Extracellular pH and lung infections in cystic fibrosis

European Journal of Cell Biology

Volumn 97, Issue 6, 2018, Pages 402-410

  Massip Copiz, María Macarena ^a   Santa Coloma, Tomás Antonio ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA ARGENTINA   (Argentina)

Author keywords

ASL; CFTR; Cystic fibrosis; Extracellular pH; Infections

Indexed keywords

BICARBONATE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

BACTERIAL STRAIN; BIOFILM; CELL PH; CYSTIC FIBROSIS; HUMAN; INFECTION SENSITIVITY; LUNG INFECTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; CHEMISTRY; EXTRACELLULAR SPACE; GENETICS; LUNG; METABOLISM; MICROBIOLOGY; PATHOLOGY; PH;

ANIMALS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EXTRACELLULAR SPACE; HUMANS; HYDROGEN-ION CONCENTRATION; LUNG;

EID: 85048711293     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2018.06.001     Document Type: Review

References (168)

1. Abou Alaiwa, M.H., Beer, A.M., Pezzulo, A.A., Launspach, J.L., Horan, R.A., Stoltz, D.A., Starner, T.D., Welsh, M.J., Zabner, J., Neonates with cystic fibrosis have a reduced nasal liquid pH; a small pilot study. J. Cyst. Fibros. 13 (2014), 373–377, 10.1016/j.jcf.2013.12.006.
2. Albert, L.S., Brown, D.G., Variation in bacterial ATP concentration during rapid changes in extracellular pH and implications for the activity of attached bacteria. Colloids Surf. B Biointerfaces 132 (2015), 111–116, 10.1016/j.colsurfb.2015.05.020.
3. Alhadeff, J.A., Glycoproteins and cystic fibrosis: a review. Clin. Genet. 14 (1978), 189–201, 10.1111/j.1399-0004.1978.tb02130.x.
4. Alka, K., Casey, J.R., Bicarbonate transport in health and disease. IUBMB Life 66 (2014), 596–615, 10.1002/iub.1315.
5. Althaus, M., ENaC inhibitors and airway re-hydration in cystic fibrosis: state of the art. Curr. Mol. Pharmacol. 6 (2013), 3–12, 10.2174/18744672112059990025.
6. Avella, M., Loriol, C., Boulukos, K., Borgese, F., Ehrenfeld, J., SLC26A9 stimulates CFTR expression and function in human bronchial cell lines. J. Cell. Physiol. 226 (2011), 212–223, 10.1002/jcp.22328.
7. Barroso, M.P., Gomez-Diaz, C., Lopez-Lluch, G., Malagon, M.M., Crane, F.L., Navas, P., Ascorbate and alpha-tocopherol prevent apoptosis induced by serum removal independent of Bcl-2. Arch. Biochem. Biophys. 343 (1997), 243–248, 10.1006/abbi.1997.0170.
8. Berkebile, A.R., McCray, P.B., Effects of airway surface liquid pH on host defense in cystic fibrosis. Int. J. Biochem. Cell Biol. 52 (2014), 124–129, 10.1016/j.biocel.2014.02.009.
9. Bertrand, C.A., Zhang, R., Pilewski, J.M., Frizzell, R.A., SLC26A9 is a constitutively active, CFTR-regulated anion conductance in human bronchial epithelia. J. Gen. Physiol. 133 (2009), 421–438, 10.1085/jgp.200810097.
10. Bhagirath, A.Y., Li, Y., Somayajula, D., Dadashi, M., Badr, S., Duan, K., Cystic fibrosis lung environment and Pseudomonas aeruginosa infection. BMC Pulm. Med., 16, 2016, 174, 10.1186/s12890-016-0339-5.
11. Bjarnsholt, T., Jensen, P.O., Fiandaca, M.J., Pedersen, J., Hansen, C.R., Andersen, C.B., Pressler, T., Givskov, M., Hoiby, N., Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol. 44 (2009), 547–558, 10.1002/ppul.21011.
12. Boron, W.F., Regulation of intracellular pH. Adv. Physiol. Educ. 28 (2004), 160–179, 10.1152/advan.00045.2004.
13. Borowitz, D., CFTR, bicarbonate, and the pathophysiology of cystic fibrosis. Pediatr. Pulmonol. 50:Suppl. 40 (2015), S24–S30, 10.1002/ppul.23247.
14. Boucher, R.C., Evidence for airway surface dehydration as the initiating event in CF airway disease. J. Intern. Med. 261 (2007), 5–16, 10.1111/j.1365-2796.2006.01744.x.
15. Brouillard, F., Bouthier, M., Leclerc, T., Clement, A., Baudouin-Legros, M., Edelman, A., NF-kappa B mediates up-regulation of CFTR gene expression in Calu-3 cells by interleukin-1beta. J. Biol. Chem. 276 (2001), 9486–9491, 10.1074/jbc.M006636200.
16. Bruscia, E.M., Bonfield, T.L., Innate and adaptive immunity in cystic fibrosis. Clin. Chest Med. 37 (2016), 17–29, 10.1016/j.ccm.2015.11.010.
17. Button, B., Cai, L.H., Ehre, C., Kesimer, M., Hill, D.B., Sheehan, J.K., Boucher, R.C., Rubinstein, M., A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337 (2012), 937–941, 10.1126/science.1223012.
18. Cafferata, E.G., González-Guerrico, A.M., Pivetta, O.H., Santa-Coloma, T.A., Identification by differential display of a mRNA specifically induced by 12-O-tetradecanoylphorbol-13-acetate (TPA) in T84 human colon carcinoma cells. Cell. Mol. Biol. (Noisy-le-grand) 42 (1996), 797–804.
19. Cafferata, E.G., Gonzalez-Guerrico, A.M., Giordano, L., Pivetta, O.H., Santa-Coloma, T.A., Interleukin-1beta regulates CFTR expression in human intestinal T84 cells. Biochim. Biophys. Acta 1500 (2000), 241–248, 10.1016/S0925-4439(99)00105-2.
20. Cafferata, E.G., González Guerrico, A.M., Di Paolo, N., Pitossi, F., Pivetta, O.H., Santa Coloma, T.A., Abstract 3. NF-Kappa B Activation Is Involved in Regulation of CFTR by IL-1beta. XIIIth International Cystic Fibrosis Congress, 4-8 June 2000. Stockholm, Sweden. Abstracts book, 2000, p89.
