Skip to main content
Log in

Amylase expression in taste receptor cells of rat circumvallate papillae

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The chemical composition of the luminal content is now accepted to have a profound influence on the performance of chemosensory receptors. Gustatory and intestinal chemoreceptors have in common their expression of molecules involved in taste sensing and signal transduction pathways. The recent finding that enterocytes of the duodenal epithelium are capable of expressing luminal pancreatic amylase suggests that taste cells of the gustatory epithelium might, in the same way, express salivary amylase in the oral cavity. Therefore, we investigated amylase expression in rat circumvallate papillae by using analyses involving immunohistochemistry, Western blot, and reverse transcription with the polymerase chain reaction. In addition, we used double-labeling confocal laser microscopy to compare amylase immunolabeling with that of the following markers: protein gene product 9.5 (PGP 9.5) and chromogranin A (CgA) for endocrine cells, α-gustducin and phospholipase C beta 2 (PLCβ2) as taste-signaling molecules, and cystic fibrosis transmembrane regulator (CFTR) and Clara-cell-specific secretory protein of 10-kDa (CC10) as secretory markers. The results showed that amylase was present in some taste bud cells; its immunoreactivity was observed in subsets of cells that expressed CgA, α-gustducin, PLCβ2, CFTR, or CC10. PGP 9.5 immunoreactivity was never colocalized with amylase. The data suggest that amylase-positive cells constitute an additional subset of taste receptor cells also associated with chemoreceptorial and/or secretory molecules, confirming the occurrence of various pathways in taste buds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Azzali G, Bucci G, Gatti R, Orlandini G, Ferrari G (1989) Fine structure of the excretory system of the deep posterior (Ebner’s) salivary glands of the human tongue. Acta Anat 136:257–268

    Article  PubMed  CAS  Google Scholar 

  • Bezencon C, Coutre J le, Damak S (2007) Taste signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32:41–49

    Article  PubMed  CAS  Google Scholar 

  • Brouwer JN, Wiersma A (1980) Stimulus-induced appearance of proteinaceous material in the taste pore. In: Starre H van der (ed) Olfaction and taste, vol VII. IRL, London, pp 179–182

    Google Scholar 

  • Cloutier M, Gingras D, Bendayan M (2006) Internalization and transcytosis of pancreatic enzymes by the intestinal mucosa. J Histochem Cytochem 54:781–794

    Article  PubMed  CAS  Google Scholar 

  • Dockray GJ (2003) Luminal sensing in the gut: an overview. J Physiol Pharmacol 54:9–17

    PubMed  Google Scholar 

  • Dvoryanchikov G, Tomchick SM, Chaudhari N (2007) Biogenic amine synthesis and uptake in rodent taste buds. J Comp Neurol 505:302–313

    Article  PubMed  CAS  Google Scholar 

  • Dyer J, Salmon KSH, Zibrik L, Shirazi-Beechey SP (2005) Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem Soc Trans 33:302–305

    Article  PubMed  CAS  Google Scholar 

  • Field RB, Spielman AI, Hand AR (1989) Purification of lingual amylase from serous glands of rat tongue and characterization of rat lingual amylase and lingual lipase. J Dent Res 68:139–145

    PubMed  CAS  Google Scholar 

  • Field RB, Kruse DH, Redman RS (2001) Immunohistochemical localization and mRNA detection of Rab3D and /or Rab3B in rat von Ebner’s glands, parotid gland, pancreas, and liver. Histochem J 33:71–77

    Article  PubMed  CAS  Google Scholar 

  • Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL (2003) Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100:8981–8986

    Article  PubMed  CAS  Google Scholar 

  • Fischer-Colbrie R, Lassmann H, Hagn C, Winkler H (1985) Immunological studies on the distribution of chromogranin A and B in endocrine and nervous tissue. Neuroscience 16:547–555

    Article  PubMed  CAS  Google Scholar 

  • Giza BK, Scott TR, Sclafani A, Antonucci RF (1991) Polysaccharides as taste stimuli: their effect in the nucleus tractus solitarius of the rat. Brain Res 555:1–9

