Skip to main content

Development of Lung Epithelial Ion Transport: Implications for Neonatal Lung Disease

  • Chapter
Lung Development

Part of the book series: Clinical Physiology Series ((CLINPHY))

  • 229 Accesses

Abstract

At birth, the lungs must immediately assume the essential job of gas exchange. There are many associated environmental changes taking place at birth, including an approximate fivefold increase in partial pressure of oxygen (PO2) as air-breathing commences, and tenfold increase in the pulmonary blood flow. For a successful transition to postnatal life, the lungs must also have developed a structural interface between the capillary microcirculation and the epithelium, have a robust antioxidant enzyme defence, and have mature synthetic pathways for surfactant synthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acarregui, M.J., J.J.Brown, and R.K. Mallampalli. Oxygen modulates surfactant protein mRNA expression and phospholipid production in human fetal lung in vitro. Am. J. Physiol. 268: L818 - L825, 1995.

    PubMed  CAS  Google Scholar 

  2. Acarregui, M.J., J.M.Snyder, and C.R. Mendelson. Oxygen modulates the differentiation of human fetal lung in vitro and its responsiveness to cAMP. Am. J. Physiol. 264: L465 - L474, 1993.

    PubMed  CAS  Google Scholar 

  3. Adams, F.H., T. Fujiwara, and G. Rowshan. The nature and origin of the fluid in fetal lamb lung. J. Pediatr. 63: 881–888, 1963.

    Article  PubMed  CAS  Google Scholar 

  4. Adams, F.H., M. Yanagisawa, D. Kuzela, and H. Martinek. The disappearance of fetal lung fluid following birth. J. Pediatr. 78: 837–843, 1971.

    Article  PubMed  CAS  Google Scholar 

  5. Adamson, I.Y.R. Alveolar injury and repair. In: Electron microscopy of the lung, edited by D.E. Schraufnagel. New York: Marcel Dekker, 1990, p. 149–176.

    Google Scholar 

  6. Adamson, I.Y.R. Development of lung structure. In: The Lung: Scientific Foundations, edited by R.G. Crystal, J.B. West, et al. New York: Raven Press, 1991, p. 663–670.

    Google Scholar 

  7. Adamson, T.M., R.D.H. Boyd, H.S. Platt, and L.B. Strang. Composition of alveolar liquid in the fetal lamb. J. Physiol. Lond. 204: 159–169, 1969.

    PubMed  CAS  Google Scholar 

  8. Adzick, N.S., M.R. Harrison, P.L. Glick, R.L. Villa, and W. Finkbeiner. Experimental pulmonary hypoplasia and oligohydramnios: relative contributions of lung fluid and fetal breathing movements. J. Pediatr. Surg. 19: 658–665, 1984

    Article  PubMed  CAS  Google Scholar 

  9. Alcorn, D., T.M. Adamson, T.F. Lambert, J.E. Maloney, B.C. Ritchie, and P.M. Robinson. Morphological effects of chronic tracheal ligation and drainage in the fetal lamb lung. J. Anat. 123: 649–660, 1977.

    PubMed  CAS  Google Scholar 

  10. Ballard, S.T., R.C. Boucher, J.T Gatzy, E.M. Krochmal, and J.R. Yankaskas. Volume and ion transport by fetal rat alveolar and tracheal epithelia in submersion culture. Am. J. Physiol. 256: F397 - F407, 1989.

    PubMed  Google Scholar 

  11. Barker, P.M., R.C. Boucher, and J.R. Yankaskas. Bioelectric properties of cultured mono-layers from epithelium of distal human fetal lung. Am. J. Physiol. 268: L270 - L277, 1995.

    PubMed  CAS  Google Scholar 

  12. Barker, P.M., K.K. Brigman, A.M. Paradiso, R.C. Boucher, and J.T. Gatzy. Cl-secretion by trachea of CFTR (+/-) and (-/-) fetal mouse. Am. J. Respir. Cell Mol. Biol. 13: 307–313, 1995.

    Article  PubMed  CAS  Google Scholar 

  13. Barker, P.M., M.J. Brown, C.A. Ramsden, L.B. Strang, and D.V Walters. The effect of thyreoidectomy in the fetal sheep on lung liquid reabsorption induced by adrenaline or cyclic AMP. J. Physiol. Lond. 407: 373–383, 1988.

    PubMed  CAS  Google Scholar 

  14. Barker, P.M., and J.T. Gatzy. Effect of gas composition on liquid secretion by explants of distal lung fetal rat in submersion culture. Am. J. Physiol. (Lung Cell. Mol. Physiol.) 265: L512 - L517, 1993.

