Olfactory signaling components and olfactory receptors are expressed in tubule cells of the human kidney

Archives of Biochemistry and Biophysics

Volumn 610, Issue , 2016, Pages 8-15

  Kalbe, Benjamin ^a   Schlimm, Marian ^a   Wojcik, Sebastian ^a   Philippou, Stathis ^b   Maßberg, Désirée ^a   Jansen, Fabian ^a   Scholz, Paul ^a   Luebbert, Hermann ^a   Ubrig, Burkhard ^b   Osterloh, Sabrina ^a   Hatt, Hanns ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b Augusta Kranken Anstalt   (Germany)

Author keywords

Calcium; GPCR; Olfactory receptors; Physiology; Proximal tubule; Signaling

Indexed keywords

4 METHYLVALERIC ACID; 9 (TETRAHYDRO 2 FURYL)ADENINE; ADENYLATE CYCLASE; CALCIUM ION; GUANINE NUCLEOTIDE BINDING PROTEIN; HEXANOIC ACID; ISOVALERIC ACID; PROTEIN HYDROLYSATE; UNCLASSIFIED DRUG; VALERIC ACID DERIVATIVE; CALCIUM; G PROTEIN COUPLED RECEPTOR; LIGAND; N-PENTANOIC ACID; OLFACTORY RECEPTOR; OR51E1 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CALCIUM CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; KIDNEY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; OLFACTORY RECEPTOR; OLFACTORY RECEPTOR11H7; OLFACTORY RECEPTOR51E1; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CELL LINE; CHEMISTRY; CYTOLOGY; CYTOSOL; GENE EXPRESSION REGULATION; KIDNEY TUBULE; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

ADENYLYL CYCLASES; CALCIUM; CELL LINE; CYTOSOL; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY TUBULES; LIGANDS; NEOPLASM PROTEINS; PENTANOIC ACIDS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION;

EID: 84989338094     PISSN: 00039861     EISSN: 10960384     Source Type: Journal    
DOI: 10.1016/j.abb.2016.09.017     Document Type: Article

References (38)

