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Expression of adiponectin receptor 1 in olfactory mucosa of mice

Cell and Tissue Research volume 334, pages 187–197 (2008)Cite this article

Abstract

AdipoR1 and AdipoR2 are receptors for the adipocyte-derived hormone adiponectin, which is an important regulator of glucose and lipid metabolism, and which has also been implicated in the control of food intake and energy homeostasis. In the present study, we have demonstrated that AdipoR1 is expressed in mature sensory neurons of the olfactory mucosa of mice, in a pattern reminiscent of the olfactory marker protein. AdipoR1 expression levels in the olfactory mucosa have been observed to increase gradually during late embryogenesis until adulthood. No local expression of adiponectin has been detected in nasal tissues, indicating that serum adiponectin is the ligand for AdipoR1 in olfactory sensory neurons. As the serum adiponectin concentration is regulated depending on adipose tissue mass, with a reduction of adiponectin levels being seen in obesity, AdipoR1 function in the olfactory epithelium seems to be directly linked to the nutritional status of the body, suggesting a potential modulatory role for AdipoR1 in the adjustment of the olfactory system to energy balance requirements.

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References

  • Baly C, Aioun J, Badonnel K, Lacroix MC, Durieux D, Schlegel C, Salesse R, Caillol M (2007) Leptin and its receptors are present in the rat olfactory mucosa and modulated by the nutritional status. Brain Res 1129:130–141

    PubMed  Article  CAS  Google Scholar 

  • Breer H, Fleischer J, Strotmann J (2006) The sense of smell: multiple olfactory subsystems. Cell Mol Life Sci 63:1465–1475

    PubMed  Article  CAS  Google Scholar 

  • Caminos JE, Nogueiras R, Gaytán F, Pineda R, González CR, Barreiro ML, Castaño JP, Malagón MM, Pinilla L, Toppari J, Diéguez C, Tena-Sempere M (2008) Novel expression and direct effects of adiponectin in the rat testis. Endocrinology 149:3390–3402

    PubMed  Article  CAS  Google Scholar 

  • Colbert HA, Bargmann CI (1997) Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn Mem 4:179–191

    PubMed  Article  CAS  Google Scholar 

  • Cota D (2008) Role of the endocannabinoid system in energy balance regulation and obesity. Front Horm Res 36:135–145

    PubMed  Article  Google Scholar 

  • Czesnik D, Schild D, Kuduz J, Manzini I (2007) Cannabinoid action in the olfactory epithelium. Proc Natl Acad Sci USA 104:2967–2972

    PubMed  Article  CAS  Google Scholar 

  • Dietze-Schroeder D, Sell H, Uhlig M, Koenen M, Eckel J (2005) Autocrine action of adiponectin on human fat cells prevents the release of insulin resistance-inducing factors. Diabetes 54:2003–2011

    PubMed  Article  CAS  Google Scholar 

  • Dulac C (2000) Sensory coding of pheromone signals in mammals. Curr Opin Neurobiol 10:511–518

    PubMed  Article  CAS  Google Scholar 

  • Fry M, Smith PM, Hoyda TD, Duncan M, Ahima RS, Sharkey KA, Ferguson AV (2006) Area postrema neurons are modulated by the adipocyte hormone adiponectin. J Neurosci 26:9695–9702

    PubMed  Article  CAS  Google Scholar 

  • Fujimoto N, Matsuo N, Sumiyoshi H, Yamaguchi K, Saikawa T, Yoshimatsu H, Yoshioka H (2005) Adiponectin is expressed in the brown adipose tissue and surrounding immature tissues in mouse embryos. Biochim Biophys Acta 1731:1–12

    PubMed  CAS  Google Scholar 

  • Getchell TV, Kwong K, Saunders CP, Stromberg AJ, Getchell ML (2006) Leptin regulates olfactory-mediated behavior in ob/ob mice. Physiol Behav 87:848–856

    PubMed  Article  CAS  Google Scholar 

  • Harrold JA, Halford JC (2006) The hypothalamus and obesity. Recent Patents CNS Drug Discov 1:305–314

    PubMed  Article  CAS  Google Scholar 

  • Kadowaki T, Yamauchi T (2005) Adiponectin and adiponectin receptors. Endocr Rev 26:439–451

    PubMed  Article  CAS  Google Scholar 

  • Kadowaki T, Yamauchi T, Kubota N (2008) The physiological and pathophysiological role of adiponectin and adiponectin receptors in the peripheral tissues and CNS. FEBS Lett 582:74–80

    PubMed  Article  CAS  Google Scholar 

  • Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Yamamoto M, Sugimoto T (2007) Adiponectin and AMP kinase activator stimulate proliferation, differentiation, and mineralization of osteoblastic MC3T3-E1 cells. BMC Cell Biol 8:51

    PubMed  Article  Google Scholar 

  • Katsiougiannis S, Kapsogeorgou EK, Manoussakis MN, Skopouli FN (2006) Salivary gland epithelial cells: a new source of the immunoregulatory hormone adiponectin. Arthritis Rheum 54:2295–2299

    PubMed  Article  CAS  Google Scholar 

  • Kawai K, Sugimoto K, Nakashima K, Miura H, Ninomiya Y (2000) Leptin as a modulator of sweet taste sensitivities in mice. Proc Natl Acad Sci USA 97:11044–11049

