Electrolyte transport properties in distal small airways from cystic fibrosis pigs with implications for host defense

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 310, Issue 7, 2016, Pages L670-L679

  Li, Xiaopeng ^a   Tang, Xiao Xiao ^a,b   Vargas Buonfiglio, Luis G ^a   Comellas, Alejandro P ^a   Thornell, Ian M ^a,b   Ramachandran, Shyam ^a   Karp, Philip H ^a,b   Taft, Peter J ^a   Sheets, Kelsey ^a   Abou Alaiwa, Mahmoud H ^a   Welsh, Michael J ^a,b   Meyerholz, David K ^a   Stoltz, David A ^a,c   Zabner, Joseph ^a  

^a UNIVERSITY OF IOWA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c IA United States   (United States)

Author keywords

Cystic fibrosis transmembrane conductance regulator

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CHLORIDE ION; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ELECTROLYTE;

ADULT; AIRWAY; AIRWAY EPITHELIAL CELL; AIRWAY SURFACE LIQUID; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; ELECTROLYTE TRANSPORT; FEMALE; HISTOPATHOLOGY; HOST RESISTANCE; HUMAN; HUMIDITY; LUNG FIBROSIS; LUNG FLUID; MALE; NONHUMAN; PH; PIG; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPIRATORY AIRFLOW; RESPIRATORY EPITHELIUM; TRACHEA; ANIMAL; CELL CULTURE; GENETICS; IMMUNOLOGY; LUNG; LUNG ALVEOLUS EPITHELIUM CELL; METABOLISM; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ALVEOLAR EPITHELIAL CELLS; ANIMALS; BICARBONATES; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FEMALE; HYDROGEN-ION CONCENTRATION; LUNG; MALE; SUS SCROFA;

EID: 84984666933     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00422.2015     Document Type: Article

References (70)