1. [1] Buck, L., Axel, R., A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65 (1991), 175–187, 10.1016/0092-8674(91)90418-X.
2. [2] 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 80 (2003), 2054–2058, 10.1126/science.1080376 299.
3. [3] Maßberg, D., Simon, A., Häussinger, D., Keitel, V., Gisselmann, G., Conrad, H., Hatt, H., Monoterpene (-)-citronellal affects hepatocarcinoma cell signaling via an olfactory receptor. Arch. Biochem. Biophys. 566 (2015), 100–109, 10.1016/j.abb.2014.12.004.
4. [4] Neuhaus, E.M., Zhang, W., Gelis, L., Deng, Y., Noldus, J., Hatt, H., Activation of an olfactory receptor inhibits proliferation of prostate Cancer cells. J. Biol. Chem. 284 (2009), 16218–16225, 10.1074/jbc.M109.012096.
5. [5] Manteniotis, S., Wojcik, S., Brauhoff, P., Möllmann, M., Petersen, L., Göthert, J., Schmiegel, W., Dührsen, U., Gisselmann, G., Hatt, H., Functional characterization of the ectopically expressed olfactory receptor 2AT4 in human myelogenous leukemia. Cell. Death Discov., 2, 2016, 15070, 10.1038/cddiscovery.2015.70.
6. [6] Busse, D., Kudella, P., Grüning, N.-M., Gisselmann, G., Ständer, S., Luger, T., Jacobsen, F., Steinsträßer, L., Paus, R., Gkogkolou, P., Böhm, M., Hatt, H., Benecke, H., A synthetic sandalwood odorant induces wound-healing processes in human keratinocytes via the olfactory receptor OR2AT4. J. Investig. Dermatol. 134 (2014), 2823–2832, 10.1038/jid.2014.273.
7. [7] Braun, T., Voland, P., Kunz, L., Prinz, C., Gratzl, M., Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132 (2007), 1890–1901, 10.1053/j.gastro.2007.02.036.
8. [8] Bakalyar, H.A., Reed, R.R., Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250 (1990), 1403–1406 http://www.ncbi.nlm.nih.gov/pubmed/2255909.
9. [9] Jones, D.T., Reed, R.R., Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244 (1989), 790–795 http://www.ncbi.nlm.nih.gov/pubmed/2499043.
10. [10] Belluscio, L., Gold, G.H., Nemes, A., Axel, R., Mice deficient in G(olf) are anosmic. Neuron 20 (1998), 69–81.
11. [11] Bradley, J., Bönigk, W., Yau, K., Frings, S., Calmodulin permanently associates with rat olfactory CNG channels under native conditions. Nat. Neurosci. 7 (2004), 705–710, 10.1038/nn1266.
12. [12] Dhallan, R., Yau, K., Schrader, K., Reed, R.R., Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347 (1990), 184–187.
13. [13] 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 (2009), 2059–2064, 10.1073/pnas.0812859106.
14. [14] 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. 110 (2013), 4410–4415, 10.1073/pnas.1215927110.
15. [15] Vockley, J., Ensenauer, R., Isovaleric acidemia: new aspects of genetic and phenotypic heterogeneity. Am. J. Med. Genet. C. Semin. Med. Genet. 142C (2006), 95–103, 10.1002/ajmg.c.30089.
16. [16] Flegel, C., Vogel, F., Hofreuter, A., Schreiner, B.S.P., Osthold, S., Veitinger, S., Becker, C., Brockmeyer, N.H., Muschol, M., Wennemuth, G., Altmüller, J., Hatt, H., Gisselmann, G., Characterization of the olfactory receptors expressed in human spermatozoa. Front. Mol. Biosci., 2, 2016, 10.3389/fmolb.2015.00073.
17. [17] Mainland, J.D., Keller, A., Li, Y.R., Zhou, T., Trimmer, C., Snyder, L.L., Moberly, A.H., Adipietro, K.A., Liu, W.L.L., Zhuang, H., Zhan, S., Lee, S.S., Lin, A., Matsunami, H., The missense of smell: functional variability in the human odorant receptor repertoire. Nat. Publ. Gr 17 (2013), 114–120, 10.1038/nn.3598.
18. [18] Fujita, Y., Takahashi, T., Suzuki, A., Kawashima, K., Nara, F., Koishi, R., Deorphanization of Dresden G protein-coupled receptor for an odorant receptor. J. Recept. Signal Transduct. Res. 27 (2007), 323–334, 10.1080/10799890701534180.
19. [19] Audouze, K., Tromelin, A., Le Bon, A.M., Belloir, C., Petersen, R.K., Kristiansen, K., Brunak, S., Taboureau, O., Identification of odorant-receptor interactions by global mapping of the human odorome. PLoS One, 9, 2014, 10.1371/journal.pone.0093037.
20. [20] Menashe, I., Abaffy, T., Hasin, Y., Goshen, S., Yahalom, V., Luetje, C.W., Lancet, D., Genetic elucidation of human hyperosmia to isovaleric acid. PLoS Biol. 5 (2007), 2462–2468, 10.1371/journal.pbio.0050284.
