Dietary experience with glucose and fructose fosters heightened avidity for glucose-containing sugars independent of TRPM5 taste transduction in mice.

Verenice Ascencio Gutierrez, Aracely Simental Ramos, Shushanna Khayoyan, Lindsey A Schier
Author Information
  1. Verenice Ascencio Gutierrez: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
  2. Aracely Simental Ramos: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
  3. Shushanna Khayoyan: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
  4. Lindsey A Schier: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.

Abstract

OBJECTIVE: Experience with metabolically distinct sugars, glucose and fructose, enhances attraction to the orosensory properties of glucose over fructose. To gain insight into which sensory signals are affected, we investigated how this nutritive learning reshapes behavioral responding to various sugars in brief access taste tests in C57BL6/J (B6) mice and assessed whether sugar-exposed mice lacking the TRPM5 channel involved in G-protein coupled taste transduction could acquire these types of preferences for glucose-containing sugars.
METHODS: B6, TRPM5 knockout (KO), and TRPM5 heterozygous (Het) mice were given extensive access to water (sugar naïve) or 0.316, 0.56, and 1.1 M glucose and fructose (sugar-exposed) and then tested, whilst food deprived, for their relative avidities for glucose, fructose, sucrose, maltose, and/or a non-metabolizable glucose analog in a series of taste tests.
RESULTS: sugar-exposed B6 mice licked relatively more for glucose than fructose, driven by an increased avidity for glucose, not an avoidance of fructose, and licked more for maltose, compared to their sugar-naïve counterparts. sugar-exposed B6 mice did not lick with such avidity for a non-metabolizable glucose analog. TRPM5 KO mice took longer to acquire the sugar discrimination than the Het controls, but both groups ultimately licked significantly more for glucose than fructose. Het mice displayed clear preferential licking for sucrose over fructose, while licking comparably high for glucose, sucrose, and maltose. KO mice licked significantly more for maltose than sucrose.
CONCLUSIONS: Collectively, the findings suggest that ingestive experience with glucose and fructose primarily reprograms behavioral responding to a TRPM5-independent orosensory signal generated by glucose-containing sugars.