    PubMed  Article  CAS  Google Scholar 

  • Lancet D (1986) Vertebrate olfactory reception. Annu Rev Neurosci 9:329–355

    PubMed  Article  CAS  Google Scholar 

  • Larue C, Le Magnen J (1970) Effect of the removal of olfactory bulbs upon hyperphagia and obesity induced in rats by V.M.H. lesion. Physiol Behav 5:509–513

    PubMed  Article  CAS  Google Scholar 

  • Larue CG, Le Magnen J (1972) The olfactory control of meal pattern in rats. Physiol Behav 9:817–821

    PubMed  Article  CAS  Google Scholar 

  • Margolis FL, Verhaagen J, Biffo S, Huang FL, Grillo M (1991) Regulation of gene expression in the olfactory neuroepithelium: a neurogenetic matrix. Prog Brain Res 89:97–122

    PubMed  Article  CAS  Google Scholar 

  • Meguid MM, Gleason JR, Yang ZJ (1993) Olfactory bulbectomy in rats modulates feeding pattern but not total food intake. Physiol Behav 54:471–475

    PubMed  Article  CAS  Google Scholar 

  • Monti-Graziadei GA, Margolis FL, Harding JW, Graziadei PP (1977) Immunocytochemistry of the olfactory marker protein. J Histochem Cytochem 25:1311–1316

    PubMed  CAS  Google Scholar 

  • Ninomiya Y, Shigemura N, Yasumatsu K, Ohta R, Sugimoto K, Nakashima K, Lindemann B (2002) Leptin and sweet taste. Vitam Horm 64:221–248

    PubMed  Article  CAS  Google Scholar 

  • Park KG, Park KS, Kim MJ, Kim HS, Suh YS, Ahn JD, Park KK, Chang YC, Lee IK (2004) Relationship between serum adiponectin and leptin concentrations and body fat distribution. Diabetes Res Clin Pract 63:135–142

    PubMed  Article  CAS  Google Scholar 

  • Redinger RN (2008) The physiology of adiposity. J Ky Med Assoc 106:53–62

    PubMed  Google Scholar 

  • Seoane LM, Al-Massadi O, Caminos JE, Tovar SA, Dieguez C, Casanueva FF (2007) Sensory stimuli directly acting at the central nervous system regulate gastric ghrelin secretion. An ex vivo organ culture study. Endocrinology 148:3998–4006

    PubMed  Article  CAS  Google Scholar 

  • Shinoda Y, Yamaguchi M, Ogata N, Akune T, Kubota N, Yamauchi T, Terauchi Y, Kadowaki T, Takeuchi Y, Fukumoto S, Ikeda T, Hoshi K, Chung UI, Nakamura K, Kawaguchi H (2006) Regulation of bone formation by adiponectin through autocrine/paracrine and endocrine pathways. J Cell Biochem 99:196–208

    PubMed  Article  CAS  Google Scholar 

  • Wang HW, Wysocki CJ, Gold GH (1993) Induction of olfactory receptor sensitivity in mice. Science 260:998–1000

    PubMed  Article  CAS  Google Scholar 

  • Wang T, Hung CC, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251

    PubMed  Article  Google Scholar 

  • Wang Y, Lam KS, Yau MH, Xu A (2008) Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem J 409:623–633

    PubMed  Article  CAS  Google Scholar 

  • Whitehead JP, Richards AA, Hickman IJ, Macdonald GA, Prins JB (2006) Adiponectin—a key adipokine in the metabolic syndrome. Diabetes Obes Metab 8:264–280

    PubMed  Article  CAS  Google Scholar 

  • Wren AM (2008) Gut and hormones and obesity. Front Horm Res 36:165–181

    PubMed  Article  Google Scholar 

  • Yee KK, Wysocki CJ (2001) Odorant exposure increases olfactory sensitivity: olfactory epithelium is implicated. Physiol Behav 72:705–711

    PubMed  Article  CAS  Google Scholar 

  • Zhou Y, Sun X, Jin L, Stringfield T, Lin L, Chen Y (2005) Expression profiles of adiponectin receptors in mouse embryos. Gene Expr Patterns 5:711–715

    PubMed  Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Kerstin Bach and Anne Baumann for their excellent technical assistance.

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Affiliations

  1. Institute of Physiology (230), University of Hohenheim, Garbenstrasse 30, 70599, Stuttgart, Germany

    Nicole Hass, Henriette Haub, Heinz Breer & Karin Schwarzenbacher

  2. Fraunhofer IGB, Nobelstrasse 12, 70569, Stuttgart, Germany

    Rebecca Stevens

Authors
  1. Nicole Hass
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  2. Henriette Haub
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  3. Rebecca Stevens
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  4. Heinz Breer
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  5. Karin Schwarzenbacher
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Corresponding author

Correspondence to Karin Schwarzenbacher.

Additional information

This work was supported by the Forschungsfonds ZEM Tübingen/Hohenheim. Nicole Hass is recipient of a Peter und Traudl Engelhorn Stiftung scholarship.

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Hass, N., Haub, H., Stevens, R. et al. Expression of adiponectin receptor 1 in olfactory mucosa of mice. Cell Tissue Res 334, 187–197 (2008). https://doi.org/10.1007/s00441-008-0677-6

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  • DOI: https://doi.org/10.1007/s00441-008-0677-6

Keywords

  • Adiponectin receptor
  • Olfactory epithelium
  • Olfactory sensory neurons
  • Olfactory marker protein
  • Chemosensation
  • Mouse (C57BL/6J; CD1)