The role of taste perception in the development and persistence of obesity is currently unclear due to conflicting results from psychophysical and other studies. No study to date has assessed whether there is an underlying fundamental difference in the physiology of taste tissue between lean and obese individuals.
We analysed the transcriptomic profile (RNA-seq) of human fungiform taste papillae biopsied from lean (n = 23) and obese (n = 13) Caucasian females (age range 18–55) to identify differences in gene expression.
Obesity status was the major contributor to variance in global gene expression between individuals. A total of 62 genes had significantly different gene expression levels between lean and obese (P < 0.0002), with the specific taste associated genes phospholipase C beta 2 (PLCβ2) and sonic hedge-hog (SHH) having significantly reduced expression in obese group. Genes associated with inflammation and immune response were the top enriched biological pathways differing between the lean and the obese groups. Analysis of a broader gene set having a twofold change in expression (2619 genes) identified three enriched theme groups (sensory perception, cell and synaptic signalling, and immune response). Further, analysis of taste associated genes identified a consistent reduction in the expression of taste-related genes (in particular reduced type II taste cell genes) in the obese compared to the lean group.
The findings show obesity is associated with altered gene expression in tastebuds. Furthermore, the results suggest the tastebud microenvironment is distinctly different between lean and obese persons and, that changes in sensory gene expression contribute to this altered microenvironment. This research provides new evidence of a link between obesity and altered taste and in the future may help design strategies to combat obesity.
Subscribe to Journal
Get full journal access for 1 year
only $41.58 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Hooper L, Abdelhamid A, Moore HJ, Douthwaite W, Skeaff CM, Summerbell CD. Effect of reducing total fat intake on body weight: systematic review and meta-analysis of randomised controlled trials and cohort studies. BMJ. 2012;345:e7666.
Morenga LT, Mallard S, Mann J. Dietary sugars and body weight: systematic review and meta-analyses of randomised controlled trials and cohort studies. BMJ. 2013;346:e7492.
French SJ, Cecil JE. Oral, gastric and intestinal influences on human feeding. Physiol Behav. 2001;74:729–34.
Smeets PAM, Erkner A, de Graaf C. Cephalic phase responses and appetite. Nutr Rev. 2010;68:643–55.
Spetter MS, Mars M, Viergever MA, de Graaf C, Smeets PAM. Taste matters – effects of bypassing oral stimulation on hormone and appetite responses. Physiol Behav. 2014;137:9–17.
Hardikar S, Höchenberger R, Villringer A, Ohla K. Higher sensitivity to sweet and salty taste in obese compared to lean individuals. Appetite. 2017;111:158–65.
Bartoshuk LM, Duffy VB, Hayes JE, Moskowitz HR, Snyder DJ. Psychophysics of sweet and fat perception in obesity: problems, solutions and new perspectives. Philos Trans R Soc Lond B Biol Sci. 2006;361:1137–48.
Ettinger L, Duizer L, Caldwell T. Body fat, sweetness sensitivity, and preference: determining the relationship. Can J Diet Pract Res. 2012;73:45–8.
Overberg J, Hummel T, Krude H, Wiegand S. Differences in taste sensitivity between obese and non-obese children and adolescents. Arch Dis Child. 2012;97:1048–52.
Pepino MY, Finkbeiner S, Beauchamp GK, Mennella JA. Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women. Obesity. 2010;18:959–65.
Stewart JE, Feinle-Bisset C, Golding M, Delahunty C, Clifton PM, Keast RSJ. Oral sensitivity to fatty acids, food consumption and BMI in human subjects. Br J Nutr. 2010;104:145–52.
Stewart JE, Seimon RV, Otto B, Keast RS, Clifton PM, Feinle-Bisset C. Marked differences in gustatory and gastrointestinal sensitivity to oleic acid between lean and obese men. Am J Clin Nutr. 2011;93:703–11.
Frijters JER, Rasmussenconrad EL. Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight. J Gen Psychol. 1982;107:233–47.
Enns MP, Vanitallie TB, Grinker JA. Contributions of age, sex and degree of fatness on preferences and magnitude estimations for sucrose in humans. Physiol Behav. 1979;22:999–1003.
Thompson DA, Moskowitz HR, Campbell RG. Taste and olfaction in human obesity. Physiol Behav. 1977;19:335–7.
