Taste and smell GPCRs in the lung: Evidence for a previously unrecognized widespread chemosensory system

Cellular Signalling

Volumn 41, Issue , 2018, Pages 82-88

  An, Steven S ^a   Liggett, Stephen B ^b  

^a The Johns Hopkins University   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Airway; Asthma; Bronchodilator; G protein; Receptor; Smooth muscle

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CALCIUM ION; G PROTEIN COUPLED RECEPTOR; PHOSPHOLIPASE C BETA; POLYSACCHARIDE; SHORT CHAIN FATTY ACID;

AIRWAY SMOOTH MUSCLE CELL; ASTHMA; BONE REMODELING; BRONCHODILATATION; CELL FUNCTION; CHEMOSENSITIVITY; CLINICAL FEATURE; FERMENTATION; HOMEOSTASIS; HUMAN; HYPERPLASIA; HYPERPOLARIZATION; INTESTINE FLORA; LUNG; MEMBRANE MICRODOMAIN; MUSCLE RELAXATION; NONHUMAN; OLFACTORY RECEPTOR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; SMELLING AND TASTE; TACHYPHYLAXIS; TASTE BUD; ANIMAL; ANIMAL MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; ODOR; PHYSIOLOGY; SMOOTH MUSCLE CELL; TASTE;

ANIMALS; ASTHMA; GASTROINTESTINAL MICROBIOME; HUMANS; LUNG; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; MYOCYTES, SMOOTH MUSCLE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SMELL; TASTE;

EID: 85011923274     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2017.02.002     Document Type: Review

References (55)