    CAS  Google Scholar 

  15. Barker, P.M., C.W. Gowen, E.E. Lawson, and M.R. Knowles. Decreased sodium ion absorption across nasal epithelium of very preterm infants with respiratory distress syndrome. J. Pediatr. 130: 373–377, 1997.

    Article  PubMed  CAS  Google Scholar 

  16. Barker, P.M., M. Markiewicz, K.A. Parker, D.V. Walters, and L.B. Strang. Synergistic action of triiodothyronine and hydrocortisone on epinephrine-induced reabsorption of fetal lung liquid. Pediatr. Res. 27: 588–591, 1990.

    Article  PubMed  CAS  Google Scholar 

  17. Barker, P.M., L.B. Strang, and D.V. Walters. The role of thyroid hormones in maturation of the adrenaline-sensitive lung liquid reabsorptive mechanism in fetal sheep. J. Physiol. Lond. 424: 473–485, 1990.

    PubMed  CAS  Google Scholar 

  18. Barker, P.M., D.V. Walters, M. Markiewicz, and L.B. Strang. Development of the lung liquid reabsorptive mechanism in fetal sheep: synergism of triiodothyronine and hydrocortisone. J. Physiol. Lond. 433: 435–449, 1991.

    PubMed  CAS  Google Scholar 

  19. Berry, D., A. Jobe, and M. Ikegami. Leakage of macromolecules in ventilated segments of preterm lamb lungs. J. Appl. Physiol. 70: 423129, 1991.

    Google Scholar 

  20. Bland, R.D. Lung epithelial ion transport and fluid movement during the perinatal period. Am. J. Physiol. 259: L30 - L37, 1990.

    PubMed  CAS  Google Scholar 

  21. Bland, R.D., and C.A.R. Boyd. Cation transport in lung epithelial cells derived from fetal, newborn, and adult rabbits. J. Appl. Physiol. 61: 507–515, 1986.

    PubMed  CAS  Google Scholar 

  22. Bland, R.D., M.A. Bressack, and D.D. McMillan. Labor decreases the lung water content of newborn rabbits. Am. J. Obstet. Gynecol. 135: 364–367, 1979.

    PubMed  CAS  Google Scholar 

  23. Bland, R.D., and D.W. Nielson. Developmental changes in lung liquid epithelial ion transport and liquid movement. Annu. Rev. Physiol. 54: 373–394, 1992.

    Article  PubMed  CAS  Google Scholar 

  24. Bland, R.D., D.D. McMillan, M.A. Bressack, and L. Dong. Clearance of liquid from lungs of newborn rabbits. J. Appl. Physiol. 49: 171–177, 1980.

    PubMed  CAS  Google Scholar 

  25. Brody, J.S., and M.C. Williams. Pulmonary alveolar epithelial cell differentiation. Annu. Rev. Physiol. 54: 351–371, 1992.

    Article  PubMed  CAS  Google Scholar 

  26. Brown, M.J., R.E. Olver, C.A. Ramsden, L.B. Strang, and D.V. Walters. Effects of adrenaline and of spontaneous labour on the secretion and absorption of lung liquid in the fetal lamb. J. Physiol. Lond. 344: 137–152, 1983.

    PubMed  CAS  Google Scholar 

  27. Burri, P.H. Fetal and postnatal development of the lung. Annu. Rev. Physiol. 46: 617–628, 1984.

    Article  PubMed  CAS  Google Scholar 

  28. Canessa, C.M., J.-D. Horisberger, and B.C. Rossier. Epithelial sodium channel related to proteins involved in neurodegeneration. Nature 361: 467–470, 1993.

    Article  PubMed  CAS  Google Scholar 

  29. Canessa, C.M., L. Schild, G. Buell, B. Thorens, I. Gautschi, J.-D. Horisberger, and B.C. Rossier. Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367: 463–467, 1994.

    Article  PubMed  CAS  Google Scholar 

  30. Carlton, D.P., J.J. Cummings, D.L. Chapman, F.R. Poulain, and R.D. Bland. Ion transport regulation of lung liquid secretion in foetal lambs. J. Dev. Physiol. 17: 99–107, 1992.

    PubMed  CAS  Google Scholar 

  31. Carlton, D.P., J.J. Cummings, R.G. Scheerer, F.R. Poulain, and R.D. Bland. Lung overex...pansion increases pulmonary microvascular protein permeability in young lambs. J. Appl. Physiol. 69: 577–583, 1990.