1. Abou Alaiwa MH, Beer AM, Pezzulo AA, Launspach JL, Horan RA, Stoltz DA, Starner TD, Welsh MJ, Zabner J. Neonates with cystic fibrosis have a reduced nasal liquid pH; a small pilot study. J Cyst Fibros 13: 373-377, 2014.
2. Abou Alaiwa MH, Reznikov LR, Gansemer ND, Sheets KA, Horswill AR, Stoltz DA, Zabner J, Welsh MJ. pH modulates the activity and synergism of the airway surface liquid antimicrobials beta-defensin-3 and LL-37. Proc Natl Acad Sci USA 111: 18703-18708, 2014.
3. Adam RJ, Michalski AS, Bauer C, Abou Alaiwa MH, Gross TJ, Awadalla MS, Bouzek DC, Gansemer ND, Taft PJ, Hoegger MJ, Diwakar A, Ochs M, Reinhardt JM, Hoffman EA, Beichel RR, Meyerholz DK, Stoltz DA. Air trapping and airflow obstruction in newborn cystic fibrosis piglets. Am J Respir Crit Care Med 188: 1434-1441, 2013.
4. - and Na+-H+ exchangers in human airways epithelium. JOP 2: 285-290, 2001.
5. Asmundsson T, Kilburn KH. Mucociliary clearance rates at various levels in dog lungs. Am Rev Respir Dis 102: 388-397, 1970.
6. Bakker EM, Borsboom GJ, van der Wiel-Kooij EC, Caudri D, Rosenfeld M, Tiddens HA. Small airway involvement in cystic fibrosis lung disease: routine spirometry as an early and sensitive marker. Pediatr Pulmonol 48: 1081-1088 2013.
7. Ballard ST, Fountain JD, Inglis SK, Corboz MR, Taylor AE. Chloride secretion across distal airway epithelium: relationship to submucosal gland distribution. Am J Physiol Lung Cell Mol Physiol 268: L526-L531, 1995.
8. Ballard ST, Schepens SM, Falcone JC, Meininger GA, Taylor AE. Regional bioelectric properties of porcine airway epithelium. J Appl Physiol 73: 2021-2027, 1992.
9. Bedrossian CW, Greenberg SD, Singer DB, Hansen JJ, Rosenberg HS. The lung in cystic fibrosis. A quantitative study including prevalence of pathologic findings among different age groups. Hum Pathol 7: 195-204, 1976.
10. Bertrand CA, Zhang R, Pilewski JM, Frizzell RA. SLC26A9 is a constitutively active, CFTR-regulated anion conductance in human bronchial epithelia. J Gen Physiol 133: 421-438, 2009.
11. Blouquit-Laye S, Chinet T. Ion and liquid transport across the bronchiolar epithelium. Respir Physiol Neurobiol 159: 278-282, 2007.
12. Blouquit-Laye S, Dannhoffer L, Braun C, Dinh-Xuan AT, Sage E, Chinet T. Effect of nitric oxide on epithelial ion transports in noncystic fibrosis and cystic fibrosis human proximal and distal airways. Am J Physiol Lung Cell Mol Physiol 303: L617-L625, 2012.
13. Blouquit S, Regnier A, Dannhoffer L, Fermanian C, Naline E, Boucher R, Chinet T. Ion and fluid transport properties of small airways in cystic fibrosis. Am J Respir Crit Care Med 174: 299-305, 2006.
14. Boucher RC. Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 13: 231-240, 2007.
15. Boucher RC. Evidence for airway surface dehydration as the initiating event in CF airway disease. J Intern Med 261: 5-16, 2007.
16. Bove PF, Dang H, Cheluvaraju C, Jones LC, Liu X, O’Neal WK, Randell SH, Schlegel R, Boucher RC. Breaking the in vitro alveolar type II cell proliferation barrier while retaining ion transport properties. Am J Respir Cell Mol Biol 50: 767-776, 2014.
17. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322: 590-594, 2008.
18. Chang EH, Tang XX, Shah VS, Launspach JL, Ernst SE, Hilkin B, Karp PH, Abou Alaiwa MH, Graham SM, Hornick DB, Welsh MJ, Stoltz DA, Zabner J. Medical reversal of chronic sinusitis in a cystic fibrosis patient with ivacaftor. Int Forum Allergy Rhinol 5: 178-181, 2015.
19. Chen JH, Stoltz DA, Karp PH, Ernst SE, Pezzulo AA, Moninger TO, Rector MV, Reznikov LR, Launspach JL, Chaloner K, Zabner J, Welsh MJ. Loss of anion transport without increased sodium absorption characterizes newborn porcine cystic fibrosis airway epithelia. Cell 143: 911-923, 2011.
20. Coakley RD, Grubb BR, Paradiso AM, Gatzy JT, Johnson LG, Kreda SM, O’Neal WK, Boucher RC. Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc Natl Acad Sci USA 100: 16083-16088, 2003.
21. Crouch E, Parghi D, Kuan SF, Persson A. Surfactant protein D: Subcellular localization in nonciliated bronchiolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 263: L60-L66, 1992.
22. Devor DC, Bridges RJ, Pilewski JM. Pharmacological modulation of ion transport across wild-type and DeltaF508 CFTR-expressing human bronchial epithelia. Am J Physiol Cell Physiol 279: C461-C479, 2000.
23. Engelhardt JF, Zepeda M, Cohn JA, Yankaskas JR, Wilson JM. Expression of the cystic fibrosis gene in adult human lung. J Clin Invest 93: 737-749, 1994.
