Skip to main content
SpringerLink
Log in

A cluster of gustducin-expressing cells in the mouse stomach associated with two distinct populations of enteroendocrine cells

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

In the gastrointestinal (GI) tract, a variety of digestive processes are continually adapted to the changing composition of ingested foods, which requires a precise chemosensory monitoring of luminal contents. Gustducin-expressing brush cells scattered throughout the GI mucosa are considered candidate sensory cells for accomplishing this task. In this study, we have investigated a large cluster of gustducin-positive cells which is located exactly at the boundary between the fundic and the oxyntic mucosa of the mouse stomach, at the so-called “limiting ridge”. In close association with the candidate chemosensory cluster, we found two populations of enteroendocrine cells: one population containing the satiety regulating hormone ghrelin, the other population comprising serotonin-secreting enterochromaffin cells. The particular arrangement of gustducin-expressing cells and enteroendocrine cells at the limiting ridge suggests a direct interplay between these cell types with immediate implications, not only for digestive processes in the stomach, but also for parameters controlling the satiety status.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

CV:

Circumvallate papilla

EC cells:

Enterochromaffin cells

ECL cells:

Enterochromaffin-like cells

GI:

Gastrointestinal

GLP-1:

Glucagon-like peptide-1

5-HT:

5-Hydroxytryptamin

References

  • Berthoud HR, Kressel M, Raybould HE, Neuhuber WL (1995) Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo DiI-tracing. Anat Embryol (Berl) 191(3):203–212

    CAS  Google Scholar 

  • Bezencon C, le Coutre J, Damak S (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32(1):41–49

    Article  PubMed  CAS  Google Scholar 

  • Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ (2000) T2Rs function as bitter taste receptors. Cell 100(6):703–711

    Article  PubMed  CAS  Google Scholar 

  • Chou HC, Chien CL, Lu KS (2001) The distribution of PGP9.5, BDNF and NGF in the vallate papilla of adult and developing mice. Anat Embryol (Berl) 204(2):161–169

    Article  CAS  Google Scholar 

  • Covington DK, Briscoe CA, Brown AJ, Jayawickreme CK (2006) The G-protein-coupled receptor 40 family (GPR40–GPR43) and its role in nutrient sensing. Biochem Soc Trans 34(Pt 5):770–773

    PubMed  CAS  Google Scholar 

  • Cummings DE, Foster-Schubert KE, Overduin J (2005) Ghrelin and energy balance: focus on current controversies. Curr Drug Targets 6(2):153–169

    PubMed  CAS  Google Scholar 

  • Debas HT (1987) Gastrin. Clin Invest Med 10(3):222–225

    PubMed  CAS  Google Scholar 

  • Dockray G, Dimaline R, Varro A (2005) Gastrin: old hormone, new functions. Pflugers Arch 449(4):344–355

    Article  PubMed  CAS  Google Scholar 

  • Dumoulin V, Moro F, Barcelo A, Dakka T, Cuber JC (1998) Peptide YY, glucagon-like peptide-1, and neurotensin responses to luminal factors in the isolated vascularly perfused rat ileum. Endocrinology 139(9):3780–3786

    Article  PubMed  CAS  Google Scholar 

  • Dyer J, Vayro S, King TP, Shirazi-Beechey SP (2003) Glucose sensing in the intestinal epithelium. Eur J Biochem 270(16):3377–3388

    Article  PubMed  CAS  Google Scholar 

  • Dyer J, Salmon KS, 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(Pt 1):302–305

    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(15):8981–8986

    Article  PubMed  CAS  Google Scholar 

  • Gershon MD (2004) Review article: serotonin receptors and transporters––roles in normal and abnormal gastrointestinal motility. Aliment Pharmacol Ther 20(Suppl 7):3–14

    Article  PubMed  CAS  Google Scholar 

  • Gershon MD, Tack J (2007) The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology 132(1):397–414

    Article  PubMed  CAS  Google Scholar 

  • He W, Yasumatsu K, Varadarajan V, Yamada A, Lem J, Ninomiya Y, Margolskee RF, Damak S (2004) Umami taste responses are mediated by alpha-transducin and alpha-gustducin. J Neurosci 24(35):7674–7680