21. Cafferata, E.G., Guerrico, A.M., Pivetta, O.H., Santa-Coloma, T.A., NF-kappaB activation is involved in regulation of cystic fibrosis transmembrane conductance regulator (CFTR) by interleukin-1beta. J. Biol. Chem. 276 (2001), 15441–15444, 10.1074/jbc.M010061200.
22. Callebaut, I., Hoffmann, B., Lehn, P., Mornon, J.P., Molecular modelling and molecular dynamics of CFTR. Cell. Mol. Life Sci. 74 (2017), 3–22, 10.1007/s00018-016-2385-9.
23. Casey, J.R., Grinstein, S., Orlowski, J., Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11 (2010), 50–61, 10.1038/nrm2820.
24. Chao, H.H., Yang, V.C., Chen, J.K., Acidic FGF and EGF are involved in the autocrine growth stimulation of a human nasopharyngeal carcinoma cell line and sub-line cells. Int. J. Cancer 54 (1993), 807–812, 10.1002/ijc.2910540515.
25. Chen, L., Wang, W.Y., Wang, Y.P., Inhibitory effects of lithospermic acid on proliferation and migration of rat vascular smooth muscle cells. Acta Pharmacol. Sin. 30 (2009), 1245–1252, 10.1038/aps.2009.122.
26. Chmiel, J.F., Aksamit, T.R., Chotirmall, S.H., Dasenbrook, E.C., Elborn, J.S., LiPuma, J.J., Ranganathan, S.C., Waters, V.J., Ratjen, F.A., Antibiotic management of lung infections in cystic fibrosis. II. Nontuberculous mycobacteria, anaerobic bacteria, and fungi. Ann. Am. Thorac. Soc. 11 (2014), 1298–1306, 10.1513/AnnalsATS.201405-203AS.
27. Ciofu, O., Tolker-Nielsen, T., Jensen, P.O., Wang, H., Hoiby, N., Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv. Drug Deliv. Rev. 85 (2015), 7–23, 10.1016/j.addr.2014.11.017.
28. Clauzure, M., Valdivieso, A.G., Massip Copiz, M.M., Schulman, G., Teiber, M.L., Santa-Coloma, T.A., Disruption of interleukin-1beta autocrine signaling rescues complex I activity and improves ROS levels in immortalized epithelial cells with impaired cystic fibrosis transmembrane conductance regulator (CFTR) function. PLoS One, 9, 2014, e99257, 10.1371/journal.pone.0099257.
29. Clauzure, M., Valdivieso, A.G., Massip-Copiz, M.M., Mori, C., Dugour, A.V., Figueroa, J.M., Santa-Coloma, T.A., Intracellular chloride concentration changes modulate IL-1beta expression and secretion in human bronchial epithelial cultured cells. J. Cell. Biochem. 118 (2017), 2131–2140, 10.1002/jcb.25850.
30. Coakley, R.D., Boucher, R.C., Regulation and functional significance of airway surface liquid pH. JOP 2 (2001), 294–300.
31. Coakley, R.J., Taggart, C., McElvaney, N.G., O'Neill, S.J., Cytosolic pH and the inflammatory microenvironment modulate cell death in human neutrophils after phagocytosis. Blood 100 (2002), 3383–3391, 10.1182/blood.V100.9.3383.
32. Coakley, R.D., Grubb, B.R., Paradiso, A.M., Gatzy, J.T., Johnson, L.G., Kreda, S.M., O'Neal, W.K., Boucher, R.C., Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 16083–16088, 10.1073/pnas.2634339100.
33. Cohen-Cymberknoh, M., Kerem, E., Ferkol, T., Elizur, A., Airway inflammation in cystic fibrosis: molecular mechanisms and clinical implications. Thorax 68 (2013), 1157–1162, 10.1136/thoraxjnl-2013-203204.
34. Cooper, J.L., Quinton, P.M., Ballard, S.T., Mucociliary transport in porcine trachea: differential effects of inhibiting chloride and bicarbonate secretion. Am. J. Physiol. Lung Cell Mol. Physiol. 304 (2013), L184–190, 10.1152/ajplung.00143.2012.
35. Danhof, H.A., Vylkova, S., Vesely, E.M., Ford, A.E., Gonzalez-Garay, M., Lorenz, M.C., Robust extracellular pH modulation by candida albicans during growth in carboxylic acids. MBio, 7, 2016, 10.1128/mBio.01646-16 e01646-e01616.
36. Danko, T., Hargitai, D., Pataki, A., Hakim, H., Molnar, M., Zsembery, A., Extracellular alkalinization stimulates calcium-activated chloride conductance in cystic fibrosis human airway epithelial cells. Cell. Physiol. Biochem. 27 (2011), 401–410, 10.1159/000327967.
37. Donaldson, S.H., Boucher, R.C., Sodium channels and cystic fibrosis. Chest 132 (2007), 1631–1636, 10.1378/chest.07-0288.
38. Egan, M.E., CFTR-associated ATP transport and release. Methods Mol. Med. 70 (2002), 395–406, 10.1385/1-59259-187-6:395.
39. Eichelbaum, K., Winter, M., Berriel Diaz, M., Herzig, S., Krijgsveld, J., Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat. Biotechnol. 30 (2012), 984–990, 10.1038/nbt.2356.
40. Farwell, W.R., Taylor, E.N., Serum anion gap, bicarbonate and biomarkers of inflammation in healthy individuals in a national survey. CMAJ 182 (2010), 137–141, 10.1503/cmaj.090329.
41. Fischer, H., Function of proton channels in lung epithelia. Wiley Interdiscip. Rev. Membr. Transp. Signal. 1 (2012), 247–258, 10.1002/wmts.17.
42. Fishelson, Z., Horstmann, R.D., Muller-Eberhard, H.J., Regulation of the alternative pathway of complement by pH. J. Immunol. 138 (1987), 3392–3395.
43. Galvin, P., Clarke, L.A., Harvey, S., Amaral, M.D., Microarray analysis in cystic fibrosis. J. Cyst. Fibros. 3:Suppl. 2 (2004), 29–33, 10.1016/j.jcf.2004.05.006.