    Article  PubMed  CAS  Google Scholar 

  • Gurkan S, Bradley RM (1987) Autonomic control of von Ebner’s lingual salivary glands and implication for taste sensation. Brain Res 419:287–293

    Article  PubMed  CAS  Google Scholar 

  • Gurkan S, Bradley RM (1988) Secretion of von Ebner’s glands influence responses from taste buds in rat circumvallate papilla. Chem Senses 13:655–661

    Article  Google Scholar 

  • Hagn C, Schmid KW, Fisher-Colbrie R, Winkler H (1986) Chromogranin A and B in adrenal medulla and endocrine tissues. Lab Invest 55:405–411

    PubMed  CAS  Google Scholar 

  • Hass N, Schwarzenbacher K, Breer H (2007) A cluster of gustducin-expressing cells in the mouse stomach associated with two distinct populations of enteroendocrine cells. Histochem Cell Biol 128:457–471

    Article  PubMed  CAS  Google Scholar 

  • Helle KB (2004) The granin family of uniquely acid proteins of the diffuse neuroendocrine system: comparative and functional aspect. Biol Rev 79:769–794

    Article  PubMed  Google Scholar 

  • Höfer D, Puschel B, Drenckhahn D (1996) Taste receptor-like cells in the rat gut identified by expression of α-gustducin. Proc Natl Acad Sci USA 93:6631–6634

    Article  PubMed  Google Scholar 

  • Höfer D, Drenckhahn D (1996) Cytoskeletal markers allowing discrimination between brush cells and other epithelial cells of the gut including enteroendocrine cells. Histochem Cell Biol 105:405–412

    Article  PubMed  Google Scholar 

  • Höfer D, Drenckhahn D (1998) Identification of the taste cell G-protein, alpha-gustducin, in brush cells of the rat pancreatic duct system. Histochem Cell Biol 110:303–309

    Article  PubMed  Google Scholar 

  • Höfer D, Asan E, Drenckhahn D (1999) Chemosensory perception in gut. New Physiol Sci 14:18–23

    Google Scholar 

  • Huang YJ, Wu YH, Lu KS (2003) Immunoelectron microscopic studies on protein gene product 9.5 and calcitonin gene-related peptide in vallate taste cells and related nerves in the guinea pig. Microsc Res Tech 62:383–395

    Article  PubMed  CAS  Google Scholar 

  • Kinnamon SC, Margolskee RF (1996) Mechanisms of taste transduction. Curr Opin Neurobiol 6:506–513

    Article  PubMed  CAS  Google Scholar 

  • Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, Bernier M, Mosinger B, Margolskee RF, Egan JM (2007) Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104:15069–15074

    Article  PubMed  CAS  Google Scholar 

  • Johnston CJ, Mango GW, Finkelstein JN, Stripp BR (1997) Altered pulmonary response to hyperoxia in Clara cell secretory protein deficient mice. Am J Respir Cell Mol Biol 17:147–155

    PubMed  CAS  Google Scholar 

  • Kataoka S, Yang R, Ishimaru Y, Matsunami H, Sévigny J, Kinnamon JC, Finger TE (2008) The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses 33:243–254

    Article  PubMed  CAS  Google Scholar 

  • Levitzki A, Steer ML (1974) The allosteric activation of mammalian alpha-amylase by chloride. Eur J Biochem 41:171–180

    Article  PubMed  CAS  Google Scholar 

  • Mace OJ, Affleck J, Patel N, Kellett GL (2007) Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol (Lond) 582:379–392

    Article  CAS  Google Scholar 

  • Mango GW, Johnston CJ, Reynolds SD, Finkelstein JN, Plopper CG, Stripp BR (1998) Clara cell secretory protein deficiency increases oxidant stress response in conducting airways. Am J Physiol 275:348–356

    Google Scholar 

  • Margolskee RF, Dyer J, Kokrashvili Z, Salmon KS, Ilegems E, Daly K, Maillet EL, Ninomiya Y, Mosinger B, Shirazi-Beechey SP (2007) T1R3 and gustducin in gut sense sugar to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci USA 104:15075–15080

