were used to analyze gene expression in all samples. Known taste receptors are preferentially expressed in the top portion of taste buds. Genes associated with the cell cycle and stem cells are preferentially expressed in the bottom portion of taste buds, suggesting that precursor cells are located there. Several chemokines including CXCL14 and CXCL8 are among the highest expressed genes in taste buds, indicating that immune system related processes are active in taste buds. Several genes expressed specifically in endocrine glands including growth hormone releasing hormone and its receptor are also strongly expressed in taste buds, suggesting a link between metabolism and taste. Cell type-specific expression of transcription factors and signaling molecules involved in cell fate, including KIT, reveals the taste bud as an active site of cell regeneration, differentiation, and development. IKBKAP, a gene mutated in familial dysautonomia, a disease that results in loss of taste buds, is expressed in taste cells that communicate with afferent nerve fibers via synaptic transmission. This database highlights the power of LCM coupled with transcriptional profiling to dissect the molecular composition of normal tissues, represents the most comprehensive molecular analysis of primate taste buds to date, and provides a foundation for further studies in diverse aspects of taste biology.

Highlights

Taste is fundamental for the selection of nutritious foods and rejection of poisonous or harmful substances [1]
Taste buds were readily identifiable in all sections used to collect samples and we estimate that the collected taste bud areas contained over 95% taste cells
Since taste cells are specialized neuroepithelial cells, we focused on genes expressed at significantly higher levels in taste buds versus adjacent non-gustatory lingual epithelium

Summary

Introduction

Taste is fundamental for the selection of nutritious foods and rejection of poisonous or harmful substances [1]. Taste plays a significant role in the hedonistic aspect of feeding. Loss of taste negatively impacts well being and is a significant morbidity factor in patients undergoing chemotherapy and radiation therapy [2]. The mouth contains thousands of specialized sensory taste buds. Each taste bud is made up of 50-100 cells classified historically by morphology and histology staining patterns into type I, II and III cells [3]. While less is known about the function(s) of type I cells, type II cells detect sweet, bitter and umami tastants via G protein-coupled receptors and type III detect sour tastants via ion channels [4,5]

Methods

Results

Conclusion