44. Garland, A.L., Walton, W.G., Coakley, R.D., Tan, C.D., Gilmore, R.C., Hobbs, C.A., Tripathy, A., Clunes, L.A., Bencharit, S., Stutts, M.J., Betts, L., Redinbo, M.R., Tarran, R., Molecular basis for pH-dependent mucosal dehydration in cystic fibrosis airways. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 15973–15978, 10.1073/pnas.1311999110.
45. Garnett, J.P., Hickman, E., Burrows, R., Hegyi, P., Tiszlavicz, L., Cuthbert, A.W., Fong, P., Gray, M.A., Novel role for pendrin in orchestrating bicarbonate secretion in cystic fibrosis transmembrane conductance regulator (CFTR)-expressing airway serous cells. J. Biol. Chem. 286 (2011), 41069–41082, 10.1074/jbc.M111.266734.
46. Gawenis, L.R., Franklin, C.L., Simpson, J.E., Palmer, B.A., Walker, N.M., Wiggins, T.M., Clarke, L.L., cAMP inhibition of murine intestinal Na/H exchange requires CFTR-mediated cell shrinkage of villus epithelium. Gastroenterology 125 (2003), 1148–1163, 10.1016/S0016-5085(03)01212-5.
47. Gelfond, D., Heltshe, S., Ma, C., Rowe, S.M., Frederick, C., Uluer, A., Sicilian, L., Konstan, M., Tullis, E., Roach, R.N., Griffin, K., Joseloff, E., Borowitz, D., Impact of CFTR modulation on intestinal pH, motility, and clinical outcomes in patients with cystic fibrosis and the G551D mutation. Clin. Transl. Gastroenterol., 8, 2017, e81, 10.1038/ctg.2017.10.
48. Giddings, O., Esther, C.R. Jr., Mapping targetable inflammation and outcomes with cystic fibrosis biomarkers. Pediatr. Pulmonol. 52 (2017), S21–S28, 10.1002/ppul.23768.
49. Gillies, R.J., Raghunand, N., Garcia-Martin, M.L., Gatenby, R.A., pH imaging. A review of pH measurement methods and applications in cancers. IEEE Eng. Med. Biol. Mag. 23 (2004), 57–64, 10.1109/MEMB.2004.1360409.
50. González Guerrico, A.M., Cafferata, E.G.M.P.V., Pivetta, O.H., Santa Coloma, T.A., Abstract. Identification of a New Gene (IIG) in IL-1b-Induced T84 Cells. VII Ibero-American Congress of Cell Biology, Montevideo. Uruguay, 1998.
51. González Guerrico, A.M., Cafferata, E.G., Gruenert, D., Pivetta, O.H., Santa-Coloma, T.A., 1999. Abstract M238 [El gen c-src es un posible marcador funcional del canal de cloruro afectado en fibrosis quística: CFTR], 35th Annual Meeting of the Argentine Society for Biochemistry and Molecular Biology Research Mendoza, Argentina. Abstracts Book. http: https://doi.org///dx.doi.org/10.13140/RG.2.1.1826.5843.
52. González-Guerrico, A.M., PhD Thesis [Expresión de Genes Asociados a Fibrosis Quística]. 2001, University of Buenos Aires, Buenos Aires, Argentina.
53. Gonzalez-Guerrico, A.M., Cafferata, E.G., Radrizzani, M., Marcucci, F., Gruenert, D., Pivetta, O.H., Favaloro, R.R., Laguens, R., Perrone, S.V., Gallo, G.C., Santa-Coloma, T.A., Tyrosine kinase c-Src constitutes a bridge between cystic fibrosis transmembrane regulator channel failure and MUC1 overexpression in cystic fibrosis. J. Biol. Chem. 277 (2002), 17239–17247, 10.1074/jbc.M112456200.
54. Gstraunthaler, G., Alternatives to the use of fetal bovine serum: serum-free cell culture. ALTEX 20 (2003), 275–281.
55. Hackam, D.J., Grinstein, S., Nathens, A., Watson, W.G., Marshall, J.C., Rotstein, O.D., Exudative neutrophils show impaired pH regulation compared with circulating neutrophils. Arch. Surg. 131 (1996), 1296–1301, 10.1001/archsurg.1996.01430240050006.
56. Halestrap, A.P., Monocarboxylic acid transport. Compr. Physiol. 3 (2013), 1611–1643, 10.1002/cphy.c130008.
57. Halestrap, A.P., The SLC16 gene family - structure, role and regulation in health and disease. Mol. Aspects Med. 34 (2013), 337–349, 10.1016/j.mam.2012.05.003.
58. Hartl, D., Gaggar, A., Bruscia, E., Hector, A., Marcos, V., Jung, A., Greene, C., McElvaney, G., Mall, M., Doring, G., Innate immunity in cystic fibrosis lung disease. J. Cyst. Fibros. 11 (2012), 363–382, 10.1016/j.jcf.2012.07.003.
59. Heming, T.A., Dave, S.K., Tuazon, D.M., Chopra, A.K., Peterson, J.W., Bidani, A., Effects of extracellular pH on tumour necrosis factor-alpha production by resident alveolar macrophages. Clin. Sci. (Lond.) 101 (2001), 267–274, 10.1042/cs1010267.
60. Henderson, A.G., Ehre, C., Button, B., Abdullah, L.H., Cai, L.H., Leigh, M.W., DeMaria, G.C., Matsui, H., Donaldson, S.H., Davis, C.W., Sheehan, J.K., Boucher, R.C., Kesimer, M., Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J. Clin. Invest. 124 (2014), 3047–3060, 10.1172/jci73469.
61. Hoiby, N., Recent advances in the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. BMC Med., 9, 2011, 32, 10.1186/1741-7015-9-32.
62. Hoiby, N., Ciofu, O., Bjarnsholt, T., Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 5 (2010), 1663–1674, 10.2217/fmb.10.125.
63. Hollomon, J.M., Grahl, N., Willger, S.D., Koeppen, K., Hogan, D.A., Global role of cyclic AMP signaling in pH-dependent responses in Candida albicans. mSphere 1 (2016), e00283–00216, 10.1128/mSphere.00283-16.
64. Huang, J., Kim, D., Shan, J., Abu-Arish, A., Luo, Y., Hanrahan, J.W., Most bicarbonate secretion by Calu-3 cells is mediated by CFTR and independent of pendrin. Physiol. Rep., 6, 2018, e13641, 10.14814/phy2.13641.
