Bitter taste receptors as targets for tocolytics in preterm labor therapy

FASEB Journal

Volumn 31, Issue 9, 2017, Pages 4037-4052

  Zheng, Kaizhi ^a,b   Lu, Ping ^b   Delpapa, Ellen ^b   Bellve, Karl ^b   Deng, Ruitang ^c   Condon, Jennifer C ^d   Fogarty, Kevin ^b   Lifshitz, Lawrence M ^b   Moore Simas, Tiffany A ^b   Shi, Fangxiong ^a   ZhuGe, Ronghua ^b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF RHODE ISLAND   (United States)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chloroquine; G protein coupled receptor; Relaxation; Uterine smooth muscle

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1,10 PHENANTHROLINE; 2 AMINOETHOXYDIPHENYLBORANE; ALPHA GUSTDUCIN; BACTERIUM LIPOPOLYSACCHARIDE; BETA ACTIN; BITTER TASTE RECEPTOR; BITTER TASTE RECEPTOR 102; BITTER TASTE RECEPTOR 103; CALCIUM; CHLOROQUINE; DENATONIUM BENZOATE; G PROTEIN COUPLED RECEPTOR; GALLEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INDOMETACIN; INOSITOL TRISPHOSPHATE RECEPTOR; MAGNESIUM SULFATE; MESSENGER RNA; MIFEPRISTONE; NIFEDIPINE; OXYTOCIN; PERTUSSIS TOXIN; PHOSPHOLIPASE C BETA2; PROGESTERONE RECEPTOR; PROTEIN INHIBITOR; RECEPTOR; SALBUTAMOL; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; 1,10-PHENANTHROLINE; GUSTDUCIN; PHENANTHROLINE DERIVATIVE; QUATERNARY AMMONIUM DERIVATIVE; TRANSDUCIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LABOR MANAGEMENT; MOUSE; MYOMETRIUM; NONHUMAN; PREMATURE LABOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; UTERINE SMOOTH MUSCLE CELL; UTERUS CONTRACTILITY; UTERUS CONTRACTION; UTERUS RELAXATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUSCLE CONTRACTION; OBSTETRIC LABOR, PREMATURE; PHYSIOLOGY; PREGNANCY; SMOOTH MUSCLE;

ALBUTEROL; ANIMALS; CALCIUM; CHLOROQUINE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MAGNESIUM SULFATE; MICE; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOMETRIUM; OBSTETRIC LABOR, PREMATURE; OXYTOCIN; PHENANTHROLINES; PREGNANCY; QUATERNARY AMMONIUM COMPOUNDS; RECEPTORS, G-PROTEIN-COUPLED; TRANSDUCIN;

EID: 85028922928     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201601323RR     Document Type: Article

References (61)