Drewnowski A, Kurth CL, Rahaim JE. Taste preferences in human obesity: environmental and familial factors. Am J Clin Nutr. 1991;54:635–41.
Rodin J, Moskowitz HR, Bray GA. Relationship between obesity, weight loss, and taste responsiveness. Physiol Behav. 1976;17:591–7.
Tucker RM, Kaiser KA, Parman MA, George BJ, Allison DB, Mattes RD. Comparisons of fatty acid taste detection thresholds in people who are lean vs. overweight or obese: a systematic review and meta-analysis. PLoS ONE. 2017;12:e0169583.
Berthoud HR, Zheng HY. Modulation of taste responsiveness and food preference by obesity and weight loss. Physiol Behav. 2012;107:527–32.
Pepino MY, Bradley D, Eagon JC, Sullivan S, Abumrad NA, Klein S. Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women. Obesity. 2014;22:E13–E20.
Burge JC, Schaumburg JZ, Choban PS, DiSilvestro RA, Flancbaum L. Changes in Patients’ Taste Acuity after Roux-en-Y Gastric Bypass for Clinically Severe Obesity. J Am Diet Assoc. 1995;95:666–70.
Bray GA, Barry RE, Benfield JR, Castelnuovo-Tedesco P, Rodin J. Intestinal bypass surgery for obesity decreases food intake and taste preferences. Am J Clin Nutr. 1976;29:779–83.
Hart SN, Therneau TM, Zhang Y, Poland GA, Kocher J-P. Calculating sample size estimates for RNA sequencing data. J Comput Biol. 2013;20:970–8.
Shahbake M, Hutchinson I, Laing DG, Jinks AL. Rapid quantitative assessment of fungiform papillae density in the human tongue. Brain Res. 2005;1052:196–201.
Archer NS, Liu D, Shaw J, Hannan G, Duesing K, Keast R. A comparison of collection techniques for gene expression analysis of human oral taste tissue. PLoS ONE. 2016;11:e0152157.
Spielman AI, Pepino MY, Feldman R, Brand JG. Technique to collect fungiform (Taste) papillae from human tongue. J Vis Exp. 2010;42:e2201.
Yan L, Ma C, Wang D, Hu Q, Qin M, Conroy JM, et al. OSAT: a tool for sample-to-batch allocations in genomics experiments. BMC Genome. 2012;13:689.
Andrews S FastQC. A quality control tool for high throughput sequence data. http://wwwbioinformaticsbbsrcacuk/projects/fastqc. 2010.
Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, et al. A survey of best practices for RNA-seq data analysis. Genome Biol. 2016;17:13.
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562–78.
Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105–11.
Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotech. 2013;31:46–53.
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech. 2010;28:511–5.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–9.
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotech. 2011;29:24–6.
Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14:178–92.
Team RC R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/. 2016.
Kassambara A, Mundt F. factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 220.127.116.110. http://www.sthda.com/english/rpkgs/factoextra. 2016.
Wickham H ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. http://ggplot2.org. 2009.
Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2008;4:44–57.
Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1–13.
Ermilov AN, Kumari A, Li L, Joiner AM, Grachtchouk MA, Allen BL, et al. Maintenance of taste organs is strictly dependent on epithelial Hedgehog/GLI signaling. PLoS Genet. 2016;12:e1006442.
Chaudhari N, Roper SD. The cell biology of taste. J Cell Biol. 2010;190:285–96.
Ren W, Lewandowski BC, Watson J, Aihara E, Iwatsuki K, Bachmanov AA, et al. Single Lgr5- or Lgr6-expressing taste stem/progenitor cells generate taste bud cells ex vivo. Proc Natl Acad Sci USA. 2014;111:16401–6.
Rocha VZ, Folco EJ. Inflammatory Concepts of Obesity. International Journal of Inflammation. 2011; Article ID 529061.
Herrera Moro Chao D, Argmann C, Van Eijk M, Boot RG, Ottenhoff R, Van Roomen C, et al. Impact of obesity on taste receptor expression in extra-oral tissues: emphasis on hypothalamus and brainstem. Sci Rep. 2016;6:29094.
Maliphol AB, Garth DJ, Medler KF. Diet-induced obesity reduces the responsiveness of the peripheral taste receptor cells. PLoS ONE. 2013;8:e79403.