Keywords

References

  1. Am J Physiol. 1997 Apr;272(4 Pt 2):R1210-8 [PMID: 9140022]
  2. Handb Exp Pharmacol. 2007;(179):287-98 [PMID: 17217064]
  3. PLoS One. 2021 Oct 6;16(10):e0256989 [PMID: 34614010]
  4. Appetite. 2018 Mar 1;122:26-31 [PMID: 28034739]
  5. Nat Neurosci. 2001 May;4(5):492-8 [PMID: 11319557]
  6. Physiol Behav. 1987;40(5):563-8 [PMID: 3671518]
  7. Am J Physiol Regul Integr Comp Physiol. 2017 Apr 1;312(4):R597-R610 [PMID: 28148491]
  8. Am J Physiol Regul Integr Comp Physiol. 2009 Apr;296(4):R855-65 [PMID: 19158407]
  9. Am J Physiol Regul Integr Comp Physiol. 2009 Apr;296(4):R866-76 [PMID: 19091911]
  10. J Neurosci. 2011 Sep 21;31(38):13527-34 [PMID: 21940444]
  11. Am J Physiol Regul Integr Comp Physiol. 2020 May 1;318(5):R901-R916 [PMID: 32160005]
  12. PLoS One. 2017 Dec 27;12(12):e0188784 [PMID: 29281655]
  13. Biochem Biophys Res Commun. 2001 Apr 27;283(1):236-42 [PMID: 11322794]
  14. Nat Genet. 2001 May;28(1):58-63 [PMID: 11326277]
  15. Cell. 2003 Oct 31;115(3):255-66 [PMID: 14636554]
  16. Cell. 2001 Aug 10;106(3):381-90 [PMID: 11509186]
  17. Neurosci Biobehav Rev. 1987 Summer;11(2):187-96 [PMID: 3614785]
  18. Percept Psychophys. 1996 Apr;58(3):327-41 [PMID: 8935894]
  19. Proc Natl Acad Sci U S A. 2016 May 24;113(21):6035-40 [PMID: 27162343]
  20. PLoS One. 2017 Aug 29;12(8):e0183008 [PMID: 28850567]
  21. Am J Physiol Regul Integr Comp Physiol. 2015 Sep;309(5):R552-60 [PMID: 26157055]
  22. Cell Tissue Res. 2011 Aug;345(2):243-52 [PMID: 21739243]
  23. J Neurosci. 2016 Jan 06;36(1):113-24 [PMID: 26740654]
  24. Am J Physiol Regul Integr Comp Physiol. 2009 Apr;296(4):R960-71 [PMID: 19211717]
  25. J Neurosci. 2007 Oct 17;27(42):11242-53 [PMID: 17942718]
  26. Am J Physiol Regul Integr Comp Physiol. 2007 Oct;293(4):R1504-13 [PMID: 17652359]
  27. Chem Senses. 2016 Nov 1;41(9):755-762 [PMID: 27553043]
  28. Am J Physiol Regul Integr Comp Physiol. 2019 May 1;316(5):R448-R462 [PMID: 30624973]
  29. Am J Physiol Regul Integr Comp Physiol. 2012 Jul 15;303(2):R218-35 [PMID: 22621968]
  30. Acta Physiol (Oxf). 2020 Dec;230(4):e13529 [PMID: 32599649]
  31. Cell. 2000 Mar 17;100(6):693-702 [PMID: 10761934]
  32. Cell. 1999 Feb 19;96(4):541-51 [PMID: 10052456]
  33. Am J Physiol Regul Integr Comp Physiol. 2017 Oct 1;313(4):R450-R462 [PMID: 28768658]
  34. Science. 2003 Aug 8;301(5634):850-3 [PMID: 12869700]
  35. Physiol Behav. 2016 Oct 1;164(Pt B):473-477 [PMID: 27126968]
  36. Chem Senses. 2001 Sep;26(7):925-33 [PMID: 11555487]
  37. Ann N Y Acad Sci. 1998 Nov 30;855:170-4 [PMID: 9929601]
  38. Physiol Behav. 2020 Aug 1;222:112945 [PMID: 32417232]
  39. Chem Senses. 2014 Nov;39(9):737-47 [PMID: 25326592]
  40. Proc Natl Acad Sci U S A. 2011 Mar 29;108(13):5431-6 [PMID: 21383163]
  41. Physiol Behav. 1994 Oct;56(4):741-5 [PMID: 7800742]

Grants

  1. R01 DC018562/NIDCD NIH HHS
  2. R25 GM095459/NIGMS NIH HHS
  3. T32 GM144920/NIGMS NIH HHS

MeSH Term

Mice
Animals
Glucose
Fructose
Sugars
Taste
Maltose
Food Preferences
Sucrose
Mice, Knockout
TRPM Cation Channels

Chemicals

Glucose
Fructose
Sugars
Maltose
Sucrose
Trpm5 protein, mouse
TRPM Cation Channels

Word Cloud

Created with Highcharts 10.0.0glucosefructosemicesugarsTRPM5tasteB6sucrosemaltoselickedglucose-containingKOHetsugaravidityorosensorylearningbehavioralrespondingaccesstestssugar-exposedtransductionacquire01non-metabolizableanalogSugar-exposedsignificantlylickingexperienceOBJECTIVE:ExperiencemetabolicallydistinctenhancesattractionpropertiesgaininsightsensorysignalsaffectedinvestigatednutritivereshapesvariousbriefC57BL6/JassessedwhetherlackingchannelinvolvedG-proteincoupledtypespreferencesMETHODS:knockoutheterozygousgivenextensivewaternaïve31656Mtestedwhilstfooddeprivedrelativeaviditiesand/orseriesRESULTS:relativelydrivenincreasedavoidancecomparedsugar-naïvecounterpartslicktooklongerdiscriminationcontrolsgroupsultimatelydisplayedclearpreferentialcomparablyhighCONCLUSIONS:CollectivelyfindingssuggestingestiveprimarilyreprogramsTRPM5-independentsignalgeneratedDietaryfostersheightenedindependentTastechemosensoryprocessingglucoregulationnutrientreward

Similar Articles

Cited By (4)