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Expression of odorant receptor Olfr78 in enteroendocrine cells of the colon

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Abstract

The precise regulation of digestive and other physiological processes in the gastrointestinal tract in accordance with the food ingested requires continuous monitoring of the luminal content by chemosensory cells. With regard to the detection of chemical compounds in the lumen of the gastrointestinal tract, G-protein-coupled receptors (GPCRs) are interesting signaling proteins, since some of them are well known to bind to macronutrients, including sugars, amino acids and lipids. We report that Olfr78, a member of the odorant receptor (OR) class of GPCRs, is expressed in the murine gut. Our results support the concept that Olfr78 is activated by propionate, an important nutrient generated in the colon by microbiota. In situ hybridization and immunohistochemical approaches show that Olfr78 is expressed in the colon but is absent from other gastrointestinal compartments, such as the stomach and small intestine. In the colon, Olfr78 is expressed by a subset of epithelial cells lining the crypts; these cells are endowed with an apical process protruding towards the crypt lumen. The Olfr78-positive cells in the colon co-express the hormonal peptide YY (PYY), a marker for given enteroendocrine cells. The expression of the propionate receptor Olfr78 in epithelial enteroendocrine cells of the colon suggests that Olfr78 is involved in the regulation of hormone secretion from such cells, as evoked by nutritional compounds.

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Abbreviations

5-HT:

Serotonin

β-gal:

β-Galactosidase

CgA:

Chromogranin A

DAPI:

4′,6-Diamidino-2-phenylindole

GFP:

Green fluorescent protein

GLP-1:

Glucagon-like peptide 1

GPCR:

G-protein-coupled receptor

MOE:

Main olfactory epithelium

OMP:

Olfactory marker protein

OR:

Odorant receptor

OSN:

Olfactory sensory neuron

PCR:

Polymerase chain reaction

PYY:

Peptide YY

SCFA:

Short chain fatty acid

PBS:

Phosphate-buffered saline

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Acknowledgments

The authors thank Elisa Mühlberger for excellent technical assistance and Sven Aschenbroich and Marcel Schirrmann for their initial contribution to the study.

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    Authors and Affiliations

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

      Joerg Fleischer, Rosolino Bumbalo, Verena Bautze, Joerg Strotmann & Heinz Breer

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    1. Joerg Fleischer
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    2. Rosolino Bumbalo
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    3. Verena Bautze
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    4. Joerg Strotmann
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    5. Heinz Breer
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    Correspondence to Joerg Fleischer.

    Additional information

    Joerg Fleischer and Rosolino Bumbalo contributed equally to this work.

    This work was supported by the Deutsche Forschungsgemeinschaft (STR 619/5-1 to J. Strotmann and BR 712/25-1 to H. Breer). J. Fleischer was supported by the Humboldt reloaded program of the University of Hohenheim financed by the Bundesministerium für Bildung und Forschung (01PL11003).

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    Suppl. Tab. 1

    Specificity of primary antibodies (PDF 174 kb)

    Suppl. Fig. 1

    Activity of Olfr78-negative glomeruli in the olfactory bulb upon exposure to propionate. a Cross-section through the glomerular layer of the olfactory bulb from an Olfr78/GFP-transgenic mouse exposed to propionate. The image depicts several glomeruli, including an Olfr78-positive glomerulus [visualized with an antibody against β-galactosidase (β-gal) in red] and adjacent Olfr78-negative glomeruli. Counterstained with DAPI (blue). b Same region of the section shown in a. In addition to the Olfr78-positive glomerulus [visualized in yellow/orange because of the overlay of intrinsic GFP fluorescence (green) and immunofluorescence with an antibody against β-gal (red)], c-Fos-expressing juxtaglomerular cells (green) were also found to encircle a few Olfr78-negative glomeruli (see asterisk). Other Olfr78-negative glomeruli are not surrounded by c-Fos-expressing juxtaglomerular cells (hash). c High-magnification image of the glomerulus denoted by asterisk in b. The glomerulus is encircled by several c-Fos-positive juxtaglomerular cells (white arrows), suggesting that the corresponding olfactory sensory neurons are activated by propionate. d Higher magnification of the glomerulus labeled by hash in b. This glomerulus is not surrounded by c-Fos-positive juxtaglomerular cells, indicating that the corresponding olfactory sensory neurons do not respond to propionate. Bars 50 μm. (PDF 207 kb)