    PubMed  CAS  Google Scholar 

  32. Carter, E.P., S.E. Duvick, C.H. Wendt, J. Dunitz, L. Nici, O.D. Wangensteen, and D.H. Ingbar. Hyperoxia increases active alveolar Na+ resorption in vivo and type II cell Na, KATPase in vitro. Chest 105: 75S - 78S, 1994.

    PubMed  CAS  Google Scholar 

  33. Cassin, S., V. DeMarco, A.M. Perks, H. Kuck, and T.M. Ellis. Regulation of lung liquid secretion in immature fetal sheep: hormonal interaction. J. Appl. Physiol. 77: 1445–1450, 1994.

    PubMed  CAS  Google Scholar 

  34. Cassin, S., G. Gausse, and A.M. Perks. The effects of bumetanide and furosemide on lung liquid secretion in fetal sheep. Proc. Exp. Biol. Med. 181: 427–431, 1986.

    CAS  Google Scholar 

  35. Cassin, S., and A.M. Perks. Amiloride inhibits arginine-vasopressin induced decrease in fetal lung liquid secretion. J. Appl. Physiol. 75: 1925–1929, 1993.

    PubMed  CAS  Google Scholar 

  36. Champigny, G., N.Voilley, E. Lingueglia, V. Friend, P. Barbry, and M. Lazdunski. Regulation of expression of the lung amiloride-sensitive Na+ channel by steroid hormones. EMBO J 13: 2177–2181, 1994.

    CAS  Google Scholar 

  37. Chang, S.S., S. Grunder, A. Hanukoglu, A. Röler, P.M. Mathew, I. Hanukoglu, L. Schild, Y Lu, R.A. Shimkets, C. Nelson-Williams, B.C. Rossier, and R.O. Lifton. Mutations in the subunits of the epithelial sodium channel cause salt wasting with hyperkalemic acidosis, pseudohypoaldosterinism type 1. Nat. Genet. 12: 248–253, 1996.

    Article  PubMed  CAS  Google Scholar 

  38. Chapman, D.L., D.P. Carlton, J.J. Cummings, F.R. Poulain, and R.D. Bland. Intrapulmonary terbutaline and aminophylline decrease lung liquid in fetal lambs. Pediatr. Res. 29: 357–361, 1991.

    Article  PubMed  CAS  Google Scholar 

  39. Compeau, C.G., O.D. Rotstein, H. Tohda, Y. Marunaka, B. Rafii, A.S. Slutsky, and H. O’Brodovich. Endotoxin-stimulated alveolar macrophages impair lung epithelial Na+ transport by an L-Arg-dependent mechanism. Am. J. Physiol. 266: C1330 - C1341, 1994.

    PubMed  CAS  Google Scholar 

  40. Cott, G.R. Modulation of bioelectric properties across alveolar type II cells by substratum. Am. J. Physiol. 257: C678 - C688, 1989.

    PubMed  CAS  Google Scholar 

  41. Cott, G.R., and A.K. Rao. Hydrocortisone promotes the maturation of Na+-dependent ion transport across the fetal pulmonary epithelium. Am. J. Respir. Cell Mol. Biol. 9: 166–171, 1993.

    Article  PubMed  CAS  Google Scholar 

  42. Cott, G.R., S.R. Walker, and R.J. Mason. The effect of substratum and serum on the lipid synthesis and morphology of alveolar Type II cells in vitro. Exp. Lung Res. 13: 427–447, 1987.

    Article  PubMed  CAS  Google Scholar 

  43. Cotton, C.U., R.C. Boucher, and J.T. Gatzy. Bioelectric properties and ion transport across excised canine fetal and neonatal airways. J. Appl. Physiol. 65: 2367–2375, 1988.

    PubMed  CAS  Google Scholar 

  44. deSa, D.J. Pulmonary fluid content in infants with respiratory distress. J. Pathol. 97: 469–479, 1969.

    Article  PubMed  CAS  Google Scholar 

  45. Egan, E.A., W.P. Dillon, and S. Zorn. Fetal lung liquid absorption and alveolar epithelial solute permeability in surfactant deficient, breathing fetal lambs. Pediatr. Res. 6: 566–570, 1984.

    Article  Google Scholar 

  46. Egan, E.A., R.E. Olver, and L.B. Strang. Changes in non-electrolyte permeability of alveoli and the absorption of lung liquid at the start of breathing in the lamb. J. Physiol. Lond. 244: 161–179, 1975.

    PubMed  CAS  Google Scholar 

  47. Feng, Z., R.B. Clark, and Y. Berthiaume. Identification of nonselective cation channels in cultured adult rat alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 9: 248–254, 1993.