1. Deshpande, D.A., Wang, W.C., McIlmoyle, E.L., Robinett, K.S., Schillinger, R.M., An, S.S., Sham, J.S., Liggett, S.B., Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat. Med. 16:11 (2010), 1299–1304.
2. Aisenberg, W.H., Huang, J., Zhu, W., Rajkumar, P., Cruz, R., Santhanam, L., Natarajan, N., Yong, H.M., De Santiago, B., Oh, J.J., Yoon, A.R., Panettieri, R.A., Homann, O., Sullivan, J.K., Liggett, S.B., Pluznick, J.L., An, S.S., Defining an olfactory receptor function in airway smooth muscle cells. Sci. Report., 6, 2016, 38231.
3. Camoretti-Mercado, B., Pauer, S.H., Yong, H.M., Smith, D.C., Deshpande, D.A., An, S.S., Liggett, S.B., Pleiotropic effects of bitter taste receptors on [Ca2 +]i mobilization, hyperpolarization, and relaxation of human airway smooth muscle cells. PLoS One, 10(6), 2015, e0131582.
4. Deshpande, D.A., Robinett, K.S., Wang, W.C., Sham, J.S., An, S.S., Liggett, S.B., Bronchodilator activity of bitter tastants in human tissue. Nat. Med. 17:7 (2011), 776–778.
5. Kim, D., Pauer, S.H., Yong, H.M., An, S.S., Liggett, S.B., Beta2-adrenergic receptors chaperone trapped bitter taste receptor 14 to the cell surface as a heterodimer and exert unidirectional desensitization of taste receptor function. J. Biol. Chem. 291:34 (2016), 17616–17628.
6. Robinett, K.S., Deshpande, D.A., Malone, M.M., Liggett, S.B., Agonist-promoted homologous desensitization of human airway smooth muscle bitter taste receptors. Am. J. Respir. Cell Mol. Biol. 45:5 (2011), 1069–1074.
7. Robinett, K.S., Koziol-White, C.J., Akoluk, A., An, S.S., Panettieri, R.A. Jr., Liggett, S.B., Bitter taste receptor function in asthmatic and nonasthmatic human airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 50:4 (2014), 678–683.
8. Adler, E., Hoon, M.A., Mueller, K.L., Chandrashekar, J., Ryba, N.J., Zuker, C.S., A novel family of mammalian taste receptors. Cell 100:6 (2000), 693–702.
9. Chandrashekar, J., Mueller, K.L., Hoon, M.A., Adler, E., Feng, L., Guo, W., Zuker, C.S., Ryba, N.J., T2Rs function as bitter taste receptors. Cell 100:6 (2000), 703–711.
10. An, S.S., Wang, W.C., Koziol-White, C.J., Ahn, K., Lee, D.Y., Kurten, R.C., Panettieri, R.A. Jr., Liggett, S.B., TAS2R activation promotes airway smooth muscle relaxation despite beta(2)-adrenergic receptor tachyphylaxis. Am. J. Phys. Lung Cell. Mol. Phys. 303:4 (2012), L304–L311.
11. Wang, N., Butler, J.P., Ingber, D.E., Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:5111 (1993), 1124–1127.
12. Fabry, B., Maksym, G.N., Butler, J.P., Glogauer, M., Navajas, D., Fredberg, J.J., Scaling the microrheology of living cells. Phys. Rev. Lett., 87(14), 2001, 148102.
13. Hu, S., Chen, J., Fabry, B., Numaguchi, Y., Gouldstone, A., Ingber, D.E., Fredberg, J.J., Butler, J.P., Wang, N., Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Phys. Cell Phys. 285:5 (2003), C1082–C1090.
14. Hubmayr, R.D., Shore, S.A., Fredberg, J.J., Planus, E., Panettieri, R.A. Jr., Moller, W., Heyder, J., Wang, N., Pharmacological activation changes stiffness of cultured human airway smooth muscle cells. Am. J. Phys. 271:5 Pt 1 (1996), C1660–C1668.
15. An, S.S., Laudadio, R.E., Lai, J., Rogers, R.A., Fredberg, J.J., Stiffness changes in cultured airway smooth muscle cells. Am. J. Phys. Cell Phys. 283:3 (2002), C792–C801.
16. An, S.S., Fabry, B., Trepat, X., Wang, N., Fredberg, J.J., Do biophysical properties of the airway smooth muscle in culture predict airway hyperresponsiveness?. Am. J. Respir. Cell Mol. Biol. 35:1 (2006), 55–64.
17. An, S.S., Mitzner, W., Tang, W.Y., Ahn, K., Yoon, A.R., Huang, J., Kilic, O., Yong, H.M., Fahey, J.W., Kumar, S., Biswal, S., Holgate, S.T., Panettieri, R.A. Jr., Solway, J., Liggett, S.B., An inflammation-independent contraction mechanophenotype of airway smooth muscle in asthma. J. Allergy Clin. Immunol. 138:1 (2016), 294–297 e4.
18. Wang, N., Tolic-Norrelykke, I.M., Chen, J., Mijailovich, S.M., Butler, J.P., Fredberg, J.J., Stamenovic, D., Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Phys. Cell Phys. 282:3 (2002), C606–C616.