65. Hug, M.J., Tamada, T., Bridges, R.J., CFTR and bicarbonate secretion by epithelial cells. News Physiol. Sci. 18 (2003), 38–42, 10.1152/nips.01412.2002.
66. Hunt, J.F., Fang, K., Malik, R., Snyder, A., Malhotra, N., Platts-Mills, T.A., Gaston, B., Endogenous airway acidification. Implications for asthma pathophysiology. Am. J. Respir. Crit. Care Med. 161 (2000), 694–699, 10.1164/ajrccm.161.3.9911005.
67. Illek, B., Yankaskas, J.R., Machen, T.E., cAMP and genistein stimulate HCO3- conductance through CFTR in human airway epithelia. Am. J. Physiol. 272 (1997), L752–761, 10.1152/ajplung.1997.272.4.L752.
68. Illek, B., Fischer, H., Machen, T.E., Genetic disorders of membrane transport. II. Regulation of CFTR by small molecules including HCO3. Am. J. Physiol. 275 (1998), G1221–G1226, 10.1152/ajpgi.1998.275.6.G1221.
69. Jakab, R.L., Collaco, A.M., Ameen, N.A., Cell-specific effects of luminal acid, bicarbonate, cAMP, and carbachol on transporter trafficking in the intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 303 (2012), G937–950, 10.1152/ajpgi.00452.2011.
70. Jung, J., Nam, J.H., Park, H.W., Oh, U., Yoon, J.H., Lee, M.G., Dynamic modulation of ANO1/TMEM16A HCO3(-) permeability by Ca2+/calmodulin. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 360–365, 10.1073/pnas.1211594110.
71. Karslake, J., Maltas, J., Brumm, P., Wood, K.B., Population density modulates drug inhibition and gives rise to potential bistability of treatment outcomes for bacterial infections. PLoS Comput. Biol., 12, 2016, e1005098, 10.1371/journal.pcbi.1005098.
72. Knowles, M.R., Boucher, R.C., Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109 (2002), 571–577, 10.1172/jci15217.
73. Ko, S.B., Shcheynikov, N., Choi, J.Y., Luo, X., Ishibashi, K., Thomas, P.J., Kim, J.Y., Kim, K.H., Lee, M.G., Naruse, S., Muallem, S., A molecular mechanism for aberrant CFTR-dependent HCO(3)(-) transport in cystic fibrosis. EMBO J. 21 (2002), 5662–5672, 10.1093/emboj/cdf580.
74. Ko, S.B., Zeng, W., Dorwart, M.R., Luo, X., Kim, K.H., Millen, L., Goto, H., Naruse, S., Soyombo, A., Thomas, P.J., Muallem, S., Gating of CFTR by the STAS domain of SLC26 transporters. Nat. Cell Biol. 6 (2004), 343–350, 10.1038/ncb1115.
75. Kogan, I., Ramjeesingh, M., Li, C., Kidd, J.F., Wang, Y., Leslie, E.M., Cole, S.P., Bear, C.E., CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J. 22 (2003), 1981–1989, 10.1093/emboj/cdg194.
76. Kreda, S.M., Davis, C.W., Rose, M.C., CFTR, mucins, and mucus obstruction in cystic fibrosis. Cold Spring Harb. Perspect. Med., 2, 2012, a009589, 10.1101/cshperspect.a009589.
77. Kunzelmann, K., Schreiber, R., Hadorn, H.B., Bicarbonate in cystic fibrosis. J. Cyst. Fibros. 16 (2017), 653–662, 10.1016/j.jcf.2017.06.005.
78. Lardner, A., The effects of extracellular pH on immune function. J. Leukoc. Biol. 69 (2001), 522–530, 10.1189/jlb.69.4.522.
79. Lee, M.G., Wigley, W.C., Zeng, W., Noel, L.E., Marino, C.R., Thomas, P.J., Muallem, S., Regulation of Cl-/ HCO3- exchange by cystic fibrosis transmembrane conductance regulator expressed in NIH 3T3 and HEK 293 cells. J. Biol. Chem. 274 (1999), 3414–3421, 10.1074/jbc.274.6.3414.
80. Lim, S.H., Legere, E.A., Snider, J., Stagljar, I., Recent progress in CFTR interactome mapping and its importance for cystic fibrosis. Front. Pharmacol., 8, 2017, 997, 10.3389/fphar.2017.00997.
81. Linsdell, P., Tabcharani, J.A., Rommens, J.M., Hou, Y.X., Chang, X.B., Tsui, L.C., Riordan, J.R., Hanrahan, J.W., Permeability of wild-type and mutant cystic fibrosis transmembrane conductance regulator chloride channels to polyatomic anions. J. Gen. Physiol. 110 (1997), 355–364, 10.1085/jgp.110.4.355.
82. Liu, H., Maruyama, H., Masuda, T., Honda, A., Arai, F., The influence of virus infection on the extracellular pH of the host cell detected on cell membrane. Front. Microbiol., 7, 2016, 1127, 10.3389/fmicb.2016.01127.
83. Liu, F., Zhang, Z., Csanady, L., Gadsby, D.C., Chen, J., Molecular structure of the human CFTR ion channel. Cell 169 (2017), 85–95, 10.1016/j.cell.2017.02.024 e88.
84. Lohi, H., Kujala, M., Makela, S., Lehtonen, E., Kestila, M., Saarialho-Kere, U., Markovich, D., Kere, J., Functional characterization of three novel tissue-specific anion exchangers SLC26A7, -A8, and -A9. J. Biol. Chem. 277 (2002), 14246–14254, 10.1074/jbc.M111802200.
85. Luan, X., Campanucci, V.A., Nair, M., Yilmaz, O., Belev, G., Machen, T.E., Chapman, D., Ianowski, J.P., Pseudomonas aeruginosa triggers CFTR-mediated airway surface liquid secretion in swine trachea. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 12930–12935, 10.1073/pnas.1406414111.
86. Luan, X., Belev, G., Tam, J.S., Jagadeeshan, S., Hassan, N., Gioino, P., Grishchenko, N., Huang, Y., Carmalt, J.L., Duke, T., Jones, T., Monson, B., Burmester, M., Simovich, T., Yilmaz, O., Campanucci, V.A., Machen, T.E., Chapman, L.D., Ianowski, J.P., Cystic fibrosis swine fail to secrete airway surface liquid in response to inhalation of pathogens. Nat. Commun., 8, 2017, 786, 10.1038/s41467-017-00835-7.