    Article  PubMed  CAS  Google Scholar 

  • Matsuo R (2000) Role of saliva in the maintenance of taste sensitivity. Crit Rev Oral Biol Med 11:216–229

    Article  PubMed  CAS  Google Scholar 

  • Merigo F, Benati D, Tizzano M, Osculati F, Sbarbati A (2005) Alpha-gustducin immunoreactivity in the airways. Cell Tissue Res 319:211–219

    Article  PubMed  CAS  Google Scholar 

  • Merigo F, Benati D, Di Chio M, Osculati F, Sbarbati A (2007) Secretory cells of the airway express molecules of the chemoreceptive cascade. Cell Tissue Res 327:231–247

    Article  PubMed  CAS  Google Scholar 

  • Merigo F, Benati D, Galiè M, Crescimanno C, Osculati F, Sbarbati A (2008) Immunohistochemical localization of cystic fibrosis transmembrane regulator and Clara cell secretory protein in taste receptor cells of rat circumvallate papillae. Chem Senses 33:231–241

    Article  PubMed  CAS  Google Scholar 

  • Mese H, Matsuo R (2007) Salivary secretion, taste and hyposalivation. J Oral Rehabil 34:711–723

    Article  PubMed  CAS  Google Scholar 

  • Pilewski JM, Frizzell RA (1999) Role of CFTR in airway disease. Physiol Rev 79:S215–S255

    PubMed  CAS  Google Scholar 

  • Quinton PM (1999) Physiological basis of cystic fibrosis: a historical perspective. Physiol Rev 79:S3–S22

    PubMed  CAS  Google Scholar 

  • Ramirez I (1991) Chemoreception for an insoluble non-volatile substance: starch taste. Am J Physiol Regul Integr Comp Physiol 260:192–199

    Google Scholar 

  • Reynolds SD, Reynolds PR, Snyder JC, Whyte F, Paavola KJ, Stripp BR (2007) CCSP regulates cross-talk between secretory cells and both ciliated cells and macrophages of the conducting airway. Am J Physiol Lung Cell Mol Physiol 293:L114–L123

    Article  PubMed  CAS  Google Scholar 

  • Riva A, Loffredo F, Puxeddu R, Testa Riva F (1999) A scanning and transmission electron microscope study of the human minor salivary glands. Arch Oral Biol 44:S27–S31

    Article  PubMed  Google Scholar 

  • Rohr G, Scheele G (1983) Fate of radioactive exocrine pancreatic proteins injected into the blood circulation of the rat. Tissue uptake and transepithelial excretion. Gastroenterology 85:991–1002

    PubMed  CAS  Google Scholar 

  • Roper SD (2006) Cell communication in taste buds. Cell Mol Life Sci 63:1494–1500

    Article  PubMed  CAS  Google Scholar 

  • Roper SD (2007) Signal transduction and information processing in mammalian taste buds. Pflügers Arch 454:759–776

    Article  PubMed  CAS  Google Scholar 

  • Rozengurt N, Wu SV, Chen MC, Huang C, Sternini C, Rozengurt E (2006) Colocalization of the alfa-subunit of gustducin with PYY and GLP-1 in L cells of human colon. Am J Physiol Gastrointest Liver Physiol 291:G792–G802

    Article  PubMed  CAS  Google Scholar 

  • Rozengurt E (2006) Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and alpha-gustducin in the mammalian gut. Am J Physiol Gastrointest Liver Physiol 291:G171–G177

    Article  PubMed  CAS  Google Scholar 

  • Sbarbati A, Crescimanno C, Osculati F (1999) The anatomy and functional role of the circumvallate papilla/von Ebner gland complex. Med Hypotheses 53:40–44

    Article  PubMed  CAS  Google Scholar 

  • Sbarbati A, Merigo F, Benati D, Tizzano M, Bernardi P, Crescimanno C, Osculati F (2004) Identification and characterization of a specific epithelium in the rat larynx. J Comp Neurol 475:188–201

    Article  PubMed  Google Scholar 

  • Sbarbati A, Osculati F (2005) The taste cell-related diffuse chemosensory system. Prog Neurobiol 75:295–307