1. Blencowe, H., Cousens, S., Chou, D., Oestergaard, M., Say, L., Moller, A. B., Kinney, M., and Lawn, J.; Born Too Soon Preterm Birth Action Group. (2013) Born too soon: the global epidemiology of 15 million preterm births. Reprod. Health 10(Suppl 1), S2
2. Erdei, C., and Dammann, O. (2014) The perfect storm: preterm birth, neurodevelopmental mechanisms, and autism causation. Perspect. Biol. Med. 57, 470–481
3. Ortinau, C., and Neil, J. (2015) The neuroanatomy of prematurity: normal brain development and the impact of preterm birth. Clin. Anat. 28, 168–183
4. Simmons, L. E., Rubens, C. E., Darmstadt, G. L., and Gravett, M. G. (2010) Preventing preterm birth and neonatal mortality: exploring the epidemiology, causes, and interventions. Semin. Perinatol. 34, 408–415
5. Romero, R., Dey, S. K., and Fisher, S. J. (2014) Preterm labor: one syndrome, many causes. Science 345, 760–765
6. Swaggart, K. A., Pavlicev, M., and Muglia, L. J. (2015) Genomics of preterm birth. Cold Spring Harb. Perspect. Med. 5, a023127
7. Illanes, S. E., Pérez-Sepúlveda, A., Rice, G. E., and Mitchell, M. D. (2014) Preterm labour: association between labour physiology, tocolysis and prevention. Expert Opin. Investig. Drugs 23, 759–771
8. Smith, R. (2007) Parturition. N. Engl. J. Med. 356, 271–283
9. Van Vliet, E. O., Boormans, E. M., de Lange, T. S., Mol, B. W., and Oudijk, M. A. (2014) Preterm labor: current pharmacotherapy options for tocolysis. Expert Opin. Pharmacother. 15, 787–797
10. Mitchell, B. F., Aguilar, H. N., Mosher, A., Wood, S., and Slater, D. M. (2013) The uterine myocyte as a target for prevention of preterm birth. Facts Views Vis. Obgyn 5, 72–81
11. Deshpande, D. A., Wang, W. C., McIlmoyle, E. L., Robinett, K. S., Schillinger, R. M., An, S. S., Sham, J. S., and Liggett, S. B. (2010) Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat. Med. 16, 1299–1304
12. Zhang, C.-H., Lifshitz, L. M., Uy, K. F., Ikebe, M., Fogarty, K. E., and ZhuGe, R. (2013) The cellular and molecular basis of bitter tastant–induced bronchodilation. PLoS Biol. 11, e1001501.
13. Erratum: Zhang, C.-H., Lifshitz, L. M., Uy, K. F., Ikebe, M., Fogarty, K. E., and ZhuGe, R. (2013) The cellular and molecular basis of bitter tastant–induced bronchodilation. PLoS Biol. 2013;11(3)
14. Chandrashekar, J., Mueller, K. L., Hoon, M. A., Adler, E., Feng, L., Guo, W., Zuker, C. S., and Ryba, N. J. (2000) T2Rs function as bitter taste receptors. Cell 100, 703–711
15. Wong, G. T., Gannon, K. S., and Margolskee, R. F. (1996) Transduction of bitter and sweet taste by gustducin. Nature 381, 796–800
16. Chaudhari, N., and Roper, S. D. (2010) The cell biology of taste. J. Cell Biol. 190, 285–296;
17. erratum Chaudhari, N., and Roper, S. D. (2010) The cell biology of taste. J. Cell Biol. 191, 429
18. Behrens, M., and Meyerhof, W. (2011) Gustatory and extragustatory functions of mammalian taste receptors. Physiol. Behav. 105, 4–13
19. 2+ sparks act as potent regulators of excitation–contraction coupling in airway smooth muscle. J. Biol. Chem. 285, 2203–2210
20. 2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J. Gen. Physiol. 113, 215–228
21. Rozengurt, N., Wu, S. V., Chen, M. C., Huang, C., Sternini, C., and Rozengurt, E. (2006) Colocalization of the alpha-subunit of gustducin with PYY and GLP-1 in L cells of human colon. Am. J. Physiol. Gastro-intest. Liver Physiol. 291, G792–G802
22. Janssen, S., Laermans, J., Verhulst, P. J., Thijs, T., Tack, J., and Depoortere, I. (2011) Bitter taste receptors and α-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. Proc. Natl. Acad. Sci. USA 108, 2094–2099
23. 3 responses to bitter denatonium. Nat. Neurosci. 2, 1055–1062
24. Mestdagh, P., Feys, T., Bernard, N., Guenther, S., Chen, C., Speleman, F., and Vandesompele, J. (2008) High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA. Nucleic Acids Res. 36, e143
25. Zhang, Y., Hoon, M. A., Chandrashekar, J., Mueller, K. L., Cook, B., Wu, D., Zuker, C. S., and Ryba, N. J. (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293–301