87. Luckie, D.B., Singh, C.N., Wine, J.J., Wilterding, J.H., CFTR activation raises extracellular pH of NIH/3T3 mouse fibroblasts and C127 epithelial cells. J. Membr. Biol. 179 (2001), 275–284, 10.1007/s002320010052.
88. Luckie, D.B., Van Alst, A.J., Massey, M.K., Flood, R.D., Shah, A.A., Malhotra, V., Kozel, B.J., Chemical rescue of DeltaF508-CFTR in C127 epithelial cells reverses aberrant extracellular pH acidification to wild-type alkalization as monitored by microphysiometry. Biochem. Biophys. Res. Commun. 451 (2014), 535–540, 10.1016/j.bbrc.2014.08.036.
89. Mall, M., Bleich, M., Kuehr, J., Brandis, M., Greger, R., Kunzelmann, K., CFTR-mediated inhibition of epithelial Na+ conductance in human colon is defective in cystic fibrosis. Am. J. Physiol. 277 (1999), G709–716, 10.1152/ajpgi.1999.277.3.G709.
90. Martinez, D., Vermeulen, M., von Euw, E., Sabatte, J., Maggini, J., Ceballos, A., Trevani, A., Nahmod, K., Salamone, G., Barrio, M., Giordano, M., Amigorena, S., Geffner, J., Extracellular acidosis triggers the maturation of human dendritic cells and the production of IL-12. J. Immunol. 179 (2007), 1950–1959, 10.4049/jimmunol.179.3.1950.
91. Martinez-Rossi, N.M., Peres, N.T., Rossi, A., Pathogenesis of dermatophytosis: sensing the host tissue. Mycopathologia 182 (2017), 215–227, 10.1007/s11046-016-0057-9.
92. Massip Copiz, M.M., Santa Coloma, T.A., C- Src and its role in cystic fibrosis. Eur. J. Cell Biol. 95 (2016), 401–413, 10.1016/j.ejcb.2016.08.001.
93. Massip-Copiz, M.M., Clauzure, M., Valdivieso, A.G., Santa-Coloma, T.A., CFTR impairment upregulates c-Src activity through IL-1beta autocrine signaling. Arch. Biochem. Biophys. 616 (2017), 1–12, 10.1016/j.abb.2017.01.003.
94. Massip-Copiz, M., Clauzure, M., Valdivieso, A.G., Santa-Coloma, T.A., Epiregulin (EREG) is upregulated through an IL-1beta autocrine loop in Caco-2 epithelial cells with reduced CFTR function. J. Cell. Biochem. 119 (2018), 2911–2922, 10.1002/jcb.26483.
95. Mastrocola, T., Porcelli, A.M., Rugolo, M., Role of CFTR and anion exchanger in bicarbonate fluxes in C127 cell lines. FEBS Lett. 440 (1998), 268–272, 10.1016/S0014-5793(98)01468-9.
96. Matsui, H., Grubb, B.R., Tarran, R., Randell, S.H., Gatzy, J.T., Davis, C.W., Boucher, R.C., Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95 (1998), 1005–1015, 10.1016/S0092-8674(00)81724-9.
97. Mauch, R.M., Jensen, P.O., Moser, C., Levy, C.E., Hoiby, N., Mechanisms of humoral immune response against Pseudomonas aeruginosa biofilm infection in cystic fibrosis. J. Cyst. Fibros. 17 (2018), 143–152, 10.1016/j.jcf.2017.08.012.
98. Mayer, M.L., Blohmke, C.J., Falsafi, R., Fjell, C.D., Madera, L., Turvey, S.E., Hancock, R.E., Rescue of dysfunctional autophagy attenuates hyperinflammatory responses from cystic fibrosis cells. J. Immunol. 190 (2013), 1227–1238, 10.4049/jimmunol.1201404.
99. McShane, D., Davies, J.C., Davies, M.G., Bush, A., Geddes, D.M., Alton, E.W., Airway surface pH in subjects with cystic fibrosis. Eur. Respir. J. 21 (2003), 37–42, 10.1183/09031936.03.00027603.
100. Nakahira, K., Cloonan, S.M., Mizumura, K., Choi, A.M., Ryter, S.W., Autophagy: a crucial moderator of redox balance, inflammation, and apoptosis in lung disease. Antioxid. Redox Signal. 20 (2014), 474–494, 10.1089/ars.2013.5373.
101. Nebert, D.W., Galvez-Peralta, M., Hay, E.B., Li, H., Johansson, E., Yin, C., Wang, B., He, L., Soleimani, M., ZIP14 and ZIP8 zinc/bicarbonate symporters in Xenopus oocytes: characterization of metal uptake and inhibition. Metallomics 4 (2012), 1218–1225, 10.1039/c2mt20177a.
102. Ngamtrakulpanit, L., Yu, Y., Adjei, A., Amoah, G., Gaston, B., Hunt, J., Identification of intrinsic airway acidification in pulmonary tuberculosis. Global J. Health Sci. 2 (2010), 106–110, 10.5539/gjhs.v2n1p106.
103. Nichols, D.P., Chmiel, J.F., Inflammation and its genesis in cystic fibrosis. Pediatr. Pulmonol. 50:Suppl. 40 (2015), S39–S56, 10.1002/ppul.23242.
104. Ojoo, J.C., Mulrennan, S.A., Kastelik, J.A., Morice, A.H., Redington, A.E., Exhaled breath condensate pH and exhaled nitric oxide in allergic asthma and in cystic fibrosis. Thorax 60 (2005), 22–26, 10.1136/thx.2003.017327.
105. Orlowski, J., Grinstein, S., Na+/H+ exchangers. Compr. Physiol. 1 (2011), 2083–2100, 10.1002/cphy.c110020.
106. Ostedgaard, L.S., Meyerholz, D.K., Chen, J.H., Pezzulo, A.A., Karp, P.H., Rokhlina, T., Ernst, S.E., Hanfland, R.A., Reznikov, L.R., Ludwig, P.S., Rogan, M.P., Davis, G.J., Dohrn, C.L., Wohlford-Lenane, C., Taft, P.J., Rector, M.V., Hornick, E., Nassar, B.S., Samuel, M., Zhang, Y., Richter, S.S., Uc, A., Shilyansky, J., Prather, R.S., McCray, P.B. Jr., Zabner, J., Welsh, M.J., Stoltz, D.A., The DeltaF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs. Sci. Transl. Med., 3, 2011, 74ra, 10.1126/scitranslmed.3001868.