    Suppl. Fig. 2

    Expression of Olfr78 in the main olfactory epithelium (MOE). a, b In situ hybridization on a coronal section from a wild-type mouse with an RNA probe specific for Olfr78 labeled a subset of cells in the MOE (arrowheads in b). b Higher magnification of boxed area in a. Bars 200 μm (a), 50 μm (b). (PDF 179 kb)

    Suppl. Fig. 3

    Number of Olfr78-positive cells in distinct colonic regions is similar between male and female mice. Counts of Olfr78-positive cells on colonic sections from female and male mice revealed that the differences in the number of Olfr78-positive cells in the proximal and distal part of the colon were not statistically significant (ns) between female and male mice. In the central colon, a slight but significant difference was seen (P-value = 0.0068). Data from in situ hybridization experiments with sections from three male and three female individuals, with 10 – 16 sections being counted from each animal. A mean of values, the standard deviation and the P-value were calculated. (PDF 103 kb)

    Suppl. Fig. 4

    Olfr78 is absent from the murine stomach. a, c In situ hybridization with an Olfr78-specific antisense RNA probe on sections through the fundus (a) and antrum/corpus (c) region: no expression of Olfr78 was detectable. b, d Higher magnification of boxed areas in a, c. Bars 100 μm (a, c), 50 μm (b, d). (PDF 197 kb)

    Suppl. Fig. 5

    Expression of Olfr78 in the caecum. In situ hybridization with an Olfr78-specific antisense probe on a section through the caecum stained cells (arrows) adjacent to crypts. Bar 50 μm. (PDF 141 kb)

    Suppl. Fig. 6

    Expression of Olfr78 in the MOE. a Immunohistochemistry with a GFP-specific antibody (green) labeled cells on a coronal section through the MOE of a mouse from the transgenic Olfr78/GFP line. b Higher magnification of boxed area in a (arrowheads Olfr78/GFP-positive olfactory sensory neurons [OSNs] endowed with an apical dendrite protruding towards the nasal cavity). Counterstained with DAPI (blue). Bars 200 μm (a), 50 μm (b). (PDF 188 kb)

    Suppl. Fig. 7

    Olfactory marker protein (OMP) is not expressed in cells of the colon mucosa. a In situ hybridization with an OMP-specific antisense probe on coronal sections through the Grueneberg ganglion of a wild-type mouse showing OMP-positive cells. b Higher magnification of boxed area in a. c Incubation of sections through the distal colon with the same OMP antisense probe gives no hybridization signals. d Higher magnification of boxed area in c. Bars 100 μm (a), 20 μm (b, d), 50 μm (c). (PDF 235 kb)

    Suppl. Fig. 8

    Specificity of primary antibody against Chromogranin A (CgA). a Immunohistochemistry with an antibody against CgA (red) stained cells in the colon mucosa. b Omitting the antibody for CgA, no labeled cells were observed. Counterstained with DAPI (blue). Bars 20 μm. (PDF 227 kb)

    Suppl. Fig. 9

    Specificity of primary antibody against serotonin (5-HT). a Immunohistochemical experiments with an antibody against 5-HT (red), labeled cells in the colon. b When the antibody against 5-HT was omitted, no immunostaining was detectable. Counterstained with DAPI (blue). Bars 20 μm. (PDF 167 kb)

    Suppl. Fig. 10

    Specificity of primary antibodies for glucagon-like peptide 1 (GLP-1) and peptide YY (PYY). a, b Immunohistochemistry with an antibody against GLP-1 (a) or PYY (b) revealed immunoreactive cells (red) in the colon (white arrow in a GLP-1). c, d Omission of the antibody for GLP-1 (c) or PYY (d) gave no detectable immunostaining. Counterstained with DAPI (blue). Bars 20 μm. (PDF 224 kb)

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    Fleischer, J., Bumbalo, R., Bautze, V. et al. Expression of odorant receptor Olfr78 in enteroendocrine cells of the colon. Cell Tissue Res 361, 697–710 (2015). https://doi.org/10.1007/s00441-015-2165-0

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