Non-genomic estrogen regulation of ion transport and airway surface liquid dynamics in cystic fibrosis bronchial epithelium

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Saint Criq, Vinciane ^a   Kim, Sung Hoon ^b   Katzenellenbogen, John A ^b   Harvey, Brian J ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BUMETANIDE; CYCLIC AMP; DENDRIMER; EPITHELIAL SODIUM CHANNEL; ESTRADIOL; ESTROGEN RECEPTOR; FORSKOLIN; POTASSIUM; PROTEIN KINASE C DELTA;

AIRWAY SURFACE LIQUID; ARTICLE; BRONCHUS CHARACTERISTICS AND FUNCTIONS; BRONCHUS MUCOSA; CASE REPORT; CHILD; CHLORIDE TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDRATION; INHIBITION KINETICS; ION TRANSPORT; PRESCHOOL CHILD; SENSITIVITY ANALYSIS; SHORT CIRCUIT CURRENT; SODIUM ABSORPTION;

AMILORIDE; BRONCHI; BUMETANIDE; CELL LINE; COLFORSIN; CYCLIC AMP; CYSTIC FIBROSIS; EPITHELIAL CELLS; EPITHELIAL SODIUM CHANNELS; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; ION TRANSPORT; MALE; OUABAIN; PROTEIN KINASE C-DELTA; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE; WATER;

EID: 84892390464     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078593     Document Type: Article

References (57)