107. Park, M., Ko, S.B., Choi, J.Y., Muallem, G., Thomas, P.J., Pushkin, A., Lee, M.S., Kim, J.Y., Lee, M.G., Muallem, S., Kurtz, I., The cystic fibrosis transmembrane conductance regulator interacts with and regulates the activity of the HCO3- salvage transporter human Na+-HCO3- cotransport isoform 3. J. Biol. Chem. 277 (2002), 50503–50509, 10.1074/jbc.M201862200.
108. Pezzulo, A.A., Starner, T.D., Scheetz, T.E., Traver, G.L., Tilley, A.E., Harvey, B.G., Crystal, R.G., McCray, P.B. Jr., Zabner, J., The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 300 (2011), L25–L31, 10.1152/ajplung.00256.2010.
109. Pezzulo, A.A., Tang, X.X., Hoegger, M.J., Abou Alaiwa, M.H., Ramachandran, S., Moninger, T.O., Karp, P.H., Wohlford-Lenane, C.L., Haagsman, H.P., van Eijk, M., Banfi, B., Horswill, A.R., Stoltz, D.A., McCray, P.B. Jr., Welsh, M.J., Zabner, J., Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487 (2012), 109–113, 10.1038/nature11130.
110. Poulsen, J.H., Fischer, H., Illek, B., Machen, T.E., Bicarbonate conductance and pH regulatory capability of cystic fibrosis transmembrane conductance regulator. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 5340–5344, 10.1073/pnas.91.12.5340.
111. Prescott, S.A., Synaptic inhibition and disinhibition in the spinal dorsal horn. Prog. Mol. Biol. Transl. Sci. 131 (2015), 359–383, 10.1016/bs.pmbts.2014.11.008.
112. Quinton, P.M., Chloride impermeability in cystic fibrosis. Nature 301 (1983), 421–422, 10.1038/301421a0.
113. Quinton, P.M., Missing Cl conductance in cystic fibrosis. Am. J. Physiol. 251 (1986), C649–652, 10.1152/ajpcell.1986.251.4.C649.
114. Quinton, P.M., Defective epithelial ion transport in cystic fibrosis. Clin. Chem. 35 (1989), 726–730.
115. Quinton, P.M., Role of epithelial HCO3(-) transport in mucin secretion: lessons from cystic fibrosis. Am. J. Physiol. Cell Physiol. 299 (2010), C1222–1233, 10.1152/ajpcell.00362.2010.
116. Ralhan, A., Laval, J., Lelis, F., Ballbach, M., Grund, C., Hector, A., Hartl, D., Current concepts and controversies in innate immunity of cystic fibrosis lung disease. J. Innate Immun. 8 (2016), 531–540, 10.1159/000446840.
117. Reddy, M.M., Kopito, R.R., Quinton, P.M., Cytosolic pH regulates GCl through control of phosphorylation states of CFTR. Am. J. Physiol. 275 (1998), C1040–C1047, 10.1152/ajpcell.1998.275.4.C1040.
118. Regan, K.H., Bhatt, J., Eradication therapy for Burkholderia cepacia complex in people with cystic fibrosis. Cochrane Database Syst. Rev., 11, 2016, CD009876, 10.1002/14651858.CD009876.pub3.
119. Riordan, J.R., CFTR function and prospects for therapy. Annu. Rev. Biochem. 77 (2008), 701–726, 10.1146/annurev.biochem.75.103004.142532.
120. Riordan, J.R., Rommens, J.M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J.L., et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245 (1989), 1066–1073, 10.1126/science.2475911.
121. Rogan, M.P., Stoltz, D.A., Hornick, D.B., Cystic fibrosis transmembrane conductance regulator intracellular processing, trafficking, and opportunities for mutation-specific treatment. Chest 139 (2011), 1480–1490, 10.1378/chest.10-2077.
122. Rogers, C.S., Hao, Y., Rokhlina, T., Samuel, M., Stoltz, D.A., Li, Y., Petroff, E., Vermeer, D.W., Kabel, A.C., Yan, Z., Spate, L., Wax, D., Murphy, C.N., Rieke, A., Whitworth, K., Linville, M.L., Korte, S.W., Engelhardt, J.F., Welsh, M.J., Prather, R.S., Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. J. Clin. Invest. 118 (2008), 1571–1577, 10.1172/JCI34773.
123. Rogers, C.S., Stoltz, D.A., Meyerholz, D.K., Ostedgaard, L.S., Rokhlina, T., Taft, P.J., Rogan, M.P., Pezzulo, A.A., Karp, P.H., Itani, O.A., Kabel, A.C., Wohlford-Lenane, C.L., Davis, G.J., Hanfland, R.A., Smith, T.L., Samuel, M., Wax, D., Murphy, C.N., Rieke, A., Whitworth, K., Uc, A., Starner, T.D., Brogden, K.A., Shilyansky, J., McCray, P.B. Jr., Zabner, J., Prather, R.S., Welsh, M.J., Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321 (2008), 1837–1841, 10.1126/science.1163600.
124. Rotstein, O.D., Interactions between leukocytes and anaerobic bacteria in polymicrobial surgical infections. Clin. Infect. Dis. 16:Suppl. 4 (1993), S190–S194, 10.1093/clinids/16.Supplement_4.S190.
125. Ruffin, V.A., Salameh, A.I., Boron, W.F., Parker, M.D., Intracellular pH regulation by acid-base transporters in mammalian neurons. Front. Physiol., 5, 2014, 43, 10.3389/fphys.2014.00043.
126. Sanhueza, C., Araos, J., Naranjo, L., Barros, E., Subiabre, M., Toledo, F., Gutierrez, J., Chiarello, D.I., Pardo, F., Leiva, A., Sobrevia, L., Nitric oxide and pH modulation in gynaecological cancer. J. Cell. Mol. Med. 20 (2016), 2223–2230, 10.1111/jcmm.12921.
127. Savant, A.P., McColley, S.A., Cystic fibrosis year in review 2016. Pediatr. Pulmonol. 52 (2017), 1092–1102, 10.1002/ppul.23747.
