Helional induces Ca2+ decrease and serotonin secretion of QGP-1 cells via a PKG-mediated pathway

Journal of Molecular Endocrinology

Volumn 57, Issue 3, 2016, Pages 201-210

  Kalbe, Benjamin ^a   Schlimm, Marian ^a   Mohrhardt, Julia ^b   Scholz, Paul ^a   Jansen, Fabian ^a   Hatt, Hanns ^a   Osterloh, Sabrina ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Calcium signaling; Enterochromaffin cells; Olfactory receptor; Serotonin

Indexed keywords

CALCIUM; CYCLIC GMP DEPENDENT PROTEIN KINASE; FATTY ACID; GLUCOSE; MESSENGER RNA; PANCRELIPASE; PHENOBARBITAL; SEROTONIN; FRAGRANCE; OLFACTORY RECEPTOR;

ARTICLE; COMPARATIVE STUDY; DOSE RESPONSE; ENTEROCHROMAFFIN CELL; HUMAN; IMMUNOCYTOCHEMISTRY; NEUROSECRETORY CELL; OLFACTORY RECEPTOR; PANCREAS CELL; PRIORITY JOURNAL; QGP 1 CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SEROTONIN RELEASE; SIGNAL TRANSDUCTION; SPICE; WESTERN BLOTTING; CALCIUM SIGNALING; CELL CULTURE; CELL LINE; GENE EXPRESSION; GENETICS; METABOLISM; SECRETION (PROCESS);

CALCIUM; CALCIUM SIGNALING; CELL LINE; CELLS, CULTURED; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENTEROCHROMAFFIN CELLS; GENE EXPRESSION; HUMANS; ODORANTS; RECEPTORS, ODORANT; SEROTONIN; SIGNAL TRANSDUCTION;

EID: 84994052049     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-16-0063     Document Type: Article

References (57)