    Article  PubMed  CAS  Google Scholar 

  • Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G (2005) Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11(1):90–94

    Article  PubMed  CAS  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(5):405–412

    Article  PubMed  Google Scholar 

  • Höfer D, Puschel B, Drenckhahn D (1996) Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 93(13):6631–6634

    Article  PubMed  Google Scholar 

  • Hunt JN, Stubbs DF (1975) The volume and energy content of meals as determinants of gastric emptying. J Physiol 245(1):209–225

    PubMed  CAS  Google Scholar 

  • Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M (2003) Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422(6928):173–176

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa H, Yoshie S (1996) The taste bud and its innervation in the rat as studied by immunohistochemistry for PGP 9.5. Arch Histol Cytol 59(4):357–367

    PubMed  CAS  Google Scholar 

  • Kellum JM Jr, Jaffe BM (1976) Release of immunoreactive serotonin following acid perfusion of the duodenum. Ann Surg 184(5):633–636

    Article  PubMed  Google Scholar 

  • Khanna MU, Abraham P (1990) Determinants of acid secretion. J Assoc Physicians India 38(Suppl 1):727–730

    PubMed  Google Scholar 

  • Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M (2003) Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 278(28):25481–25489

    Article  PubMed  CAS  Google Scholar 

  • Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99(7):4692–4696

    Article  PubMed  CAS  Google Scholar 

  • Luciano L, Reale E (1992) The “limiting ridge” of the rat stomach. Arch Histol Cytol 55(Suppl):131–138

    PubMed  Google Scholar 

  • Mace OJ, Affleck JA, Patel N, Kellett GL (2007) Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol 582(Pt 1):379–392

    Article  PubMed  CAS  Google Scholar 

  • Matsumura S, Mizushige T, Yoneda T, Iwanaga T, Tsuzuki S, Inoue K, Fushiki T (2007) GPR expression in the rat taste bud relating to fatty acid sensing. Biomed Res 28(1):49–55

    Article  PubMed  CAS  Google Scholar 

  • Mei N (1985) Intestinal chemosensitivity. Physiol Rev 65(2):211–237

    PubMed  CAS  Google Scholar 

  • Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106(3):381–390

    Article  PubMed  CAS  Google Scholar 

  • Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS (2002) An amino-acid taste receptor. Nature 416(6877):199–202

    Article  PubMed  CAS  Google Scholar 

  • Ormsbee HS 3rd, Fondacaro JD (1985) Action of serotonin on the gastrointestinal tract. Proc Soc Exp Biol Med 178(3):333–338

    PubMed  CAS  Google Scholar 

  • Popovic V, Duntas LH (2005) Brain somatic cross-talk: ghrelin, leptin and ultimate challengers of obesity. Nutr Neurosci 8(1):1–5

    Article  PubMed  CAS  Google Scholar 

  • Raybould HE, Zittel TT (1995) Inhibition of gastric motility induced by intestinal glucose in awake rats: role of Na(+)-glucose co-transporter. Neurogastroenterol Motil 7(1):9–14

    PubMed  CAS  Google Scholar 

  • Rindi G, Leiter AB, Kopin AS, Bordi C, Solcia E (2004) The “normal” endocrine cell of the gut: changing concepts and new evidences. Ann N Y Acad Sci 1014:1–12

    Article  PubMed  CAS  Google Scholar 

  • Robert A (1971) Proposed terminology for the anatomy of the rat stomach. Gastroenterology 60(2):344–345

    PubMed  CAS  Google Scholar 

  • Roper SD (2006) Cell communication in taste buds. Cell Mol Life Sci 63(13):1494–1500

    Article  PubMed  CAS  Google Scholar 

  • Rössler P, Kroner C, Freitag J, Noe J, Breer H (1998) Identification of a phospholipase C beta subtype in rat taste cells. Eur J Cell Biol 77(3):253–261