1. Musselman TM, Zhang Z, Masilamani SM (2010) Differential regulation of the bumetanide-sensitive cotransporter (NKCC2) by ovarian hormones. Steroids 75: 760-765.
2. Beers KW, Thompson MA, Chini EN, Dousa TP (1996) beta-Estradiol inhibits Na+-P(i) cotransport across renal brush border membranes from ovarectomized rats. Biochem Biophys Res Commun 221: 442-445.
3. Hofmeister MV, Damkier HH, Christensen BM, Olde B, Fredrik Leeb- Lundberg LM, et al. (2012) 17beta-Estradiol induces nongenomic effects in renal intercalated cells through G protein-coupled estrogen receptor 1. Am J Physiol Renal Physiol 302: F358-368.
4. Cao G, van der Wijst J, van der Kemp A, van Zeeland F, Bindels RJ, et al. (2009) Regulation of the epithelial Mg2 + channel TRPM6 by estrogen and the associated repressor protein of estrogen receptor activity (REA). J Biol Chem 284: 14788-14795.
5. Groenestege WM, Hoenderop JG, van den Heuvel L, Knoers N, Bindels RJ (2006) The epithelial Mg2+ channel transient receptor potential melastatin 6 is regulated by dietary Mg2+ content and estrogens. J Am Soc Nephrol 17: 1035-1043.
6. Irnaten M, Blanchard-Gutton N, Praetorius J, Harvey BJ (2009) Rapid effects of 17beta-estradiol on TRPV5 epithelial Ca2+ channels in rat renal cells. Steroids 74: 642-649.
7. Alzamora R, O'Mahony F, Harvey BJ (2011) Estrogen inhibits chloride secretion caused by cholera and Escherichia coli enterotoxins in female rat distal colon. Steroids 76: 867-876.
8. Condliffe SB, Doolan CM, Harvey BJ (2001) 17beta-oestradiol acutely regulates Cl- secretion in rat distal colonic epithelium. J Physiol 530: 47-54.
9. O'Mahony F, Alzamora R, Chung HL, Thomas W, Harvey BJ (2009) Genomic priming of the antisecretory response to estrogen in rat distal colon throughout the estrous cycle. Mol Endocrinol 23: 1885-1899.
10. Doolan CM, Harvey BJ (1996) Modulation of cytosolic protein kinase C and calcium ion activity by steroid hormones in rat distal colon. J Biol Chem 271: 8763-8767.
11. Doolan CM, Harvey BJ (1996) Rapid effects of steroid hormones on free intracellular calcium in T84 colonic epithelial cells. Am J Physiol 271: C1935-1941.
12. Doolan CM, Condliffe SB, Harvey BJ (2000) Rapid non-genomic activation of cytosolic cyclic AMP-dependent protein kinase activity and [Ca(2+)](i) by 17beta-oestradiol in female rat distal colon. Br J Pharmacol 129: 1375-1386.
13. O'Mahony F, Alzamora R, Betts V, LaPaix F, Carter D, et al. (2007) Female gender-specific inhibition of KCNQ1 channels and chloride secretion by 17beta-estradiol in rat distal colonic crypts. J Biol Chem 282: 24563-24573.
14. Singh AK, Schultz BD, Katzenellenbogen JA, Price EM, Bridges RJ, et al. (2000) Estrogen inhibition of cystic fibrosis transmembrane conductance regulator-mediated chloride secretion. J Pharmacol Exp Ther 295: 195-204.
15. Tam A, Morrish D, Wadsworth S, Dorscheid D, Man SP, et al. (2011) The role of female hormones on lung function in chronic lung diseases. BMC Womens Health 11: 24.
16. Matsui H, Grubb BR, Tarran R, Randell SH, Gatzy JT, et al. (1998) Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
17. Corey M (1996) Survival estimates in cystic fibrosis: snapshots of a moving target. Pediatr Pulmonol 21: 149-150.
18. Corey M, Edwards L, Levison H, Knowles M (1997) Longitudinal analysis of pulmonary function decline in patients with cystic fibrosis. J Pediatr 131: 809-814.
19. Coakley RD, Sun H, Clunes LA, Rasmussen JE, Stackhouse JR, et al. (2008) 17beta-Estradiol inhibits Ca2+-dependent homeostasis of airway surface liquid volume in human cystic fibrosis airway epithelia. J Clin Invest 118: 4025-4035.
20. Laube M, Kuppers E, Thome UH (2011) Modulation of sodium transport in alveolar epithelial cells by estradiol and progesterone. Pediatr Res 69: 200-205.
21. Chotirmall SH, Greene CM, Oglesby IK, Thomas W, O'Neill SJ, et al. (2010) 17Beta-estradiol inhibits IL-8 in cystic fibrosis by up-regulating secretory leucoprotease inhibitor. Am J Respir Crit Care Med 182: 62-72.
22. Chotirmall SH, Smith SG, Gunaratnam C, Cosgrove S, Dimitrov BD, et al. (2012) Effect of estrogen on pseudomonas mucoidy and exacerbations in cystic fibrosis. N Engl J Med 366: 1978-1986.
23. Guilbault C, Martin P, Houle D, Boghdady ML, Guiot MC, et al. (2005) Cystic fibrosis lung disease following infection with Pseudomonas aeruginosa in Cftr knockout mice using novel non-invasive direct pulmonary infection technique. Lab Anim 39: 336-352.
24. Wang Y, Cela E, Gagnon S, Sweezey NB (2010) Estrogen aggravates inflammation in Pseudomonas aeruginosa pneumonia in cystic fibrosis mice. Respir Res 11: 166.
25. Gerlach U, Brendel J, Lang HJ, Paulus EF, Weidmann K, et al. (2001) Synthesis and activity of novel and selective I(Ks)-channel blockers. J Med Chem 44: 3831-3837.
26. Harrington WR, Kim SH, Funk CC, Madak-Erdogan Z, Schiff R, et al. (2006) Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol Endocrinol 20: 491-502.
27. Kim SH, Katzenellenbogen JA (2006) Hormone-PAMAM dendrimer conjugates: polymer dynamics and tether structure affect ligand access to receptors. Angew Chem Int Ed Engl 45: 7243-7248.
28. Zabner J, Karp P, Seiler M, Phillips SL, Mitchell CJ, et al. (2003) Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol 284: L844-854.