Chandrashekar J, Hoon MA, Ryba NJP, Zuker CS. The receptors and cells for mammalian taste. Nature. 2006;444:288–94.
Tizzano M, Grigereit L, Shultz N, Clary MS, Finger TE. Immunohistochemical analysis of human vallate taste buds. Chem Senses. 2015;40:655–60.
Iwatsuki K, Liu H-X, Grónder A, Singer MA, Lane TF, Grosschedl R, et al. Wnt signaling interacts with Shh to regulate taste papilla development. Proc Natl Acad Sci USA. 2007;104:2253–8.
Castillo-Azofeifa D, Losacco JT, Salcedo E, Golden EJ, Finger TE, Barlow LA. Sonic hedgehog from both nerves and epithelium is a key trophic factor for taste bud maintenance. Development. 2017;144:3054–65.
Castillo D, Seidel K, Salcedo E, Ahn C, de Sauvage FJ, Klein OD, et al. Induction of ectopic taste buds by SHH reveals the competency and plasticity of adult lingual epithelium. Development. 2014;141:2993–3002.
Yang H, Cong W-n, Yoon JS, Egan JM. Vismodegib, an antagonist of hedgehog signaling, directly alters taste molecular signaling in taste buds. Cancer Med. 2015;4:245–52.
Sekulic A, Migden MR, Oro AE, Dirix L, Lewis KD, Hainsworth JD, et al. Efficacy and safety of Vismodegib in advanced basal-cell carcinoma. New Engl J Med. 2012;366:2171–9.
Kaufman A, Choo E, Koh A, Dando R. Inflammation arising from obesity reduces taste bud abundance and inhibits renewal. PLoS Biol. 2018;16:e2001959.
Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003;112:293–301.
Dotson CD, Roper SD, Spector AC. PLCβ2-independent behavioral avoidance of prototypical bitter-tasting ligands. Chem Senses. 2005;30:593–600.
Gautier JF, Chen K, Salbe AD, Bandy D, Pratley RE, Heiman M, et al. Differential brain responses to satiation in obese and lean men. Diabetes. 2000;49:838–46.
Mojet J, Heidema J, Christ-Hazelhof E. Taste Perception with age: generic or specific losses in supra-threshold intensities of five taste qualities? Chem Senses. 2003;28:397–413.
Boyce JM, Shone GR. Effects of ageing on smell and taste. Postgrad Med J. 2006;82:239–41.
Dreher J-C, Schmidt PJ, Kohn P, Furman D, Rubinow D, Berman KF. Menstrual cycle phase modulates reward-related neural function in women. Proc Natl Acad Sci USA. 2007;104:2465–70.
Ozdener MH, Brand JG, Spielman AI, Lischka FW, Teeter JH, Breslin PAS, et al. Characterization of human fungiform papillae cells in culture. Chem Senses. 2011;36:601–12.
DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, et al. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006;26:3971–80.
Perea-Martinez I, Nagai T, Chaudhari N. Functional cell types in taste buds have distinct longevities. PLoS ONE. 2013;8:e53399.
Hamamichi R, Asano-Miyoshi M, Emori Y. Taste bud contains both short-lived and long-lived cell populations. Neuroscience. 2006;141:2129–38.
Barlow LA. Progress and renewal in gustation: new insights into taste bud development. Development. 2015;142:3620–9.
This work was supported by the Commonwealth Scientific and Industrial Research Organisation (CSIRO) collaborative start-up grant. Nicholas Archer was supported by a CSIRO OCE Postdoctoral Fellowship.
Conflict of interest
The authors declare that they have no conflict of interest.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Archer, N., Shaw, J., Cochet-Broch, M. et al. Obesity is associated with altered gene expression in human tastebuds. Int J Obes 43, 1475–1484 (2019). https://doi.org/10.1038/s41366-018-0303-y
International Journal of Obesity (2020)
Diabetes & Metabolism Journal (2020)
Correlation of PTC Taste Status with Fungiform Papillae Count and Body Mass Index in Smokers and Non-Smokers of Eastern Province, Saudi Arabia
International Journal of Environmental Research and Public Health (2020)
Chronic exposure to liquid sucrose and dry sucrose diet have differential effects on peripheral taste responses in female rats