    PubMed  Google Scholar 

  • Rozengurt N, Wu SV, Chen MC, Huang C, Sternini C, Rozengurt E (2006) Colocalization of the alpha-subunit of gustducin with PYY and GLP-1 in L cells of human colon. Am J Physiol Gastrointest Liver Physiol 291(5):G792–G802

    Article  PubMed  CAS  Google Scholar 

  • Salehi A, Flodgren E, Nilsson NE, Jimenez-Feltstrom J, Miyazaki J, Owman C, Olde B (2005) Free fatty acid receptor 1 (FFA(1)R/GPR40) and its involvement in fatty-acid-stimulated insulin secretion. Cell Tissue Res 322(2):207–215

    Article  PubMed  CAS  Google Scholar 

  • Spielman AI (1998) Gustducin and its role in taste. J Dent Res 77(4):539–544

    Article  PubMed  CAS  Google Scholar 

  • Sugita M (2006) Taste perception and coding in the periphery. Cell Mol Life Sci 63(17):2000–2015

    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(5):G1420–G1428

    Article  PubMed  CAS  Google Scholar 

  • Takeda N, Hasegawa S, Morita M, Matsunaga T (1993) Pica in rats is analogous to emesis: an animal model in emesis research. Pharmacol Biochem Behav 45(4):817–821

    Article  PubMed  CAS  Google Scholar 

  • Tassone F, Broglio F, Gianotti L, Arvat E, Ghigo E, Maccario M (2007) Ghrelin and other gastrointestinal peptides involved in the control of food intake. Mini Rev Med Chem 7(1):47–53

    Article  PubMed  CAS  Google Scholar 

  • Thompson RJ, Doran JF, Jackson P, Dhillon AP, Rode J (1983) PGP 9.5––a new marker for vertebrate neurons and neuroendocrine cells. Brain Res 278(1–2):224–228

    Article  PubMed  CAS  Google Scholar 

  • Tomasetto C, Karam SM, Ribieras S, Masson R, Lefebvre O, Staub A, Alexander G, Chenard MP, Rio MC (2000) Identification and characterization of a novel gastric peptide hormone: the motilin-related peptide. Gastroenterology 119(2):395–405

    Article  PubMed  CAS  Google Scholar 

  • Wakisaka S, Miyawaki Y, Youn SH, Kato J, Kurisu K (1996) Protein gene-product 9.5 in developing mouse circumvallate papilla: comparison with neuron-specific enolase and calcitonin gene-related peptide. Anat Embryol (Berl) 194(4):365–372

    CAS  Google Scholar 

  • Wattel W, Geuze JJ (1978) The cells of the rat gastric groove and cardia. An ultrastructural and carbohydrate histochemical study, with special reference to the fibrillovesicular cells. Cell Tissue Res 186(3):375–391

    Article  PubMed  CAS  Google Scholar 

  • Wong GT, Gannon KS, Margolskee RF (1996) Transduction of bitter and sweet taste by gustducin. Nature 381(6585):796–800

    Article  PubMed  CAS  Google Scholar 

  • Wren AM, Bloom SR (2007) Gut hormones and appetite control. Gastroenterology 132(6):2116–2130

    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(4):2392–2397

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto K, Matsunaga S, Matsui M, Takeda N, Yamatodani A (2002) Pica in mice as a new model for the study of emesis. Methods Find Exp Clin Pharmacol 24(3):135–138

    Article  PubMed  CAS  Google Scholar 

  • 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(3):293–301

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Kerstin Bach for excellent technical assistance. This work was supported by the Schwerpunktprogramm Baden-Württemberg.

Author information

Authors and Affiliations

  1. University of Hohenheim, Institute of Physiology, Garbenstrasse 30, 70599, Stuttgart, Germany

    Nicole Hass, Karin Schwarzenbacher & Heinz Breer

Authors
  1. Nicole Hass
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Schwarzenbacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heinz Breer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heinz Breer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hass, N., Schwarzenbacher, K. & Breer, H. A cluster of gustducin-expressing cells in the mouse stomach associated with two distinct populations of enteroendocrine cells. Histochem Cell Biol 128, 457–471 (2007). https://doi.org/10.1007/s00418-007-0325-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-007-0325-3

Keywords

Search

Navigation