    Article  PubMed  CAS  Google Scholar 

  48. Gonzalez, A., I.R.S. Sosenko, J. Chandar, H. Hummler, N. Claure, and E. Bancalari. Influence of infection on patent ductus arteriosus and chronic lung disease in premature infants weighing 1000 grams or less. J. Pediatr. 128: 470–478, 1996.

    Article  PubMed  CAS  Google Scholar 

  49. Gowen, C.V., E.E. Lawson, J. Gingras, R. Boucher, J.T. Gatzy, and M. Knowles. Electrical potential difference and ion transport across nasal epithelium of term neonates: correlation with mode of delivery, transient tachypnea of the newborn, and respiratory rate. J. Pediatr. 113: 121–127, 1988.

    Article  PubMed  Google Scholar 

  50. Haddad, I.Y., G. Pataki, P. Hu, C. Galliani, J.S. Beckman, and S. Matalon. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J. Clin. Invest. 94: 2407–2413, 1994.

    Article  PubMed  CAS  Google Scholar 

  51. Haskell, J.F., G. Yue, D.J. Benos, and S. Matalon. Upregulation of sodium conductive pathways in alveolar type II cells in sublethal hyperoxia. Am. J. Physiol. 266: L30 - L37, 1994.

    PubMed  CAS  Google Scholar 

  52. Hooper, S.B., M.J. Wallace, and R. Harding. Amiloride blocks the inhibition of fetal lung liquid secretion caused by AVP but not asphyxia. J. Appl. Physiol. 74: 111–115, 1993.

    Article  PubMed  CAS  Google Scholar 

  53. Huang, M., and M. Chalfie. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367: 467–470, 1994.

    Article  CAS  Google Scholar 

  54. Hummler, E., P. Barker, J. Gatzy, F. Beermann, C. Verdumo, A. Schmidt, R. Boucher, and B.C. Rossier. Early death due to defective neonatal lung liquid clearance in a-ENaC-deficient mice. Nat. Genet. 12: 325–328, 1996.

    Article  PubMed  CAS  Google Scholar 

  55. Ingbar, D.H., C.B. Weeks, M. Gilmore-Hebert, E. Jacobsen, S. Duvick, R. Dowin, S.K. Savik, and J.D. Jamieson. Developmental regulation of Na, K-ATPase in rat lung. Am. J. Physiol. 270: L619 - L629, 1996.

    CAS  Google Scholar 

  56. Jackson, C., A. Mackenzie, E. Chi, T. Standaert, W. Truog, and W. Hodson. Mechanisms for reduced total lung capacity at birth and during hyaline membrane disease in premature newborn monkeys. Am. Rev. Respir. Dis. 142: 413–419, 1990.

    Article  PubMed  CAS  Google Scholar 

  57. Jefferies, A.L., G. Coates, and H.M. O’Brodovich. Pulmonary epithelial permeability in hyaline-membrane disease. N. Engl. J. Med. 311: 1075–1080, 1984.

    Article  PubMed  CAS  Google Scholar 

  58. Jefferies, A.L., and K.F.Y. Tai. Sequential changes in pulmonary epithelial permeability after birth in term and preterm rabbits. Biol. Neonate 66: 86–92, 1994.

    Article  PubMed  CAS  Google Scholar 

  59. Jobe, A., and M. Ikegami. State of the art: surfactant for the treatment of respiratory distress syndrome. Am. Rev. Respir. Dis. 136: 1256–1275, 1987.

    Article  PubMed  CAS  Google Scholar 

  60. Jost, A., and A. Policard. Contribution expérimentale a l’étude du development prénatal du poumon chez la lapin. Arch. Anat. Microsc. Morphol. Exp. 37: 323–332, 1948.

    Google Scholar 

  61. Kemp, P.J., G.G. MacGregor, and R.E. Olver. G protein-regulated large-conductance chloride channels in freshly isolated fetal type II alveolar epithelial cells. Am. J. Physiol. 265: L323–329, 1993.

    CAS  Google Scholar 

  62. Lingueglia, E., N. Voilley, R. Waldmann, M. Lazdunski, and P. Barbry. Expression cloning of an epithelial amiloride-sensitive Na+ channel: a new channel type with homologies to Caenorhabditis elegans degenerins. FEBS Lett. 318: 95–99, 1993.

    Article  PubMed  CAS  Google Scholar 

  63. Leung, C.K.H., I.Y.R. Adamson,, and D.H. Bowden. Uptake of 3H prednisolone by fetal lung explants: role of intercellular contacts in epithelial maturation. Exp. Lung Res. 1: 111–120, 1980.