128. Schultz, B.D., Airway epithelial cells:’ Bicarbonate in’ not equal’ Bicarbonate out’. J. Physiol. 590 (2012), 5263–5264, 10.1113/jphysiol.2012.242586.
129. Schultz, A., Puvvadi, R., Borisov, S.M., Shaw, N.C., Klimant, I., Berry, L.J., Montgomery, S.T., Nguyen, T., Kreda, S.M., Kicic, A., Noble, P.B., Button, B., Stick, S.M., Airway surface liquid pH is not acidic in children with cystic fibrosis. Nat. Commun., 8, 2017, 1409, 10.1038/s41467-017-00532-5.
130. Schwerdt, M., Neumann, C., Schwartbeck, B., Kampmeier, S., Herzog, S., Görlich, D., Dübbers, A., Große-Onnebrink, J., Kessler, C., Küster, P., Schültingkemper, H., Treffon, J., Peters, G., Kahl, B.C., Staphylococcus aureus in the airways of cystic fibrosis patients - a retrospective long-term study. Int. J. Med. Microbiol., 2018, 10.1016/j.ijmm.2018.02.003 pii: S1438-4221(17)30448-4.
131. Schwiebert, E.M., Cid-Soto, L.P., Stafford, D., Carter, M., Blaisdell, C.J., Zeitlin, P.L., Guggino, W.B., Cutting, G.R., Analysis of ClC-2 channels as an alternative pathway for chloride conduction in cystic fibrosis airway cells. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 3879–3884, 10.1073/pnas.95.7.3879.
132. Seifter, J.L., Chang, H.Y., Extracellular acid-Base balance and ion transport between body fluid compartments. Physiology (Bethesda) 32 (2017), 367–379, 10.1152/physiol.00007.2017.
133. Shah, V.S., Meyerholz, D.K., Tang, X.X., Reznikov, L., Abou Alaiwa, M., Ernst, S.E., Karp, P.H., Wohlford-Lenane, C.L., Heilmann, K.P., Leidinger, M.R., Allen, P.D., Zabner, J., McCray, P.B. Jr., Ostedgaard, L.S., Stoltz, D.A., Randak, C.O., Welsh, M.J., Airway acidification initiates host defense abnormalities in cystic fibrosis mice. Science 351 (2016), 503–507, 10.1126/science.aad5589.
134. Shamsuddin, A.K., Quinton, P.M., Native small airways secrete bicarbonate. Am. J. Respir. Cell Mol. Biol. 50 (2014), 796–804, 10.1165/rcmb.2013-0418OC.
135. Shan, J., Liao, J., Huang, J., Robert, R., Palmer, M.L., Fahrenkrug, S.C., O'Grady, S.M., Hanrahan, J.W., Bicarbonate-dependent chloride transport drives fluid secretion by the human airway epithelial cell line Calu-3. J. Physiol. 590 (2012), 5273–5297, 10.1113/jphysiol.2012.236893.
136. Shcheynikov, N., Yang, D., Wang, Y., Zeng, W., Karniski, L.P., So, I., Wall, S.M., Muallem, S., The Slc26a4 transporter functions as an electroneutral Cl-/I-/HCO3- exchanger: role of Slc26a4 and Slc26a6 in I- and HCO3- secretion and in regulation of CFTR in the parotid duct. J. Physiol. 586 (2008), 3813–3824, 10.1113/jphysiol.2008.154468.
137. Sherry, A.M., Cuppoletti, J., Malinowska, D.H., Differential acidic pH sensitivity of delta F508 CFTR Cl- channel activity in lipid bilayers. Am. J. Physiol. 266 (1994), C870–875, 10.1152/ajpcell.1994.266.3.C870.
138. Smith, J.J., Welsh, M.J., Fluid and electrolyte transport by cultured human airway epithelia. J. Clin. Invest. 91 (1993), 1590–1597, 10.1172/jci116365.
139. Smith, J.J., Travis, S.M., Greenberg, E.P., Welsh, M.J., Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85 (1996), 229–236, 10.1016/S0092-8674(00)81099-5.
140. Snell, G., Reed, A., Stern, M., Hadjiliadis, D., The evolution of lung transplantation for cystic fibrosis: a 2017 update. J Cyst. Fibros. 16 (2017), 553–564, 10.1016/j.jcf.2017.06.008.
141. Soleti, R., Porro, C., Martinez, M.C., Apoptotic process in cystic fibrosis cells. Apoptosis 18 (2013), 1029–1038, 10.1007/s10495-013-0874-y.
142. Song, Y., Salinas, D., Nielson, D.W., Verkman, A.S., Hyperacidity of secreted fluid from submucosal glands in early cystic fibrosis. Am. J. Physiol. Cell Physiol. 290 (2006), C741–749, 10.1152/ajpcell.00379.2005.
143. Spiegel, S., Phillipper, M., Rossmann, H., Riederer, B., Gregor, M., Seidler, U., Independence of apical Cl-/HCO3- exchange and anion conductance in duodenal HCO3- secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 285 (2003), G887–897, 10.1152/ajpgi.00083.2003.
144. Sporn, M.B., Roberts, A.B., Autocrine growth factors and cancer. Nature 313 (1985), 745–747, 10.1038/313745a0.
145. Srivastava, M., Eidelman, O., Pollard, H.B., Pharmacogenomics of the cystic fibrosis transmembrane conductance regulator (CFTR) and the cystic fibrosis drug CPX using genome microarray analysis. Mol. Med. 5 (1999), 753–767.
146. Srivastava, M., Eidelman, O., Pollard, H.B., cDNA microarrays for pharmacogenomic analysis of cystic fibrosis. Methods Mol. Med. 70 (2002), 21–29, 10.1385/1-59259-187-6:21.
147. Starner, T.D., Zhang, N., Kim, G., Apicella, M.A., McCray, P.B. Jr., Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am. J. Respir. Crit. Care Med. 174 (2006), 213–220, 10.1164/rccm.200509-1459OC.
148. Taminelli, G.L., Sotomayor, V., Valdivieso, A.G., Teiber, M.L., Marin, M.C., Santa-Coloma, T.A., CISD1 codifies a mitochondrial protein upregulated by the CFTR channel. Biochem. Biophys. Res. Commun. 365 (2008), 856–862, 10.1016/j.bbrc.2007.11.076.