24. Fischer H, Widdicombe JH. Mechanisms of acid and base secretion by the airway epithelium. J Membr Biol 211: 139-150, 2006.
25. Fishman AP. Structure and function. In: Pulmonary Diseases and Disorders. New York, NY: McGraw-Hill, 1988.
26. Garnett JP, Hickman E, Burrows R, Hegyi P, Tiszlavicz L, Cuthbert AW, Fong P, Gray MA. Novel role for pendrin in orchestrating bicarbonate secretion in cystic fibrosis transmembrane conductance regulator (CFTR)-expressing airway serous cells. J Biol Chem 286: 41069-41082, 2011.
27. Gavriely N, Eckmann DM, Grotberg JB. Intra-airway gas transport during high-frequency chest vibration with tracheal insufflation in dogs. J Appl Physiol 79: 243-250, 1995.
28. Grubb BR, Boucher RC. Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol Rev 79: S193-S214, 1999.
29. Herias MV, Hogenkamp A, van Asten AJ, Tersteeg MH, van Eijk M, Haagsman HP. Expression sites of the collectin SP-D suggest its importance in first line host defence: power of combining in situ hybridisation, RT-PCR and immunohistochemistry. Mol Immunol 44: 3324-3332, 2007.
30. Hoegger MJ, Fischer AJ, McMenimen JD, Ostedgaard LS, Tucker AJ, Awadalla MA, Moninger TO, Michalski AS, Hoffman EA, Zabner J, Stoltz DA, Welsh MJ. Impaired mucus detachment disrupts mucociliary transport in a piglet model of cystic fibrosis. Science 345: 818-822, 2014.
31. Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med 278: 1355-1360, 1968.
32. Hug MJ, Tamada T, Bridges RJ. CFTR and bicarbonate secretion by [correction of to] epithelial cells. News Physiol Sci 18: 38-42, 2003.
33. Itani OA, Chen JH, Karp PH, Ernst S, Keshavjee S, Parekh K, Klesney-Tait J, Zabner J, Welsh MJ. Human cystic fibrosis airway epithelia have reduced Cl-conductance but not increased Na+ conductance. Proc Natl Acad Sci USA 108: 10260-10265, 2011.
34. Jegalian BG, De Robertis EM. Homeotic transformations in the mouse induced by overexpression of a human Hox3.3 transgene. Cell 71: 901-910, 1992.
35. Joris L, Dab I, Quinton PM. Elemental composition of human airway surface fluid in healthy and diseased airways. Am Rev Respir Dis 148: 1633-1637, 1993.
36. Keiser NW, Birket SE, Evans IA, Tyler SR, Crooke AK, Sun X, Zhou W, Nellis JR, Stroebele EK, Chu KK, Tearney GJ, Stevens MJ, Harris JK, Rowe SM, Engelhardt JF. Defective innate immunity and hyperinflammation in newborn cystic fibrosis transmembrane conductance regulator-knockout ferret lungs. Am J Respir Cell Mol Biol 52: 683-694, 2015.
37. Kreda SM, Gynn MC, Fenstermacher DA, Boucher RC, Gabriel SE. Expression and localization of epithelial aquaporins in the adult human lung. Am J Respir Cell Mol Biol 24: 224-234, 2001.
38. Li X, Comellas AP, Karp PH, Ernst SE, Moninger TO, Gansemer ND, Taft PJ, Pezzulo AA, Rector MV, Rossen N, Stoltz DA, McCray PB Jr, Welsh MJ, Zabner J. CFTR is required for maximal transepithelial liquid transport in pig alveolar epithelia. Am J Physiol Lung Cell Mol Physiol 303: L152-L160, 2012.
39. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, Haddad BR, Rhim JS, Dritschilo A, Riegel A, McBride A, Schlegel R. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol 180: 599-607, 2012.
40. Madsen J, Kliem A, Tornoe I, Skjodt K, Koch C, Holmskov U. Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol 164: 5866-5870, 2000.
41. Oppenheimer EH, Esterly JR. Pathology of cystic fibrosis review of the literature and comparison with 146 autopsied cases. Perspect Pediatr Pathol 2: 241-278, 1975.
42. Ostedgaard LS, Meyerholz DK, Chen JH, Pezzulo AA, Karp PH, Rokhlina T, Ernst SE, Hanfland RA, Reznikov LR, Ludwig PS, Rogan MP, Davis GJ, Dohrn CL, Wohlford-Lenane C, Taft PJ, Rector MV, Hornick E, Nassar BS, Samuel M, Zhang Y, Richter SS, Uc A, Shilyansky J, Prather RS, McCray PB Jr, Zabner J, Welsh MJ, Stoltz DA. The DeltaF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs. Sci Transl Med 3: 24-74, 2011.
43. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, Banfi B, Horswill AR, Stoltz DA, McCray PB Jr, Welsh MJ, Zabner J. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487: 109-113, 2012.
44. Piacentini S, Polimanti R, Iorio A, Cortesi M, Papa F, Rongioletti M, Liumbruno GM, Manfellotto D, Fuciarelli M. GSTA1*-69C/T and GSTO2*N142D as asthma-and allergy-related risk factors in Italian adult patients. Clin Exp Pharmacol Physiol 41: 180-184, 2014.
45. Quinton PM. Cystic fibrosis: impaired bicarbonate secretion and mucoviscidosis. Lancet 372: 415-417, 2008.
46. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6: 331-343, 1975.