1. Ache BW 2010 Odorant-specific modes of signaling in mammalian olfaction. Chemical Senses 35 533-539. (doi:10.1093/chemse/bjq045)
2. Adipietro KA, Mainland JD & Matsunami H 2012 Functional evolution of mammalian odorant receptors. PLoS Genetics 8 e1002821. (doi:10.1371/journal.pgen.1002821)
3. Bakalyar HA & Reed RR 1990 Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250 1403-1406. (doi:10.1126/science.2255909)
4. Bischoff SC, Barbara G, Buurman W, Ockhuizen T, Schulzke J-D, Serino M, Tilg H, Watson A & Wells JM 2014 Intestinal permeability-a new target for disease prevention and therapy. BMC Gastroenterology 14 189. (doi:10.1186/s12876-014-0189-7)
5. Braun T, Voland P, Kunz L, Prinz C & Gratzl M 2007 Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132 1890-1901. (doi:10.1053/j.gastro.2007.02.036)
6. Busse D, Kudella P, Grüning N-M, Gisselmann G, Ständer S, Luger T, Jacobsen F, Steinsträßer L, Paus R, Gkogkolou P, et al. 2014 A synthetic sandalwood odorant induces wound-healing processes in human keratinocytes via the olfactory receptor OR2AT4. Journal of Investigative Dermatology 134 2823-2832. (doi:10.1038/jid.2014.273)
7. Chin A, Svejda B, Gustafsson BI, Granlund AB, Sandvik AK, Timberlake A, Sumpio BE, Pfragner R, Modlin IM & Kidd M 2012 The role of mechanical forces and adenosine in the regulation of intestinal enterochromaffin cell serotonin secretion. American Journal of Physiology: Gastrointestinal and Liver Physiology 302 G397-G405. (doi:10.1152/ajpgi.00087.2011)
8. D’Ascenzo M, Martinotti G, Azzena GB & Grassi C 2002 cGMP/protein kinase G-dependent inhibition of N-type Ca2+ channels induced by nitric oxide in human neuroblastoma IMR32 cells. Journal of Neuroscience 22 7485-7492.
9. Delay RJ 2002 Two second messengers mediate amino acid responses in olfactory sensory neurons of the salamander, necturus maculosus. Chemical Senses 27 673-680. (doi:10.1093/chemse/27.8.673)
10. Doihara H, Nozawa K, Kojima R, Kawabata-Shoda E, Yokoyama T & Ito H 2009 QGP-1 cells release 5-HT via TRPA1 activation; a model of human enterochromaffin cells. Molecular and Cellular Biochemistry 331 239-245. (doi:10.1007/s11010-009-0165-7)
11. Feldmesser E, Olender T, Khen M, Yanai I, Ophir R & Lancet D 2006 Widespread ectopic expression of olfactory receptor genes. BMC Genomics 7 121. (doi:10.1186/1471-2164-7-121)
12. Flegel C, Manteniotis S, Osthold S, Hatt H & Gisselmann G 2013 Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS ONE 8 e55368. (doi:10.1371/journal.pone.0055368)
13. García-Sáinz JA & Torres-Padilla ME 1999 Modulation of basal intracellular calcium by inverse agonists and phorbol myristate acetate in rat-1 fibroblasts stably expressing α(1d)-adrenoceptors. FEBS Letters 443 277-281. (doi:10.1016/S0014-5793(98)01738-4)
14. Gershon MD 2004 Review article: serotonin receptors and transporters-roles in normal and abnormal gastrointestinal motility. Alimentary Pharmacology & Therapeutics 20 (Supplement 7) 3-14. (doi:10.1111/j.1365-2036.2004.02180.x)
15. Gershon MD 2013 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Current Opinion in Endocrinology, Diabetes Obesity 20 14-21. (doi:10.1097/MED.0b013e32835bc703)
16. Gomez G, Rawson NE, Cowart B, Lowry LD, Pribitkin EA & Restrepo D 2000 Modulation of odor-induced increases in [Ca2+]i by inhibitors of protein kinases A and C in rat and human olfactory receptor neurons. Neuroscience 98 181-189. (doi:10.1016/S0306-4522(00)00112-3)
17. Gomez G, Lischka FW, Haskins ME & Rawson NE 2005 Evidence for multiple calcium response mechanisms in mammalian olfactory receptor neurons. Chemical Senses 30 317-326. (doi:10.1093/chemse/ bji026)
18. Heredia DJ, Gershon MD, Koh SD, Corrigan RD, Okamoto T & Smith TK 2013 Important role of mucosal serotonin in colonic propulsion and peristaltic reflexes: in vitro analyses in mice lacking tryptophan hydroxylase 1. Journal of Physiology 591 5939-5957. (doi:10.1113/ jphysiol.2013.256230)
19. Iguchi H, Hayashi I & Kono A 1990 A somatostatin-secreting cell line established from a human pancreatic islet cell carcinoma (somatostatinoma): release experiment and immunohistochemical study. Cancer Research 50 3691-3693.