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Abrams M (1986) Rats show only a weak preference for the artificial sweetener aspartame. Physiol Behav 37:253–256

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Mann S (1987) Carbohydrate taste preferences in rats: glucose, sucrose, maltose, fructose, and Polycose compared. Physiol Behav 40:563–568

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Nissenbaum JW, Vigorito M (1987) Starch preference in rats. Neurosci Biobehav Rev 11:253–262

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A (2004) The sixth taste? Appetite 43:1–3

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Zukerman S, Glendinning JI, Margolskee RF (2007) Fat and carbohydrate preferences in mice: the contribution of α-gustducin and Trpm5 taste signaling proteins. Am J Physiol Regul Integr Comp Physiol 293:1504–1513

    Google Scholar 

  • Spielman AI (1990) Interaction of saliva and taste. J Dent Res 69:838–843

    PubMed  CAS  Google Scholar 

  • Steer ML, Levitzki A (1973) The metal specificity of mammalian-amylase as revealed by enzyme activity and structural probes. FEBS Lett 31:89–92

    Article  PubMed  CAS  Google Scholar 

  • Sternini C (2007) Taste receptors in the gastrointestinal tract. IV. Functional implications of bitter taste receptors in gastrointestinal chemosensing. Am J Physiol Gastrointest Liver Physiol 292:G457–G461

    Article  PubMed  Google Scholar 

  • Sternini C, Anselmi L, Rozengurt E (2008) Enteroendocrine cells: a site of “taste” in gastrointestinal chemosensing. Curr Opin Endocrinol Diabetes Obes 15:73–78

    PubMed  CAS  Google Scholar 

  • Sunderland G, Sclafani A (1988) Taste preference of squirrel monkey and bonnet macaques for polycose, maltose and sucrose. Physiol Behav 43:685–690

    Article  PubMed  CAS  Google Scholar 

  • Sutherland K, Young RL, Cooper NJ, Horowitz M, Blackshaw LA (2007) Phenotypic characterization of taste cells of the mouse small intestine. Am J Physiol Gastrointest Liver Physiol 292:G1420–G1428

    Article  PubMed  CAS  Google Scholar 

  • Tizzano M, Merigo F, Sbarbati A (2006) Evidence of solitary chemosensory cells in a large mammal: the diffuse chemosensory system in Bos taurus airways. J Anat 209:333–337

    Article  PubMed  Google Scholar 

  • Tremblay G, Charest J (1968) Modified starch film method for the histochemical localization of amylase activity. J Histochem Cytochem 16:147–148

    PubMed  CAS  Google Scholar 

  • Vigorito M, Sclafani A (1988) Ontogeny of polycose and sucrose appetite in neonatal rats. Dev Psychobiol 21:457–465

    Article  PubMed  CAS  Google Scholar 

  • Witt M, Miller IJ Jr (1992) Comparative lectin histochemistry on taste buds in foliate, circumvallate and fungiform papillae of the rabbit tongue. Histochemistry 98:173–182

    Article  PubMed  CAS  Google Scholar 

  • Wu SV, Rozengurt N, Yang M, Young SH, Sinnett-Smith J, Rozengurt E (2002) Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA 99:2392–2397

    Article  PubMed  CAS  Google Scholar 

  • Yee CL, Yang R, Bottger B, Finger TE, Kinnamon JC (2001) “Type III” cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol 440:97–108

    Article  PubMed  CAS  Google Scholar 

  • Zancanaro C, Mucignat Caretta C, Merigo F, Cavaggioni A, Osculati F (1999) Alpha-gustducin expression in the vomeronasal organ of the mouse. Eur J Neurosci 11:4473–4475

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

The authors thank Christine Harris for revising the manuscript, and Marzia Di Chio for technical assistance with the confocal microscope.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Flavia Merigo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Merigo, F., Benati, D., Cecchini, M.P. et al. Amylase expression in taste receptor cells of rat circumvallate papillae. Cell Tissue Res 336, 411–421 (2009). https://doi.org/10.1007/s00441-009-0789-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-009-0789-7

Keywords