47. Rogers CS, Abraham WM, Brogden KA, Engelhardt JF, Fisher JT, McCray PB Jr, McLennan G, Meyerholz DK, Namati E, Ostedgaard LS, Prather RS, Sabater JR, Stoltz DA, Zabner J, Welsh MJ. The porcine lung as a potential model for cystic fibrosis. Am J Physiol Lung Cell Mol Physiol 295: L240-L263, 2008.
48. Rogers CS, Stoltz DA, Meyerholz DK, Ostedgaard LS, Rokhlina T, Taft PJ, Rogan MP, Pezzulo AA, Karp PH, Itani OA, Kabel AC, Wohlford-Lenane CL, Davis GJ, Hanfland RA, Smith TL, Samuel M, Wax D, Murphy CN, Rieke A, Whitworth K, Uc A, Starner TD, Brogden KA, Shilyansky J, McCray PB Jr, Zabner J, Prather RS, Welsh MJ. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321: 1837-1841, 2008.
49. Schroeder BC, Cheng T, Jan YN, Jan LY. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134: 1019-1029, 2008.
50. Shamsuddin AK, Quinton PM. Native small airways secrete bicarbonate. Am J Respir Cell Mol Biol 50: 796-804, 2014.
51. Shamsuddin AK, Quinton PM. Surface fluid absorption and secretion in small airways. J Physiol 590: 3561-3574, 2012.
52. Sheppard DN, Welsh MJ. Structure and function of the CFTR chloride channel. Physiol Rev 79: S23-S45, 1999.
53. Skovgaard K, Mortensen S, Boye M, Hedegaard J, Heegaard PM. Hepatic gene expression changes in pigs experimentally infected with the lung pathogen Actinobacillus pleuropneumoniae as analysed with an innate immunity focused microarray. Innate Immun 16: 343-353, 2010.
54. Smith JJ, Karp PH, Welsh MJ. Defective fluid transport by cystic fibrosis airway epithelia. J Clin Invest 93: 1307-1311, 1994.
55. Smith JJ, Travis SM, Greenberg EP, Welsh MJ. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85: 229-236, 1996.
56. Smith JJ, Welsh MJ. cAMP stimulates bicarbonate secretion across normal, but not cystic fibrosis airway epithelia. J Clin Invest 89: 1148-1153, 1992.
57. Smith JJ, Welsh MJ. Fluid and electrolyte transport by cultured human airway epithelia. J Clin Invest 91: 1590-1597, 1993.
58. Sobonya RE, Taussig LM. Quantitative aspects of lung pathology in cystic fibrosis. Am Rev Respir Dis 134: 290-295, 1986.
59. Song Y, Salinas D, Nielson DW, Verkman AS. Hyperacidity of secreted fluid from submucosal glands in early cystic fibrosis. Am J Physiol Cell Physiol 290: C741-C749, 2006.
60. Stoltz DA, Meyerholz DK, Pezzulo AA, Ramachandran S, Rogan MP, Davis GJ, Hanfland RA, Wohlford-Lenane C, Dohrn CL, Bartlett JA, Nelson GAt Chang EH, Taft PJ, Ludwig PS, Estin M, Hornick EE, Launspach JL, Samuel M, Rokhlina T, Karp PH, Ostedgaard LS, Uc A, Starner TD, Horswill AR, Brogden KA, Prather RS, Richter SS, Shilyansky J, McCray PB Jr, Zabner J, Welsh MJ. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2: 29-31, 2010.
61. Stoltz DA, Meyerholz DK, Welsh MJ. Origins of cystic fibrosis lung disease. N Engl J Med 372: 351-362, 2015.
62. Stoltz DA, Rokhlina T, Ernst SE, Pezzulo AA, Ostedgaard LS, Karp PH, Samuel MS, Reznikov LR, Rector MV, Gansemer ND, Bouzek DC, Alaiwa MH, Hoegger MJ, Ludwig PS, Taft PJ, Wallen TJ, Wohlford-Lenane C, McMenimen JD, Chen JH, Bogan KL, Adam RJ, Hornick EE, Nelson GAt Hoffman EA, Chang EH, Zabner J, McCray PB Jr, Prather RS, Meyerholz DK, Welsh MJ. Intestinal CFTR expression alleviates meconium ileus in cystic fibrosis pigs. J Clin Invest 123: 2685-2693, 2013.
63. Suprynowicz FA, Upadhyay G, Krawczyk E, Kramer SC, Hebert JD, Liu X, Yuan H, Cheluvaraju C, Clapp PW, Boucher RC Jr, Kamonjoh CM, Randell SH, Schlegel R. Conditionally reprogrammed cells represent a stem-like state of adult epithelial cells. Proc Natl Acad Sci USA 109: 20035-20040, 2012.
64. Tang XX, Ostedgaard LS, Hoegger MJ, Moninger TO, Karp PH, McMenimen JD, Choudhury B, Varki A, Stoltz DA, Welsh MJ. Acidic pH increases airway surface liquid viscosity in cystic fibrosis. J Clin Invest In press.
65. Tiddens HA, Donaldson SH, Rosenfeld M, Pare PD. Cystic fibrosis lung disease starts in the small airways: can we treat it more effectively? Pediatr Pulmonol 45: 107-117, 2010.
66. Wang X, Lytle C, Quinton PM. Predominant constitutive CFTR conductance in small airways. Respir Res 6: 7, 2005.
67. Weibel ER. Morphometry of the Human Lung. Berlin, Germany: Springer-Verlag, 1963.
68. Widdicombe JH, Wine JJ. Airway Gland Structure and Function. Physiol Rev 95: 1241-1319, 2015.
69. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455: 1210-1215, 2008.
70. Zabner J, Wadsworth SC, Smith AE, Welsh MJ. Adenovirus-mediated generation of cAMP-stimulated Cl-transport in cystic fibrosis airway epithelia in vitro: effect of promoter and administration method. Gene Ther 3: 458-465, 1996.