20. Jacquier V, Pick H & Vogel H 2006 Characterization of an extended receptive ligand repertoire of the human olfactory receptor OR17-40 comprising structurally related compounds. Journal of Neurochemistry 97 537-544. (doi:10.1111/j.1471-4159.2006.03771.x)
21. John M, Wiedenmann B, Kruhøffer M, Adermann K, Ankorina-Stark I, Schlatter E, Ahnert-Hilger G, Forssmann WG & Kuhn M 1998 Guanylin stimulates regulated secretion from human neuroendocrine pancreatic cells. Gastroenterology 114 791-797. (doi:10.1016/S0016-5085(98)70593-1)
22. Kidd M, Modlin IM, Gustafsson BI, Drozdov I, Hauso O & Pfragner R 2008 Luminal regulation of normal and neoplastic human EC cell serotonin release is mediated by bile salts, amines, tastants, and olfactants. American Journal of Physiology: Gastrointestinal and Liver Physiology 295 G260-G272. (doi:10.1152/ajpgi.00056.2008)
23. Kim M, Cooke HJ, Javed NH, Carey H V, Christofi F & Raybould HE 2001 D-glucose releases 5-hydroxytryptamine from human BON cells as a model of enterochromaffin cells. Gastroenterology 121 1400-1406. (doi:10.1053/gast.2001.29567)
24. Koitabashi N, Aiba T, Hesketh GG, Rowell J, Zhang M, Takimoto E, Tomaselli GF & Kass DA 2010 Cyclic GMP/PKG-dependent inhibition of TRPC6 channel activity and expression negatively regulates cardiomyocyte NFAT activation. Journal of Molecular and Cellular Cardiology 48 713-724. (doi:10.1016/j.yjmcc.2009.11.015)
25. Kwan HY, Huang Y & Yao X 2004 Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. PNAS 101 2625-2630. (doi:10.1073/pnas.0304471101)
26. Lang J, Ushkaryov Y, Grasso A & Wollheim CB 1998 Ca2+-independent insulin exocytosis induced by α-latrotoxin requires latrophilin, a G protein-coupled receptor. EMBO Journal 17 648-657. (doi:10.1093/ emboj/17.3.648)
27. Li Z, Zhang G, Feil R, Han J & Du X 2006 Sequential activation of p38 and ERK pathways by cGMP-dependent protein kinase leading to activation of the platelet integrin α IIbβ3. Blood 107 965-972. (doi:10.1182/blood-2005-03-1308)
28. Li Z, Chalazonitis A, Huang Y-Y, Mann JJ, Margolis KG, Yang QM, Kim DO, Côté F, Mallet J & Gershon MD 2011 Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. Journal of Neuroscience 31 8998-9009. (doi:10.1523/JNEUROSCI.6684-10.2011)
29. Lowe G, Nakamura T & Gold GH 1989 Adenylate cyclase mediates olfactory transduction for a wide variety of odorants. PNAS 86 5641-5645. (doi:10.1073/pnas.86.14.5641)
30. Mainland JD, Li YR, Zhou T, Liu WLL & Matsunami H 2015 Human olfactory receptor responses to odorants. Scientific Data 2 150002. (doi:10.1038/sdata.2015.2)
31. Manocha M & Khan WI 2012 Serotonin and GI disorders: an update on clinical and experimental studies. Clinical and Translational Gastroenterology 3 e13. (doi:10.1038/ctg.2012.8)
32. Manteniotis S, Wojcik S, Brauhoff P, Möllmann M, Petersen L, Göthert J, Schmiegel W, Dührsen U, Gisselmann G & Hatt H 2016 Functional characterization of the ectopically expressed olfactory receptor 2AT4 in human myelogenous leukemia. Cell Death Discovery 2 15070. (doi:10.1038/cddiscovery.2015.70)
33. Maßberg D, Simon A, Häussinger D, Keitel V, Gisselmann G, Conrad H & Hatt H 2015 Monoterpene (-)-citronellal affects hepatocarcinoma cell signaling via an olfactory receptor. Archives of Biochemistry and Biophysics 566 100-109. (doi:10.1016/j.abb.2014.12.004)
34. McRae JF, Mainland JD, Jaeger SR, Adipietro KA, Matsunami H & Newcomb RD 2012 Genetic variation in the odorant receptor OR2J3 is associated with the ability to detect the ‘grassy’ smelling odor, cis-3-hexen-1-ol. Chemical Senses 37 585-593. (doi:10.1093/chemse/ bjs049)
35. Moran GW, Leslie FC, Levison SE & McLaughlin JT 2008 Review: enteroendocrine cells: neglected players in gastrointestinal disorders? Therapeutic Advances in Gastroenterology 1 51-60. (doi:10.1177/17562 83X08093943)
36. Nakamura T & Gold GH 1987 A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325 443-444. (doi:10.1038/325442a0)
37. Neuhaus EM, Mashukova A, Zhang W, Barbour J & Hatt H 2006 A specific heat shock protein enhances the expression of mammalian olfactory receptor proteins. Chemical Senses 31 445-452. (doi:10.1093/chemse/bjj049)
38. Neuhaus EM, Zhang W, Gelis L, Deng Y, Noldus J & Hatt H 2009 Activation of an olfactory receptor inhibits proliferation of prostate cancer cells. Journal of Biological Chemistry 284 16218-16225. (doi:10.1074/jbc.M109.012096)