    Article  PubMed  CAS  Google Scholar 

  64. Lwebuga-Mukasa, J. Matrix-driven pneumocyte differentiation. Am. Rev. Respir. Dis. 144: 452–457, 1991.

    Article  PubMed  CAS  Google Scholar 

  65. MacLeod, R.J., J.R. Hamilton, H. Kopelman, and N.B. Sweezey. Developmental differences of cystic fibrosis transmembrane conductance regulator functional expression in rat fetal distal airway epithelial cells. Pediatr. Res. 35: 45–49, 1994.

    Article  PubMed  CAS  Google Scholar 

  66. Matalon, S., M.L. Bauer, D.J. Benos, T.R. Kleyman, C. Lin, E.R Cragoe, Jr., and H. O’Brodovich. Fetal lung epithelial cells contain two populations of amiloride-sensitive Na+ channels. Am. J. Physiol. 264: L357–364, 1993.

    PubMed  CAS  Google Scholar 

  67. Matalon, S., R.J. Bridges, and D.J. Benos. Amiloride inhibitable Na conductive pathways in alveolar type II pneumonocytes. Am. J. Physiol. 264: L90 - L96, 1991.

    Google Scholar 

  68. Matalon, S., and E.A. Egan. Effects of 100% 02 breathing on permeability of alveolar epithelium to solute. J. Appl. Physiol. 50: 859863, 1981.

    Google Scholar 

  69. Matalon, S., K.L. Kirk, J.K. Bubien, Y. Oh, P. Hu, G. Yue, R. Shoemaker, E.J.J. Cragoe, and D.J. Benos. Immunocytochemical and functional characterization of Na+ conductance in adult alveolar pneumonocytes. Am. J. Physiol. 262: C1228 - C1238, 1992.

    PubMed  CAS  Google Scholar 

  70. Matthay, M.A., and J.P. Wiener-Kronish, Intact epithelial barrier function is critical for the resolution of alveolar edema in man. Am. Rev. Respir. Dis. 142: 1250–1257, 1990.

    Article  PubMed  CAS  Google Scholar 

  71. McCray, P.B., and M.K. Welsh. Developing fetal alveolar epithelial cells secrete fluid in primary culture. Am. J. Physiol. 260: L494 - L500, 1991.

    PubMed  CAS  Google Scholar 

  72. McCray, P.B., Jr., C.L. Wohlford-Lenane, and J.M. Snyder. Localization of cystic fibrosis transmembrane conductance regulator mRNA in human fetal lung tissue by in situ hybridization. J. Clin. Invest. 90: 619–625, 1992.

    Article  PubMed  CAS  Google Scholar 

  73. McCray, P.B., Jr., W.W. Reenstra, E. Louie, J. Johnson, J.D. Bettencourt, and J. Bastacky. Expression of CFTR and presence of cAMP-mediated fluid secretion in human fetal lung. Am. J. Physiol. 262: L472 - L481, 1992.

    PubMed  CAS  Google Scholar 

  74. McCray, P.B. Jr., J.D. Bettencourt, J. Bastacky, G.M. Denning, and M.J. Welsh. Expression of CFTR and cAMP-stimulated chloride secretory current in cultured human fetal alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 9: 578–585, 1993.

    Article  PubMed  CAS  Google Scholar 

  75. McDonald, F.J., P.M. Snyder, P.B. McCray, and M.J. Welsh. Cloning, expression, and tissue distribution of the human epithelial sodium channel. Am. J. Physiol. 268: L728–734, 1995.

    Google Scholar 

  76. McGowan, S.E. Extracellular matrix and the regulation of lung development and repair. FASEB J. 6: 2895–2904, 1992.

    PubMed  CAS  Google Scholar 

  77. McPherson, M.A., and R.L. Dormer. Abnormalities in the intracellular regulation in cystic fibrosis. In: Cystic Fibrosis, edited by J.O. Warner. New York: Churchill Livingstone, 1992, p. 766–784.

    Google Scholar 

  78. Moessinger, A.C., R.D. Harding, T.M. Adamson, M. Singh, and G.T. Kiu. Role of lung liquid volume in growth and maturation of the fetal sheep lung. J. Clin. Invest. 86: 1270 1277, 1990.

    Google Scholar 

  79. Murray, C.B., M.M. Morales, T.R. Flotte, S.A. McGrath-Morrow, W.B. Guggino, W.B., and P.L. Zeitlin. C1C-2: a developmentally dependent chloride channel expressed in the fetal lung and downregulated after birth. Am. J. Respir. Cell Mol. Biol. 12: 597–604, 1995.