26. Aguilar, H. N., and Mitchell, B. F. (2010) Physiological pathways and molecular mechanisms regulating uterine contractility. Hum. Reprod. Update 16, 725–744
27. Sanborn, B. M., Ku, C. Y., Shlykov, S., and Babich, L. (2005) Molecular signaling through G-protein-coupled receptors and the control of intracellular calcium in myometrium. J. Soc. Gynecol. Investig. 12, 479–487
28. Committee on Understanding Premature Birth and Assuring Healthy Outcomes. (2007) Diagnosis and treatment of preterm labor. In Preterm Birth: Causes, Consequences, and Prevention (Behrman, R. E., and Butler, A. S., eds.), pp. 259–310, National Academies Press, Washington, DC
29. 2+ channels. J. Pharmacol. Exp. Ther. 326, 871–878
30. Orr, A. W., Pallero, M. A., and Murphy-Ullrich, J. E. (2002) Thrombospondin stimulates focal adhesion disassembly through Gi- and phosphoinositide 3-kinase-dependent ERK activation. J. Biol. Chem. 277, 20453–20460
31. Meyerhof, W., Batram, C., Kuhn, C., Brockhoff, A., Chudoba, E., Bufe, B., Appendino, G., and Behrens, M. (2010) The molecular receptive ranges of human TAS2R bitter taste receptors. Chem. Senses 35, 157–170
32. Kaga, N., Katsuki, Y., Obata, M., and Shibutani, Y. (1996) Repeated administration of low-dose lipopolysaccharide induces preterm delivery in mice: a model for human preterm parturition and for assessment of the therapeutic ability of drugs against preterm delivery. Am. J. Obstet. Gynecol. 174, 754–759
33. Elovitz, M. A., and Mrinalini, C. (2004) Animal models of preterm birth. Trends Endocrinol. Metab. 15, 479–487
34. Ehn, N. L., Cooper, M. E., Orr, K., Shi, M., Johnson, M. K., Caprau, D., Dagle, J., Steffen, K., Johnson, K., Marazita, M. L., Merrill, D., and Murray, J. C. (2007) Evaluation of fetal and maternal genetic variation in the progesterone receptor gene for contributions to preterm birth. Pediatr. Res. 62, 630–635
35. Romero, R., Yeo, L., Chaemsaithong, P., Chaiworapongsa, T., and Hassan, S. S. (2014) Progesterone to prevent spontaneous preterm birth. Semin. Fetal Neonatal Med. 19, 15–26
36. Stamatelou, F., Deligeoroglou, E., Farmakides, G., and Creatsas, G. (2009) Abnormal progesterone and corticotropin releasing hormone levels are associated with preterm labour. Ann. Acad. Med. Singapore 38, 1011–1016
37. Darne, J., McGarrigle, H. H., and Lachelin, G. C. (1987) Increased saliva oestriol to progesterone ratio before preterm delivery: a possible predictor for preterm labor? Br. Med. J. (Clin. Res. Ed.) 294, 270–272
38. Lachelin, G. C., McGarrigle, H. H., Seed, P. T., Briley, A., Shennan, A. H., and Poston, L. (2009) Low saliva progesterone concentrations are associated with spontaneous early preterm labour (before 34 weeks of gestation) in women at increased risk of preterm delivery. BJOG 116, 1515–1519
39. Priya, B., Mustafa, M. D., Guleria, K., Vaid, N. B., Banerjee, B. D., and Ahmed, R. S. (2013) Salivary progesterone as a biochemical marker to predict early preterm birth in asymptomatic high-risk women. BJOG 120, 1003–1011
40. Maged, A. M., Mohesen, M., Elhalwagy, A., and Abdelhafiz, A. (2015) Salivary progesterone and cervical length measurement as predictors of spontaneous preterm birth. J. Matern. Fetal Neonatal Med. 28, 1147–1151
41. Manuck, T. A., Lai, Y., Meis, P. J., Dombrowski, M. P., Sibai, B., Spong, C. Y., Rouse, D. J., Durnwald, C. P., Caritis, S. N., Wapner, R. J., Mercer, B. M., and Ramin, S. M. (2011) Progesterone receptor polymorphisms and clinical response to 17-alpha-hydroxyprogesterone caproate. Am. J. Obstet. Gynecol. 205, 135.e131–135.e139
42. Dudley, D. J., Branch, D. W., Edwin, S. S., and Mitchell, M. D. (1996) Induction of preterm birth in mice by RU486. Biol. Reprod. 55, 992–995
43. Gupta, S., and Roman, A. S. (2012) 17-α Hydroxyprogesterone caproate for the prevention of preterm birth. Womens Health (Lond) 8, 21–30