39. Nilius B 2007 TRP channels in disease. Biochimica et Biophysica Acta 1772 805-812. (doi:10.1016/j.bbadis.2007.02.002)
40. Pavlath GK 2010 A new function for odorant receptors: MOR23 is necessary for normal tissue repair in skeletal muscle. Cell Adhesion and Migration 4 502-506. (doi:10.4161/cam.4.4.12291)
41. Pfragner R, Behmel A, Höger H, Beham A, Ingolic E, Stelzer I, Svejda B, Moser VA, Obenauf AC, Siegl V, et al. 2009 Establishment and characterization of three novel cell lines-P-STS, L-STS, H-STS-derived from a human metastatic midgut carcinoid. Anticancer Research 29 1951-1961.
42. Racké K, Reimann A, Schwörer H & Kilbinger H 1996 Regulation of 5-HT release from enterochromaffin cells. Behavioural Brain Research 73 83-87. (doi:10.1016/0166-4328(96)00075-7)
43. Rawson NE, Gomez G, Cowart B, Brand JG, Lowry LD, Pribitkin EA & Restrepo D 1997 Selectivity and response characteristics of human olfactory neurons. Journal of Neurophysiology 77 1606-1613.
44. Saito H, Chi Q, Zhuang H, Matsunami H & Mainland JD 2009 Odor coding by a mammalian receptor repertoire. Science Signaling 2 ra9. (doi:10.1126/scisignal.2000016)
45. Sanz G, Schlegel C, Pernollet J-C & Briand L 2005 Comparison of odorant specificity of two human olfactory receptors from different phylogenetic classes and evidence for antagonism. Chemical Senses 30 69-80. (doi:10.1093/chemse/bji002)
46. Schmiedeberg K, Shirokova E, Weber HP, Schilling B, Meyerhof W & Krautwurst D 2007 Structural determinants of odorant recognition by the human olfactory receptors OR1A1 and OR1A2. Journal of Structural Biology 159 400-412. (doi:10.1016/j.jsb.2007.04.013)
47. Schulze A, Oehler B, Urban N, Schaefer M & Hill K 2013 Apomorphine is a bimodal modulator of TRPA1 channels. Molecular Pharmacology 83 542-551. (doi:10.1124/mol.112.081976)
48. Siddique ZL, Drozdov I, Floch J, Gustafsson BI, Stunes K, Pfragner R, Kidd M & Modlin IM 2009 KRJ-I and bon cell lines: defining an appropriate enterochromaffin cell neuroendocrine tumor model. Neuroendocrinology 89 458-470. (doi:10.1159/000209330)
49. Spehr M, Wetzel CH, Hatt H & Ache BW 2002 3-Phosphoinositides modulate cyclic nucleotide signaling in olfactory receptor neurons. Neuron 33 731-739. (doi:10.1016/S0896-6273(02)00610-4)
50. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK & Hatt H 2003 Identification of a testicular odorant receptor mediating human sperm chemotaxis. Science 299 2054-2058. (doi:10.1126/science.1080376)
51. Spehr J, Gelis L, Osterloh M, Oberland S, Hatt H, Spehr M & Neuhaus EM 2011 G protein-coupled receptor signaling via Src kinase induces endogenous human transient receptor potential vanilloid type 6 (TRPV6) channel activation. Journal of Biological Chemistry 286 13184-13192. (doi:10.1074/jbc.M110.183525)
52. Taylor MS, Okwuchukwuasanya C, Nickl CK, Tegge W, Brayden JE & Dostmann WRG 2004 Inhibition of cGMP-dependent protein kinase by the cell-permeable peptide DT-2 reveals a novel mechanism of vasoregulation. Molecular Pharmacology 65 1111-1119. (doi:10.1124/ mol.65.5.1111)
53. Veitinger T, Riffell JR, Veitinger S, Nascimento JM, Triller A, Chandsawangbhuwana C, Schwane K, Geerts A, Wunder F, Berns MW, et al. 2011 Chemosensory Ca2+ dynamics correlate with diverse behavioral phenotypes in human sperm. Journal of Biological Chemistry 286 17311-17325. (doi:10.1074/jbc. M110.211524)
54. Wang YG, Wagner MB, Joyner RW & Kumar R 2000 cGMP-dependent protein kinase mediates stimulation of L-type calcium current by cGMP in rabbit atrial cells. Cardiovascular Research 48 310-322. (doi:10.1016/S0008-6363(00)00178-4)
55. Wetzel CH, Oles M, Wellerdieck C, Kuczkowiak M, Gisselmann G & Hatt H 1999 Specificity and sensitivity of a human olfactory receptor functionally expressed in human embryonic kidney 293 cells and Xenopus Laevis oocytes. Journal of Neuroscience 19 7426-7433.
56. 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. PNAS 99 2392-2397. (doi:10.1073/pnas.042617699)
57. Zhuang D 2004 Essential role of protein kinase G and decreased cytoplasmic Ca2+ levels in NO-induced inhibition of rat aortic smooth muscle cell motility. American Journal of Physiology: Heart and Circulatory Physiology 288 H1859-H1866. (doi:10.1152/ajpheart.01031.2004)