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Effect of salivary gland removal on taste preference in mice

  • Sensory Physiology
  • Published:
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A Correction to this article was published on 16 November 2023

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Abstract

To evaluate the effect of decreased salivary secretion on taste preference, we investigated taste preference for five basic tastes by a 48 h two-bottle preference test using a mouse model (desalivated mice) that underwent surgical removal of three major salivary glands: the parotid, submandibular, and sublingual glands. In the desalivated mice, the avoidance behaviors for bitter and salty tastes and the attractive behaviors for sweet and umami tastes were significantly decreased. We confirmed that saliva is necessary to maintain normal taste preference. To estimate the cause of the preference changes, we investigated the effects of salivary gland removal on the expression of taste-related molecules in the taste buds. No apparent changes were observed in the expression levels or patterns of taste-related molecules after salivary gland removal. When the protein concentration and composition in the saliva were compared between the control and desalivated mice, the protein concentration decreased and its composition changed after major salivary gland removal. These results suggest that changes in protein concentration and composition in the saliva may be one of the factors responsible for the changes in taste preferences observed in the desalivated mice.

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References

  1. Canon F, Neiers F, Guichard E (2018) Saliva and flavor perception: Perspectives. J Agric Food Chem 66:7873–7879. https://doi.org/10.1021/acs.jafc.8b01998

    Article  CAS  PubMed  Google Scholar 

  2. Catalanotto FA, Sweeney EA (1972) The effects of surgical desalivation of the rat upon taste acuity. Arch Oral Biol 17:1455–1465. https://doi.org/10.1016/0003-9969(72)90105-7

    Article  CAS  PubMed  Google Scholar 

  3. Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky DA, Hummler E, Ryba NJ, Zuker CS (2010) The cells and peripheral representation of sodium taste in mice. Nature 464:297–301. https://doi.org/10.1038/nature08783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Clapp TR, Stone LM, Margolskee RF, Kinnamon SC (2001) Immunocytochemical evidence for co-expression of type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci 2:6. https://doi.org/10.1186/1471-2202-2-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Dsamou M, Palicki O, Septier C, Chabanet C, Lucchi G, Ducoroy P, Chagnon MC, Morzel M (2012) Salivary protein profiles and sensitivity to the bitter taste of caffeine. Chem Senses 37:87–95. https://doi.org/10.1093/chemse/bjr070

    Article  CAS  PubMed  Google Scholar 

  6. Duca FA, Swartz TD, Covasa M (2014) Effect of diet on preference and intake of sucrose in obese prone and resistant rats. PLoS One 9:e111232. https://doi.org/10.1371/journal.pone.0111232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Foguem C, Seror R, Gosset M (2022) Chemosensory dysfunction in primary sjögren’s syndrome: A topical review. Clin Rheumatol 42:1–14. https://doi.org/10.1007/s10067-022-06359-w

    Article  PubMed  PubMed Central  Google Scholar 

  8. Galili D, Maller O, Brightman VJ (1981) The effects of desalivation by duct ligation or salivary gland extirpation on taste preference in rats. Arch Oral Biol 26:853–858. https://doi.org/10.1016/0003-9969(81)90142-4

    Article  CAS  PubMed  Google Scholar 

  9. Kasahara Y, Narukawa M, Ishimaru Y, Kanda S, Umatani C, Takayama Y, Tominaga M, Oka Y, Kondo K, Kondo T, Takeuchi A, Misaka T, Abe K, Asakura T (2021) TMC4 is a novel chloride channel involved in high-concentration salt taste sensation. J Physiol Sci 71:23. https://doi.org/10.1186/s12576-021-00807-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lamy E, Graça G, da Costa G, Franco C, FC ES, Baptista ES, Coelho AV (2010) Changes in mouse whole saliva soluble proteome induced by tannin-enriched diet. Proteome Sci 8:65.https://doi.org/10.1186/1477-5956-8-65

  11. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  12. Matsuo R, Yamauchi Y, Morimoto T (1997) Role of submandibular and sublingual saliva in maintenance of taste sensitivity recorded in the chorda tympani of rats. J Physiol 498(Pt 3):797–807. https://doi.org/10.1113/jphysiol.1997.sp021903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nanda R, Catalanotto FA (1981) Long-term effects of surgical desalivation upon taste acuity, fluid intake, and taste buds in the rat. J Dent Res 60:69–76. https://doi.org/10.1177/00220345810600011401

    Article  CAS  PubMed  Google Scholar 

  14. Narukawa M, Kitagawa-Iseki K, Oike H, Abe K, Mori T, Hayashi Y (2008) Characterization of umami receptor and coupling G protein in mouse taste cells. NeuroReport 19:1169–1173. https://doi.org/10.1097/WNR.0b013e328308b36c

    Article  CAS  PubMed  Google Scholar 

  15. Narukawa M, Minamisawa E, Hayashi Y (2009) Signalling mechanisms in mouse bitter responsive taste cells. NeuroReport 20:936–940. https://doi.org/10.1097/WNR.0b013e32832c5e80

    Article  CAS  PubMed  Google Scholar 

  16. Narukawa M, Misaka T (2018) Tas2r125 functions as the main receptor for detecting bitterness of tea catechins in the oral cavity of mice. Biochem Biophys Res Commun 503:2301–2305. https://doi.org/10.1016/j.bbrc.2018.06.152

    Article  CAS  PubMed  Google Scholar 

  17. Narukawa M, Mori T, Hayashi Y (2006) Umami changes intracellular Ca2+ levels using intracellular and extracellular sources in mouse taste receptor cells. Biosci Biotechnol Biochem 70:2613–2619. https://doi.org/10.1271/bbb.60159