    Article  PubMed  CAS  Google Scholar 

  80. Nardo, L., S.B. Hooper, and R. Harding. Lung hypoplasia can be reversed by short-term obstruction of the trachea in fetal sheep. Pediatr. Res. 38: 690–696, 1995.

    Article  PubMed  CAS  Google Scholar 

  81. O’Brodovich, H.M. The role of active Na+ transport by lung epithelium in the clearance of airspace fluid. New Horizons 3: 240–247, 1995.

    PubMed  Google Scholar 

  82. O’Brodovich, H.M. Immature epithelial Na+ channel expression is one of the pathogenetic mechanisms leading to human neonatal respiratory distress syndrome. Proc. Assoc. Am. Phys. 108: 345–355, 1996.

    PubMed  Google Scholar 

  83. O’Brodovich, H., C. Canessa, J. Ueda, B. Rafii, B.C. Rossier, and J. Edelson. Expression of the epithelial Na+ channel in the developing rat lung. Am. J. Physiol. 265: C491 - C496, 1993.

    PubMed  Google Scholar 

  84. O’Brodovich, H.M., and V. Hannam. Exogenous surfactant rapidly increases PaO2 in mature rabbits with lungs that contain large amounts of saline. Am. Rev. Respir. Dis. 147: 1087–1090, 1993.

    Article  PubMed  Google Scholar 

  85. O’Brodovich, H., V. Hannam, and B. Rafii. Sodium channel but neither Na+-H+ nor Na glucose symport inhibitors slow neonatal lung water clearance. Am. J. Respir. Cell Mol. Biol. 5: 377–384, 1991.

    Article  PubMed  Google Scholar 

  86. O’Brodovich, H., V. Hannam, M. Seear, and J.B.M. Mullen. Amiloride impairs lung water clearance in newborn guinea pigs. J. Appl. Physiol. 68: 1758–1762, 1990.

    PubMed  Google Scholar 

  87. O’Brodovich, H.M., and R.B. Mellins. Bronchopulmonary dysplasia. Unresolved neonatal lung injury. Am. Rev. Respir. Dis. 132: 694–709, 1985.

    PubMed  Google Scholar 

  88. O’Brodovich, H., and T.A. Merritt. Bicarbonate concentration in rhesus monkey and guinea pig fetal lung liquid. Am. Rev. Respir. Dis. 146: 1613–1618, 1992.

    Article  PubMed  Google Scholar 

  89. O’Brodovich, H., B. Rafii, and M. Post. Bioelectric properties of fetal alveolar epithelial monolayers. Am. J. Physiol. 258: L201–206, 1990.

    PubMed  Google Scholar 

  90. O’Brodovich, H., O. Staub, B.C. Rossier, K. Geering,, and J.-P. Kraehenbuhl. Ontogeny of a1- and 131-isoforms of Na+-K+-ATPase in fetal distal rat lung epithelium. Am. J. Physiol. 264: C1137 - C1143, 1993.

    PubMed  Google Scholar 

  91. Olivera, W., K. Ridge, L.D.H. Wood, and J.I. Sznajder. Active sodium transport and alveolar epithelial Na-K-ATPase increase during subacute hyperoxia in rats. Am. J. Physiol. 266: L577 - L584, 1994.

    PubMed  CAS  Google Scholar 

  92. Olver, R.E., C.A. Ramsden, L.B. Strang, and D.V. Walters. The role of amiloride-blockable sodium transport in adrenaline-induced lung liquid reabsorption in the fetal lung. J. Physiol. 376: 321–340, 1986.

    PubMed  CAS  Google Scholar 

  93. Olver, R.E., and L.B. Strang. Ion fluxes across pulmonary epithelium and the secretion of lung liquid in the foetal lamb. J. Physiol. Lond. 241: 327–257, 1974.

    PubMed  CAS  Google Scholar 

  94. Olver, R.E., E.E. Schneeberger, and D.V. Walters. Epithelial solute permeability, ion transport and tight junction morphology in the developing lung of the fetal lamb. J. Physiol. Lond. 315: 395–412, 1981.

    PubMed  CAS  Google Scholar 

  95. Orlowski, J., and J.B. Lingrel. Tissue-specific and developmental regulation of rat Na, KATPase catalytic a isoform and ß subunit mRNAs. J. Biol. Chem. 263: 10436–10442, 1988.

    PubMed  CAS  Google Scholar 

  96. Orser, B.A., M. Bertlik, L. Fedorko, and H.M. O’Brodovich. Non-selective cation channel in fetal alveolar type II epithelium. Biochim. Biophys. Acta (Mol. Cell Struct.) 1094: 19–26, 1991.