44. Jarde, A., Lutsiv, O., Park, C. K., Beyene, J., Dodd, J. M., Barrett, J., Shah, P. S., Cook, J. L., Saito, S., Biringer, A. B., Sabatino, L., Giglia, L., Han, Z., Staub, K., Mundle, W., Chamberlain, J., and McDonald, S. D. (2017) Effectiveness of progesterone, cerclage and pessary for preventing preterm birth in singleton pregnancies: a systematic review and network meta-analysis. [E-pub ahead of print] BJOG doi: 10.1111/1471-0528.14624
45. Mitchell, B. F., and Taggart, M. J. (2009) Are animal models relevant to key aspects of human parturition? Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R525–R545
46. Krishna, U. T. D., and Daftary, S. (2001) Pregnancy at Risk Current Concepts, 4th ed., Jaypee Brothers Medical Publishers, New Delhi, India
47. Radeva-Petrova, D., Kayentao, K., ter Kuile, F. O., Sinclair, D., and Garner, P. (2014) Drugs for preventing malaria in pregnant women in endemic areas: any drug regimen versus placebo or no treatment. Cochrane Database Syst. Rev. (10):CD000169
48. Garner, P., and Gülmezoglu, A. M. (2006) Drugs for preventing malaria in pregnant women. Cochrane Database Syst. Rev. (4): CD000169
49. Ngassa, P. C. (2000) Malaria parasitaemia and the risk of preterm labour: a re-evaluation of the evidence. Afr. J. Reprod. Health 4, 53–61
50. Zhang, T., Luo, X. J., Sai, W. B., Yu, M. F., Li, W. E., Ma, Y. F., Chen, W., Zhai, K., Qin, G., Guo, D., Zheng, Y. M., Wang, Y. X., Shen, J. H., Ji, G., and Liu, Q. H. (2014) Non-selective cation channels mediate chloroquine-induced relaxation in precontracted mouse airway smooth muscle. PLoS One 9, e101578
51. Tan, X., and Sanderson, M. J. (2014) Bitter tasting compounds dilate airways by inhibiting airway smooth muscle calcium oscillations and calcium sensitivity. Br. J. Pharmacol. 171, 646–662
52. Moynihan, A. T., Smith, T. J., and Morrison, J. J. (2008) The relaxant effect of nifedipine in human uterine smooth muscle and the BK(Ca) channel. Am. J. Obstet. Gynecol. 198, 237.e1–237.e8
53. 2+ by membrane voltage: toward understanding the excitation–contraction coupling in human myometrium. Ann. N. Y. Acad. Sci. 1101, 97–109
54. Sai, W. B., Yu, M. F., Wei, M. Y., Lu, Z., Zheng, Y. M., Wang, Y. X., Qin, G., Guo, D., Ji, G., Shen, J., and Liu, Q. H. (2014) Bitter tastants induce relaxation of rat thoracic aorta precontracted with high K(+). Clin. Exp. Pharmacol. Physiol. 41, 301–308
55. Upadhyaya, J. D., Singh, N., Sikarwar, A. S., Chakraborty, R., Pydi, S. P., Bhullar, R. P., Dakshinamurti, S., and Chelikani, P. (2014) Dextromethorphan mediated bitter taste receptor activation in the pulmonary circuit causes vasoconstriction. PLoS One 9, e110373
56. Avau, B., Rotondo, A., Thijs, T., Andrews, C. N., Janssen, P., Tack, J., and Depoortere, I. (2015) Targeting extra-oral bitter taste receptors modulates gastrointestinal motility with effects on satiation. Sci. Rep. 5, 15985
57. Sakai, H., Sato, K., Kai, Y., Chiba, Y., and Narita, M. (2016) Denatonium and 6-n-propyl-2-thiouracil, agonists of bitter taste receptor, inhibit contraction of various types of smooth muscles in the rat and mouse. Biol. Pharm. Bull. 39, 33–41
58. Clapp, T. R., Trubey, K. R., Vandenbeuch, A., Stone, L. M., Margolskee, R. F., Chaudhari, N., and Kinnamon, S. C. (2008) Tonic activity of Galpha-gustducin regulates taste cell responsivity. FEBS Lett. 582, 3783–3787
59. Caicedo, A., Pereira, E., Margolskee, R. F., and Roper, S. D. (2003) Role of the G-protein subunit alpha-gustducin in taste cell responses to bitter stimuli. J. Neurosci. 23, 9947–9952
60. Ueda, T., Ugawa, S., Yamamura, H., Imaizumi, Y., and Shimada, S. (2003) Functional interaction between T2R taste receptors and G-protein alpha subunits expressed in taste receptor cells. J. Neurosci. 23, 7376–7380
61. Ruiz-Avila, L., McLaughlin, S. K., Wildman, D., McKinnon, P. J., Robichon, A., Spickofsky, N., and Margolskee, R. F. (1995) Coupling of bitter receptor to phosphodiesterase through transducin in taste receptor cells. Nature 376, 80–85