29. Verriere V, Higgins G, Al-Alawi M, Costello RW, McNally P, et al. (2012) Lipoxin A4 stimulates calcium-activated chloride currents and increases airway surface liquid height in normal and cystic fibrosis airway epithelia. PLoS One 7: e37746.
30. Lam RS, App EM, Nahirney D, Szkotak AJ, Vieira-Coelho MA, et al. (2003) Regulation of Cl- secretion by alpha2-adrenergic receptors in mouse colonic epithelium. J Physiol 548: 475-484.
31. Santanam N, Shern-Brewer R, McClatchey R, Castellano PZ, Murphy AA, et al. (1998) Estradiol as an antioxidant: incompatible with its physiological concentrations and function. J Lipid Res 39: 2111-2118.
32. Stevis PE, Deecher DC, Suhadolnik L, Mallis LM, Frail DE (1999) Differential effects of estradiol and estradiol-BSA conjugates. Endocrinology 140: 5455-5458.
33. Taguchi Y, Koslowski M, Bodenner DL (2004) Binding of estrogen receptor with estrogen conjugated to bovine serum albumin (BSA). Nucl Recept 2: 5.
34. Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, et al. (2008) Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol Endocrinol 22: 2116-2127.
35. Rosenfeld M, Davis R, FitzSimmons S, Pepe M, Ramsey B (1997) Gender gap in cystic fibrosis mortality. Am J Epidemiol 145: 794-803.
36. Verma N, Bush A, Buchdahl R (2005) Is there still a gender gap in cystic fibrosis? Chest 128: 2824-2834.
37. Arrington-Sanders R, Yi MS, Tsevat J, Wilmott RW, Mrus JM, et al. (2006) Gender differences in health-related quality of life of adolescents with cystic fibrosis. Health Qual Life Outcomes 4: 5.
38. Block JK, Vandemheen KL, Tullis E, Fergusson D, Doucette S, et al. (2006) Predictors of pulmonary exacerbations in patients with cystic fibrosis infected with multi-resistant bacteria. Thorax 61: 969-974.
39. Boucher RC (2002) An overview of the pathogenesis of cystic fibrosis lung disease. Adv Drug Deliv Rev 54: 1359-1371.
40. Rochwerger L, Buchwald M (1993) Stimulation of the cystic fibrosis transmembrane regulator expression by estrogen in vivo. Endocrinology 133: 921-930.
41. Sweezey NB, Ghibu F, Gagnon S (1997) Sex hormones regulate CFTR in developing fetal rat lung epithelial cells. Am J Physiol 272: L844-851.
42. Yang GZ, Nie HG, Lu L, Chen J, Lu XY, et al. (2011) Estrogen regulates the expression and activity of epithelial sodium channel in mouse osteoblasts. Cell Mol Biol (Noisy-le-grand) 57 Suppl: OL1480-1486.
43. Mohrmann M, Cantiello HF, Ausiello DA (1987) Inhibition of epithelial Na+ transport by atriopeptin, protein kinase c, and pertussis toxin. Am J Physiol 253: F372-376.
44. Soukup B, Benjamin A, Orogo-Wenn M, Walters D (2012) Physiological effect of protein kinase C on ENaC-mediated lung liquid regulation in the adult rat lung. Am J Physiol Lung Cell Mol Physiol 302: L133-139.
45. Li Y, Yang J, Li S, Zhang J, Zheng J, et al. (2011) N-myc downstream-regulated gene 2, a novel estrogen-targeted gene, is involved in the regulation of Na+/K+-ATPase. J Biol Chem 286: 32289-32299.
46. Burchfield JG, Lennard AJ, Narasimhan S, Hughes WE, Wasinger VC, et al. (2004) Akt mediates insulin-stimulated phosphorylation of Ndrg2: evidence for cross-talk with protein kinase C theta. J Biol Chem 279: 18623-18632.
47. Saint-Criq V, Rapetti-Mauss R, Yusef YR, Harvey BJ (2012) Estrogen regulation of epithelial ion transport: Implications in health and disease. Steroids 77: 918-923.
48. Levin ER (2009) Membrane oestrogen receptor alpha signalling to cell functions. J Physiol 587: 5019-5023.
49. Moro L, Reineri S, Piranda D, Pietrapiana D, Lova P, et al. (2005) Nongenomic effects of 17beta-estradiol in human platelets: potentiation of thrombin-induced aggregation through estrogen receptor beta and Src kinase. Blood 105: 115-121.
50. Razandi M, Pedram A, Merchenthaler I, Greene GL, Levin ER (2004) Plasma membrane estrogen receptors exist and functions as dimers. Mol Endocrinol 18: 2854-2865.
51. Hammes SR, Levin ER (2007) Extranuclear steroid receptors: nature and actions. Endocr Rev 28: 726-741.
52. Alyea RA, Laurence SE, Kim SH, Katzenellenbogen BS, Katzenellenbogen JA, et al. (2008) The roles of membrane estrogen receptor subtypes in modulating dopamine transporters in PC-12 cells. J Neurochem 106: 1525-1533.
53. Chambliss KL, Wu Q, Oltmann S, Konaniah ES, Umetani M, et al. (2010) Non-nuclear estrogen receptor alpha signaling promotes cardiovascular protection but not uterine or breast cancer growth in mice. J Clin Invest 120: 2319-2330.
54. Yang LC, Zhang QG, Zhou CF, Yang F, Zhang YD, et al. (2010) Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One 5: e9851.
55. Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, et al. (2006) A variant of estrogen receptor-{alpha}, hER-{alpha}36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signaling. Proc Natl Acad Sci U S A 103: 9063-9068.
56. Wang Z, Zhang X, Shen P, Loggie BW, Chang Y, et al. (2005) Identification, cloning, and expression of human estrogen receptor-alpha36, a novel variant of human estrogen receptor-alpha66. Biochem Biophys Res Commun 336: 1023-1027.
57. Tong JS, Zhang QH, Wang ZB, Li S, Yang CR, et al. (2010) ER-alpha36, a novel variant of ER-alpha, mediates estrogen-stimulated proliferation of endometrial carcinoma cells via the PKCdelta/ERK pathway. PLoS One 5: e15408.