    Article  CAS  PubMed  Google Scholar 

  18. Narukawa M, Noga C, Ueno Y, Sato T, Misaka T, Watanabe T (2011) Evaluation of the bitterness of green tea catechins by a cell-based assay with the human bitter taste receptor hTAS2R39. Biochem Biophys Res Commun 405:620–625. https://doi.org/10.1016/j.bbrc.2011.01.079

    Article  CAS  PubMed  Google Scholar 

  19. Ohmoto M, Matsumoto I, Misaka T, Abe K (2006) Taste receptor cells express voltage-dependent potassium channels in a cell age-specific manner. Chem Senses 31:739–746. https://doi.org/10.1093/chemse/bjl016

    Article  CAS  PubMed  Google Scholar 

  20. Okada S, Abuyama M, Yamamoto R, Kondo T, Narukawa M, Misaka T (2012) Dietary zinc status reversibly alters both the feeding behaviors of the rats and gene expression patterns in diencephalon. BioFactors 38:203–218. https://doi.org/10.1002/biof.1007

    Article  CAS  PubMed  Google Scholar 

  21. Pedersen A, Sørensen CE, Proctor GB, Carpenter GH (2018) Salivary functions in mastication, taste and textural perception, swallowing and initial digestion. Oral Dis 24:1399–1416. https://doi.org/10.1111/odi.12867

    Article  PubMed  Google Scholar 

  22. Rodrigues L, Costa G, Cordeiro C, Pinheiro C, Amado F, Lamy E (2017) Salivary proteome and glucose levels are related with sweet taste sensitivity in young adults. Food Nutr Res 61:1389208. https://doi.org/10.1080/16546628.2017.1389208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sorensen LB, Moller P, Flint A, Martens M, Raben A (2003) Effect of sensory perception of foods on appetite and food intake: A review of studies on humans. Int J Obes Relat Metab Disord 27:1152–1166. https://doi.org/10.1038/sj.ijo.08023910802391

    Article  CAS  PubMed  Google Scholar 

  24. Stolle T, Grondinger F, Dunkel A, Meng C, Médard G, Kuster B, Hofmann T (2017) Salivary proteome patterns affecting human salt taste sensitivity. J Agric Food Chem 65:9275–9286. https://doi.org/10.1021/acs.jafc.7b03862

    Article  CAS  PubMed  Google Scholar 

  25. Teng B, Wilson CE, Tu YH, Joshi NR, Kinnamon SC, Liman ER (2019) Cellular and neural responses to sour stimuli require the proton channel Otop1. Cur Biol 29:3647-3656.e3645. https://doi.org/10.1016/j.cub.2019.08.077

    Article  CAS  Google Scholar 

  26. Vissink A, Spijkervet FK, Van Nieuw AA (1996) Aging and saliva: A review of the literature. Spec Care Dentist 16:95–103. https://doi.org/10.1111/j.1754-4505.1996.tb00842.x

    Article  CAS  PubMed  Google Scholar 

  27. Yamazaki T, Narukawa M, Mochizuki M, Misaka T, Watanabe T (2013) Activation of the hTAS2R14 human bitter-taste receptor by (-)-epigallocatechin gallate and (-)-epicatechin gallate. Biosci Biotechnol Biochem 77:1981–1983. https://doi.org/10.1271/bbb.130329

    Article  CAS  PubMed  Google Scholar 

  28. Yarmolinsky DA, Zuker CS, Ryba NJ (2009) Common sense about taste: From mammals to insects. Cell 139:234–244. https://doi.org/10.1016/j.cell.2009.10.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zhang J, Jin H, Zhang W, Ding C, O'Keeffe S, Ye M, Zuker CS (2019) Sour sensing from the tongue to the brain. Cell 179:392-402.e315.https://doi.org/10.1016/j.cell.2019.08.031

  30. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: Different receptor cells sharing similar signaling pathways. Cell 112:293–301. https://doi.org/10.1016/s0092-8674(03)00071-0

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Riko Nishida and Yuko Mori (Kyoto Women’s University, Japan) for their support with the animal experiment.

Funding

This work was supported in part by a Grant-in-Aid for Scientific Research (B) 19H02905 and 22H02292 to MN from the Japan Society for the Promotion of Science, by The Salt Science Research Foundation No. 2046 and No. 2242 to MN and by the Japanese Orthodontic Society (JOS) Centennial Research Grant to MN, IW, and TO.

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Authors

Contributions

Masataka Narukawa: Research conception and design, animal experiment, qPCR, tissue staining, SDS‒PAGE, statistical analysis of the data, interpretation of the data, writing of the manuscript. Rina Matsuda: Animal experiment. Ippei Watari and Takashi Ono: interpretation of the data. Takumi Misaka: Research conception and design, interpretation of the data, writing of the manuscript. All authors contributed to and have approved the final manuscript.

Corresponding author

Correspondence to Masataka Narukawa.

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Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

Ethical approval

The experiments were approved by the Ethical Committee for Animal Research of the Kyoto Women’s University. Every attempt was made to reduce animal sufering, discomfort and the total number of animals needed to obtain reliable results.

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The original online version of this article was revised: The originally published article contains an error. The Supplementary figures 1-3 (correspond with Supplementary files 3-5) have missing captions during processing and online publication. These have now been updated.

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Narukawa, M., Matsuda, R., Watari, I. et al. Effect of salivary gland removal on taste preference in mice. Pflugers Arch - Eur J Physiol 476, 111–121 (2024). https://doi.org/10.1007/s00424-023-02873-1

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