19. Butler, J.P., Tolic-Norrelykke, I.M., Fabry, B., Fredberg, J.J., Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Phys. Cell Phys. 282:3 (2002), C595–C605.
20. An, S.S., Kim, J., Ahn, K., Trepat, X., Drake, K.J., Kumar, S., Ling, G., Purington, C., Rangasamy, T., Kensler, T.W., Mitzner, W., Fredberg, J.J., Biswal, S., Cell stiffness, contractile stress and the role of extracellular matrix. Biochem. Biophys. Res. Commun. 382:4 (2009), 697–703.
21. Tolic-Norrelykke, I.M., Butler, J.P., Chen, J., Wang, N., Spatial and temporal traction response in human airway smooth muscle cells. Am. J. Phys. Cell Phys. 283:4 (2002), C1254–C1266.
22. Maksym, G.N., Fabry, B., Butler, J.P., Navajas, D., Tschumperlin, D.J., Laporte, J.D., Fredberg, J.J., Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. J. Appl. Physiol. 89:4 (1985), 1619–1632 (2000).
23. Bursac, P., Fabry, B., Trepat, X., Lenormand, G., Butler, J.P., Wang, N., Fredberg, J.J., An, S.S., Cytoskeleton dynamics: fluctuations within the network. Biochem. Biophys. Res. Commun. 355:2 (2007), 324–330.
24. An, S.S., Fabry, B., Mellema, M., Bursac, P., Gerthoffer, W.T., Kayyali, U.S., Gaestel, M., Shore, S.A., Fredberg, J.J., Role of heat shock protein 27 in cytoskeletal remodeling of the airway smooth muscle cell. J. Appl. Physiol. 96:5 (1985), 1701–1713 (2004).
25. Bursac, P., Lenormand, G., Fabry, B., Oliver, M., Weitz, D.A., Viasnoff, V., Butler, J.P., Fredberg, J.J., Cytoskeletal remodelling and slow dynamics in the living cell. Nat. Mater. 4:7 (2005), 557–561.
26. Mehta, D., Gunst, S.J., Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J. Physiol. 519:Pt 3 (1999), 829–840.
27. Seow, C.Y., Pratusevich, V.R., Ford, L.E., Series-to-parallel transition in the filament lattice of airway smooth muscle. J. Appl. Physiol. 89:3 (1985), 869–876 (2000).
28. An, S.S., Bai, T.R., Bates, J.H., Black, J.L., Brown, R.H., Brusasco, V., Chitano, P., Deng, L., Dowell, M., Eidelman, D.H., Fabry, B., Fairbank, N.J., Ford, L.E., Fredberg, J.J., Gerthoffer, W.T., Gilbert, S.H., Gosens, R., Gunst, S.J., Halayko, A.J., Ingram, R.H., Irvin, C.G., James, A.L., Janssen, L.J., King, G.G., Knight, D.A., Lauzon, A.M., Lakser, O.J., Ludwig, M.S., Lutchen, K.R., Maksym, G.N., Martin, J.G., Mauad, T., McParland, B.E., Mijailovich, S.M., Mitchell, H.W., Mitchell, R.W., Mitzner, W., Murphy, T.M., Pare, P.D., Pellegrino, R., Sanderson, M.J., Schellenberg, R.R., Seow, C.Y., Silveira, P.S., Smith, P.G., Solway, J., Stephens, N.L., Sterk, P.J., Stewart, A.G., Tang, D.D., Tepper, R.S., Tran, T., Wang, L., Airway smooth muscle dynamics: a common pathway of airway obstruction in asthma. Eur. Respir. J. 29:5 (2007), 834–860.
29. An, S.S., Robinett, K.S., Deshpande, D.A., Wang, W.C., Liggett, S.B., Reply to: activation of BK channels may not be required for bitter tastant-induced bronchodilation. Nat. Med. 18:5 (2012), 650–651.
30. Zhang, C.H., Lifshitz, L.M., Uy, K.F., Ikebe, M., Fogarty, K.E., ZhuGe, R., The cellular and molecular basis of bitter tastant-induced bronchodilation. PLoS Biol., 11(3), 2013, e1001501.
31. Dickinson, G.D., Ellefsen, K.L., Dawson, S.P., Pearson, J.E., Parker, I., Hindered cytoplasmic diffusion of inositol trisphosphate restricts its cellular range of action. Sci. Signal., 9(453), 2016, ra108.
32. Lechleiter, J., Girard, S., Clapham, D., Peralta, E., Subcellular patterns of calcium release determined by G protein-specific residues of muscarinic receptors. Nature 350:6318 (1991), 505–508.
33. 2-agonist controversy: observations, explanations and relationship to asthma epidemiology. Drug Saf. 11:4 (1994), 259–283.
34. Beasley, R., Pearce, N., Crane, J., Burgess, C., Beta-agonists: what is the evidence that their use increases the risk of asthma morbidity and mortality?. J. Allergy Clin. Immunol. 103 (1999), S18–S30.
35. Lipworth, B.J., Airway subsensitivity with long-acting beta 2-agonists. Is there cause for concern?. Drug Saf. 16 (1997), 295–308.
36. Drazen, J.M., Silverman, E.K., Lee, T.H., Heterogeneity of therapeutic responses in asthma. Br. Med. Bull. 56:4 (2000), 1054–1070.
37. Salpeter, S.R., Wall, A.J., Buckley, N.S., Long-acting beta-agonists with and without inhaled corticosteroids and catastrophic asthma events. Am. J. Med. 123:4 (2010), 322–328.