21. [21] Mainland, J.D., Li, Y.R., Zhou, T., Liu, W.L.L., Matsunami, H., Human olfactory receptor responses to odorants. Sci. Data, 2, 2015, 150002, 10.1038/sdata.2015.2.
22. [22] Li, Y.R., Matsunami, H., Materials, S., Press, H., This, B., Signaling, S., Avenue, N.Y., Activation state of the M3 muscarinic acetylcholine receptor modulates mammalian odorant receptor signaling. Sci. Signal, 4, 2011, 10.1126/scisignal.2001230 ra1.
23. [23] Adipietro, K.A., Mainland, J.D., Matsunami, H., Functional evolution of mammalian odorant receptors. PLoS Genet., 8, 2012, e1002821, 10.1371/journal.pgen.1002821.
24. [24] Priori, D., Colombo, M., Clavenzani, P., Jansman, A.J.M., Lallès, J.-P., Trevisi, P., Bosi, P., The olfactory receptor OR51E1 is present along the gastrointestinal tract of pigs, Co-Localizes with enteroendocrine cells and is modulated by intestinal microbiota. PLoS One, 10, 2015, e0129501, 10.1371/journal.pone.0129501.
25. [25] Spehr, J., Gelis, L., Osterloh, M., Oberland, S., Hatt, H., Spehr, M., Neuhaus, E.M., G protein-coupled receptor signaling via Src kinase induces endogenous human transient receptor potential vanilloid type 6 (TRPV6) channel activation. J. Biol. Chem. 286 (2011), 13184–13192, 10.1074/jbc.M110.183525.
26. [26] Leinders-Zufall, T., Greer, C.A., Shepherd, G.M., Zufall, F., Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18 (1998), 5630–5639.
27. [27] Cygnar, K.D., Zhao, H., Phosphodiesterase 1C is dispensable for rapid response termination of olfactory sensory neurons. Nat. Neurosci. 12 (2009), 454–462, 10.1038/nn.2289.
28. [28] Rajkumar, P., Aisenberg, W.H., Acres, O.W., Protzko, R.J., Pluznick, J.L., Identification and characterization of novel renal sensory receptors. PLoS One, 9, 2014, 10.1371/journal.pone.0111053.
29. [29] Bozic, M., de Rooij, J., Parisi, E., Ortega, M.R., Fernandez, E., Valdivielso, J.M., Glutamatergic signaling maintains the epithelial phenotype of proximal tubular cells. J. Am. Soc. Nephrol. 22 (2011), 1099–1111, 10.1681/ASN.2010070701.
30. [30] Plotnikova, O.V., Pugacheva, E.N., Golemis, E.A., Aurora A kinase activity influences calcium signaling in kidney cells. J. Cell. Biol. 193 (2011), 1021–1032, 10.1083/jcb.201012061.
31. [31] Plotnikova, O.V., Pugacheva, E.N., Dunbrack, R.L., Golemis, E.A., Rapid calcium-dependent activation of Aurora-A kinase. Nat. Commun. 1 (2010), 1–8, 10.1038/ncomms1061.
32. [32] van Rooijen, E., Giles, R.H., Voest, E.E., van Rooijen, C., Schulte-Merker, S., van Eeden, F.J., LRRC50, a conserved ciliary protein implicated in polycystic kidney disease. J. Am. Soc. Nephrol. 19 (2008), 1128–1138, 10.1681/ASN.2007080917.
33. [33] Wang, S., Wei, Q., Dong, G., Dong, Z., ERK-mediated suppression of cilia in cisplatin-induced tubular cell apoptosis and acute kidney injury. Biochim. Biophys. Acta Mol. Basis Dis. 1832 (2013), 1582–1590, 10.1016/j.bbadis.2013.05.023.
34. [34] Hartman, T.R., Liu, D., Zilfou, J.T., Robb, V., Morrison, T., Watnick, T., Henske, E.P., The tuberous sclerosis proteins regulate formation of the primary cilium via a rapamycin-insensitive and polycystin 1-independent pathway. Hum. Mol. Genet. 18 (2009), 151–163, 10.1093/hmg/ddn325.
35. [35] Plotnikova, O.V., Pugacheva, E.N., Golemis, E.A., Primary cilia and the cell cycle. Methods Cell. Biol. 94 (2009), 137–160, 10.1016/S0091-679X(08)94007-3.Primary.
36. [36] Delling, M., DeCaen, P.G., Doerner, J.F., Febvay, S., Clapham, D.E., Primary cilia are specialized calcium signalling organelles. Nature 504 (2013), 311–314, 10.1038/nature12833.
37. [37] Raychowdhury, M.K., Ramos, A.J., Zhang, P., McLaughin, M., Dai, X.-Q., Chen, X.-Z., Montalbetti, N., Del Rocío Cantero, M., Ausiello, D.A., Cantiello, H.F., Vasopressin receptor-mediated functional signaling pathway in primary cilia of renal epithelial cells. Am. J. Physiol. Ren. Physiol. 296 (2009), F87–F97, 10.1152/ajprenal.90509.2008.
38. [38] Decaen, P.G., Delling, M., Vien, T.N., Clapham, D.E., Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504 (2013), 315–318, 10.1038/nature13631.