    Article  CAS  Google Scholar 

  97. Orzalesi, M., M. Motoyama, H.N. Jacobson, Y. Kikkawa, E.O.R. Reynolds, and C.D. Cook. The development of lung liquid in fetal goats. Pediatrics 35: 373–381, 1965.

    PubMed  CAS  Google Scholar 

  98. Palazzo, R.M., O.D. Wangensteen, and D.E. Niewoehner. Time course of functional repair of the alveolar epithelium after hyperoxic injury. J. Appl. Physiol. 73: 1881–1887, 1992.

    PubMed  CAS  Google Scholar 

  99. Perks, A.M., and S. Cassin. The effects of arginine vasopressin and other factors on the production of lung liquid in fetal goats. Chest 81: 63S - 65S, 1982.

    Article  Google Scholar 

  100. Pierce, M.R., and E. Bancalari. The role of inflammation in the pathogenesis of bronchopulmonary dysplasia. Pediatr. Pulmonol. 19: 371–378, 1995.

    Article  PubMed  CAS  Google Scholar 

  101. Pitkänen, O.M., A.K. Tanswell, and H.M. O’Brodovich. Fetal lung cell-derived matrix alters distal lung epithelial ion transport. Am. J. Physiol. 268: L762 - L771, 1995.

    PubMed  Google Scholar 

  102. Pitkänen, O., A.K. Tanswell, G. Downey, and H. O’Brodovich. Increased PO, alters bioelectric properties of fetal lung epithelium. Am. J. Physiol. 270: L1060 - L1066, 1996.

    PubMed  Google Scholar 

  103. Rao, A.K., and G.R. Cott. Ontogeny of ion transport across fetal pulmonary epithelial cells in monolayer culture. Am. J. Physiol. 261: L178 - L187, 1991.

    PubMed  CAS  Google Scholar 

  104. Ruddy, M.K., J.M. Drazen, O.M. Pitkänen, B. Rafii, H.M. O’Brodovich, and H.W. Harris. Modulation of aquaporin 4 and the amiloride-inhibitable sodium channel in perinatal rat lung epithelial cells. Am. J. Physiol. 274: L1066 - L1072, 1998.

    PubMed  CAS  Google Scholar 

  105. Sakuma, T., G. Okaniwa, T. Nakada, T. Nishimura, S. Fujimura, and M.A. Matthay. Alveolar fluid clearance in the resected human lung. Am. J. Respir. Crit. Care Med. 150: 305–310, 1994.

    Article  PubMed  CAS  Google Scholar 

  106. Schneeberger, E.E., and K.M. McCarthy. Cytochemical localization of Na+-K+-ATPase in rat type II pneumocytes. J. Appl. Physiol. 60: 1584–1589, 1986.

    Article  PubMed  CAS  Google Scholar 

  107. Scurry, J.P., T.M. Adamson, and L.J. Cussen. Fetal lung growth in laryngeal atresia and tracheal agenesis. Austr. Pediatr. J. 25: 47–51, 1989.

    CAS  Google Scholar 

  108. Souza, P., H. O’Brodovich, and M. Post. Lung fluid restriction affects growth, but not airway branching of embryonic rat lung. Int. J. Dev. Biol. 39: 629–637, 1995.

    PubMed  CAS  Google Scholar 

  109. Strang, L.B. Fetal lung liquid: secretion and reabsorption. Physiol. Rev. 71: 991–1016, 1991.

    PubMed  CAS  Google Scholar 

  110. Sznajder, J.I., W.G. Olivera, K.M. Ridge, and D.H. Rutschman. Mechanisms of lung liquid clearance during hyperoxia in isolated rat lungs. Am. J. Respir. Crit. Care Med. 151: 1519–1525, 1995.

    Article  PubMed  CAS  Google Scholar 

  111. Tchepichev, S., J. Ueda, C. Canessa, B.C. Rossier, and H. O’Brodovich. Lung epithelial Na channel subunits are differentially regulated during development and by steroids. Am. J. Physiol. 269: C805 - C812, 1995.

    PubMed  CAS  Google Scholar 

  112. Tizzano, E.F., H. O’Brodovich, D. Chitayat, J.-C. Bènichou, and M. Buchwald. Regional expression of CFTR in developing human respiratory tissues. Am. J. Respir. Cell. Mol. Biol. 10: 355–362, 1994.