149. Tang, X.X., Ostedgaard, L.S., Hoegger, M.J., Moninger, T.O., Karp, P.H., McMenimen, J.D., Choudhury, B., Varki, A., Stoltz, D.A., Welsh, M.J., Acidic pH increases airway surface liquid viscosity in cystic fibrosis. J. Clin. Invest. 126 (2016), 879–891, 10.1172/jci83922.
150. Tate, S., MacGregor, G., Davis, M., Innes, J.A., Greening, A.P., Airways in cystic fibrosis are acidified: detection by exhaled breath condensate. Thorax 57 (2002), 926–929, 10.1136/thorax.57.11.926.
151. Valdivieso, A.G., Santa-Coloma, T.A., CFTR activity and mitochondrial function. Redox Biol. 1 (2013), 190–202, 10.1016/j.redox.2012.11.007.
152. Valdivieso, A.G., Marcucci, F., Taminelli, G., Guerrico, A.G., Alvarez, S., Teiber, M.L., Dankert, M.A., Santa-Coloma, T.A., The expression of the mitochondrial gene MTND4 is downregulated in cystic fibrosis. Biochem. Biophys. Res. Commun. 356 (2007), 805–809, 10.1016/j.bbrc.2007.03.057.
153. Valdivieso, A.G., Clauzure, M., Marin, M.C., Taminelli, G.L., Massip Copiz, M.M., Sanchez, F., Schulman, G., Teiber, M.L., Santa-Coloma, T.A., The mitochondrial complex I activity is reduced in cells with impaired cystic fibrosis transmembrane conductance regulator (CFTR) function. PLoS One, 7, 2012, e48059, 10.1371/journal.pone.0048059.
154. Valdivieso, A.G., Clauzure, M., Massip-Copiz, M., Santa-Coloma, T.A., The chloride anion acts as a second messenger in mammalian cells - modifying the expression of specific genes. Cell. Physiol. Biochem. 38 (2016), 49–64, 10.1159/000438608.
155. Valdivieso, A.G., Mori, C., Clauzure, M., Massip-Copiz, M., Santa-Coloma, T.A., CFTR modulates RPS27 gene expression using chloride anion as signaling effector. Arch. Biochem. Biophys. 633 (2017), 103–109, 10.1016/j.abb.2017.09.014.
156. Veit, G., Avramescu, R.G., Chiang, A.N., Houck, S.A., Cai, Z., Peters, K.W., Hong, J.S., Pollard, H.B., Guggino, W.B., Balch, W.E., Skach, W.R., Cutting, G.R., Frizzell, R.A., Sheppard, D.N., Cyr, D.M., Sorscher, E.J., Brodsky, J.L., Lukacs, G.L., From CFTR biology toward combinatorial pharmacotherapy: expanded classification of cystic fibrosis mutations. Mol. Biol. Cell 27 (2016), 424–433, 10.1091/mbc.E14-04-0935.
157. Villella, V.R., Esposito, S., Bruscia, E.M., Maiuri, M.C., Raia, V., Kroemer, G., Maiuri, L., Targeting the intracellular environment in cystic fibrosis: restoring autophagy as a novel strategy to circumvent the CFTR defect. Front. Pharmacol., 4, 2013, 1, 10.3389/fphar.2013.00001.
158. Wang, X.F., Zhou, C.X., Shi, Q.X., Yuan, Y.Y., Yu, M.K., Ajonuma, L.C., Ho, L.S., Lo, P.S., Tsang, L.L., Liu, Y., Lam, S.Y., Chan, L.N., Zhao, W.C., Chung, Y.W., Chan, H.C., Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat. Cell Biol. 5 (2003), 902–906, 10.1038/ncb1047.
159. Wang, Y., Soyombo, A.A., Shcheynikov, N., Zeng, W., Dorwart, M., Marino, C.R., Thomas, P.J., Muallem, S., Slc26a6 regulates CFTR activity in vivo to determine pancreatic duct HCO3- secretion: relevance to cystic fibrosis. EMBO J. 25 (2006), 5049–5057, 10.1038/sj.emboj.7601387.
160. Wang, Y., Wrennall, J.A., Cai, Z., Li, H., Sheppard, D.N., Understanding how cystic fibrosis mutations disrupt CFTR function: from single molecules to animal models. Int. J. Biochem. Cell Biol. 52 (2014), 47–57, 10.1016/j.biocel.2014.04.001.
161. Wiencek, J.R., Lo, S.F., Advances in the diagnosis and management of cystic fibrosis in the genomic era. Clin. Chem. 64 (2018), 898–908, 10.1373/clinchem.2017.274670.
162. Wine, J.J., The genesis of cystic fibrosis lung disease. J. Clin. Invest. 103 (1999), 309–312, 10.1172/jci6222.
163. Wong, J.K., Ranganathan, S.C., Hart, E., Australian Respiratory Early Surveillance Team for Cystic, F, Staphylococcus aureus in early cystic fibrosis lung disease. Pediatr. Pulmonol. 48 (2013), 1151–1159, 10.1002/ppul.22863.
164. Xu, Y., Clark, J.C., Aronow, B.J., Dey, C.R., Liu, C., Wooldridge, J.L., Whitsett, J.A., Transcriptional adaptation to cystic fibrosis transmembrane conductance regulator deficiency. J. Biol. Chem. 278 (2003), 7674–7682, 10.1074/jbc.M210277200.
165. Ye, X., Lotan, R., Potential misinterpretation of data on differential gene expression in normal and malignant cells in vitro. Brief. Funct. Genomic Proteomic 7 (2008), 322–326, 10.1093/bfgp/eln021.
166. Yu, K., Lujan, R., Marmorstein, A., Gabriel, S., Hartzell, H.C., Bestrophin-2 mediates bicarbonate transport by goblet cells in mouse colon. J. Clin. Invest. 120 (2010), 1722–1735, 10.1172/jci41129.
167. Zabner, J., Smith, J.J., Karp, P.H., Widdicombe, J.H., Welsh, M.J., Loss of CFTR chloride channels alters salt absorption by cystic fibrosis airway epithelia in vitro. Mol. Cell 2 (1998), 397–403, 10.1016/S1097-2765(00)80284-1.
168. Ziady, A.G., Hansen, J., Redox balance in cystic fibrosis. Int. J. Biochem. Cell Biol. 52 (2014), 113–123, 10.1016/j.biocel.2014.03.006.