38. Cheung, D., Timmers, M.C., Zwinderman, A.H., Bel, E.H., Dijkman, J.H., Sterk, P.J., Long-term effects of a long-acting beta-2-adrenoceptor agonist, salmeterol, on airway hyperresponsiveness in patients with mild asthma. N. Engl. J. Med. 327:17 (1992), 1198–1203.
39. Kraan, J., Koeter, G.H., Vandermark, T.W., Sluiter, H.J., Devries, K., Changes in bronchial hyperreactivity induced by 4 weeks of treatment with antiasthmatic drugs in patients with allergic-asthma - a comparison between budesonide and terbutaline. J. Allergy Clin. Immunol. 76:4 (1985), 628–636.
40. McGraw, D.W., Elwing, J.M., Fogel, K.M., Wang, W.C., Glinka, C.B., Mihlbachler, K.A., Rothenberg, M.E., Liggett, S.B., Crosstalk between Gi and Gq/Gs pathways in airway smooth muscle regulates bronchial contractility and relaxation. J. Clin. Invest. 117:5 (2007), 1391–1398.
41. Trian, T., Burgess, J.K., Niimi, K., Moir, L.M., Ge, Q., Berger, P., Liggett, S.B., Black, J.L., Oliver, B.G., B2-agonist induced cAMP is decreased in asthmatic airway smooth muscle due to increased PDE4D. PLoS One, 6(5), 2011, e20000.
42. An, S.S., Mitzner, W., Tang, W.Y., Ahn, K., Yoon, A.R., Huang, J., Kilic, O., Yong, H.M., Fahey, J.W., Kumar, S., Biswal, S., Holgate, S.T., Panettieri, R.A. Jr., Solway, J., Liggett, S.B., An inflammation-independent contraction mechanophenotype of airway smooth muscle in asthma. J. Allergy Clin. Immunol. 138:1 (2016), 294–297.
43. Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., Blanchard, C., Junt, T., Nicod, L.P., Harris, N.L., Marsland, B.J., Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20:2 (2014), 159–166.
44. Kumari, M., Kozyrskyj, A.L., Gut microbial metabolism defines host metabolism: an emerging perspective in obesity and allergic inflammation. Obes. Rev. 18:1 (2017), 18–31.
45. Xanthopoulos, M., Tapia, I.E., Obesity and common respiratory diseases in children. Paediatr. Respir. Rev., 2016 (Epub ahead of print).
46. Kalbe, B., Knobloch, J., Schulz, V.M., Wecker, C., Schlimm, M., Scholz, P., Jansen, F., Stoelben, E., Philippou, S., Hecker, E., Lubbert, H., Koch, A., Hatt, H., Osterloh, S., Olfactory receptors modulate physiological processes in human airway smooth muscle cells. Front. Physiol., 7, 2016, 339.
47. Clark, A.A., Liggett, S.B., Munger, S.D., Extraoral bitter taste receptors as mediators of off-target drug effects. FASEB J. 26:12 (2012), 4827–4831.
48. Lu, P., Zhang, C.H., Lifshitz, L.M., ZhuGe, R., Extraoral bitter taste receptors in health and disease. J. Gen. Physiol., 2017 (Epub ahead of print).
49. Pluznick, J.L., Zou, D.J., Zhang, X., Yan, Q., Rodriguez-Gil, D.J., Eisner, C., Wells, E., Greer, C.A., Wang, T., Firestein, S., Schnermann, J., Caplan, M.J., Functional expression of the olfactory signaling system in the kidney. Proc. Natl. Acad. Sci. U. S. A. 106:6 (2009), 2059–2064.
50. Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J.A., Wetzel, C.H., Zimmer, R.K., Hatt, H., Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299:5615 (2003), 2054–2058.
51. Griffin, C.A., Kafadar, K.A., Pavlath, G.K., MOR23 promotes muscle regeneration and regulates cell adhesion and migration. Dev. Cell 17:5 (2009), 649–661.
52. Pluznick, J.L., Renal and cardiovascular sensory receptors and blood pressure regulation. Am. J. Physiol. Ren. Physiol. 305:4 (2013), F439–F444.
53. Pluznick, J.L., Protzko, R.J., Gevorgyan, H., Peterlin, Z., Sipos, A., Han, J., Brunet, I., Wan, L.X., Rey, F., Wang, T., Firestein, S.J., Yanagisawa, M., Gordon, J.I., Eichmann, A., Peti-Peterdi, J., Caplan, M.J., Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc. Natl. Acad. Sci. U. S. A. 110:11 (2013), 4410–4415.
54. Chang, A.J., Ortega, F.E., Riegler, J., Madison, D.V., Krasnow, M.A., Oxygen regulation of breathing through an olfactory receptor activated by lactate. Nature 527:7577 (2015), 240–244.
55. Clark, A.A., Dotson, C.D., Elson, A.E., Voigt, A., Boehm, U., Meyerhof, W., Steinle, N.I., Munger, S.D., TAS2R bitter taste receptors regulate thyroid function. FASEB J. 29:1 (2015), 164–172.