    Article  PubMed  CAS  Google Scholar 

  113. Thom, J., and A.M. Perks. The effects of furosemide and bumetanide on lung liquid production in vitro lungs from fetal guinea pigs. Can. J. Physiol. Pharmacol. 68: 1131–1135, 1990.

    Article  PubMed  CAS  Google Scholar 

  114. Tohda, H., J.K. Foskett, H. O’Brodovich, and Y. Marunaka. Cl-regulaton of a Caz+ activated nonselective cation channel in ß-agonist-treated fetal distal lung epithelium. Am. J. Physiol. 266: C104 - C109, 1994.

    CAS  Google Scholar 

  115. Tohda, H., and Y. Marunaka. Insulin-activated amiloride-blockable nonselective cation and Na+ channels in the fetal distal lung epithelium. Gen. Pharmacol. 26: 755–763, 1995.

    Article  PubMed  CAS  Google Scholar 

  116. Voilley, N., E. Lingueglia, G. Champigny, M.-G. Mattéi, R. Waldmann, M. Lazdunski, and P. Barbry. The lung amiloride-sensitive Na+ channel: biophysical properties, pharmacology, ontogenesis, and molecular cloning. Proc. Natl. Acad. Sci. USA 91: 247–251, 1994.

    Article  PubMed  CAS  Google Scholar 

  117. Volk, K.A., R.D. Sigmund, P.M. Snyder, J. McDonald, M.J. Welsh, and J.B. Stokes. rENaC is the predominant Na+ channel in the apical membrane of the rat renal inner medullary collecting duct. J. Clin. Invest. 96: 2748–2757, 1995.

    Article  CAS  Google Scholar 

  118. Vukicevic, S., H. Kleinman, F. Luyten, A. Roberts, N. Roche,, and A.H. Reddi. Identification of multiple active growth factors in basement membrane matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp. Cell. Res. 202: 1–8, 1992.

    Article  PubMed  CAS  Google Scholar 

  119. Wallace, M.J., S.B. Hooper, and R. Harding. Regulation of lung liquid secretion by arginine vasopressin in fetal sheep. Am. J. Physiol. 258: R104 - R111, 1990.

    PubMed  CAS  Google Scholar 

  120. Wallace, M.J., S.B. Hooper, and R. Harding. Effects of elevated cortisol concentrations on the volume, secretion, and reabsorption of lung liquid. Am. J. Physiol. 269: R881 - R887, 1995.

    PubMed  CAS  Google Scholar 

  121. Wallace M.J., S.B. Hooper, and R. Harding. Role of the adrenal glands in the maturation of lung liquid secretory mechanisms in fetal sheep. Am. J. Physiol. 270: R33 - R40, 1996.

    PubMed  CAS  Google Scholar 

  122. Walters, D.V. Fetal lung liquid: secretion and absorption. In: Fetus and Neonate: Physiology and Clinical Application:. Vol. 2 Breathing, edited by M.A. Hanson, J.A.D. Spencer, and C.H. Rodeck. Cambridge: Cambridge University Press, 1994, p. 42–62.

    Google Scholar 

  123. Walters, D.V., and R.E. Olver. The role of catecholamines in lung liquid absorption at birth. Pediatr. Res. 12: 239–242, 1978.

    Article  PubMed  CAS  Google Scholar 

  124. Walters, D.V., C.A. Ramsden, and R.E. Olver. Dibutyryl cAMP induces a gestation-dependent absorption of fetal lung liquid. J. Appl. Physiol. 68: 2054–2059, 1990.

    PubMed  CAS  Google Scholar 

  125. Wang, X., T. Kleyman, H. Tohda, Y. Marunaka, and H.M. O’Brodovich. EIPA sensitive Na+ currents in intact fetal distal lung epithelial cells. Can. J. Physiol. Pharmacol. 71: 58–62, 1993.

    Article  PubMed  CAS  Google Scholar 

  126. Yue, G., W.J. Russell, D.J. Benos, R.M. Jackson, M.A. Olman, and S. Matalon, Increased expression and activity of sodium channels in alveolar type II cells of hyperoxic rats. Proc. Natl. Acad. Sci. USA 92: 8418–8422, 1995.

    Article  PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1999 American Physiological Society

About this chapter

Cite this chapter

Pitkänen, O., O’Brodovich, H. (1999). Development of Lung Epithelial Ion Transport: Implications for Neonatal Lung Disease. In: Gaultier, C., Bourbon, J.R., Post, M. (eds) Lung Development. Clinical Physiology Series. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7537-8_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-7537-8_9

  • Publisher Name: Springer, New York, NY

  • Online ISBN: 978-1-4614-7537-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics