Claudin-18 deficiency results in alveolar barrier dysfunction and impaired alveologenesis in mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 51, Issue 4, 2014, Pages 550-558

  LaFemina, Michael J ^a,b   Sutherland, Katherine M ^a   Bentley, Trevor ^c   Gonzales, Linda W ^d   Allen, Lennell ^a   Chapin, Cheryl J ^a   Rokkam, Deepti ^c   Sweerus, Kelly A ^a   Dobbs, Leland G ^a   Ballard, Philip L ^a   Frank, James A ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c NORTHERN CALIFORNIA INSTITUTE FOR RESEARCH AND EDUCATION   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Bronchopulmonary dysplasia; Claudins; Lung injury; Tight junctions

Indexed keywords

MUS;

CLAUDIN; CLDN18 PROTEIN, HUMAN; CLDN18 PROTEIN, MOUSE;

ANIMAL; C57BL MOUSE; DEFICIENCY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFANT; KNOCKOUT MOUSE; LUNG ALVEOLUS; LUNG DYSPLASIA; METABOLISM; NEWBORN; PATHOLOGY; PERMEABILITY; RISK FACTOR; TIGHT JUNCTION;

ANIMALS; BRONCHOPULMONARY DYSPLASIA; CLAUDINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HUMANS; INFANT; INFANT, NEWBORN; MICE, INBRED C57BL; MICE, KNOCKOUT; PERMEABILITY; PULMONARY ALVEOLI; RISK FACTORS; TIGHT JUNCTIONS;

EID: 84907481396     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0456OC     Document Type: Article

References (42)

1. Kinsella JP, Greenough A, Abman SH. Bronchopulmonary dysplasia. Lancet 2006;367:1421-1431.
2. Northway WH Jr, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease: bronchopulmonary dysplasia. N Engl J Med 1967;276:357-368.
3. Walsh MC, Szefler S, Davis J, Allen M, Van Marter L, Abman S, Blackmon L, Jobe A. Summary proceedings from the bronchopulmonary dysplasia group. Pediatrics 2006;117:S52-S56.
4. Coalson JJ. Pathology of new bronchopulmonary dysplasia. Semin Neonatol 2003;8:73-81.
5. Baraldi E, Filippone M. Chronic lung disease after premature birth. N Engl J Med 2007;357:1946-1955.
6. Furuse M, Sasaki H, Fujimoto K, Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 1998;143:391-401.
7. Morita K, Furuse M, Fujimoto K, Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 1999;96:511-516.
8. Angelow S, Ahlstrom R, Yu AS. Biology of claudins. Am J Physiol Renal Physiol 2008;295:F867-F876.
9. Frank JA. Claudins and alveolar epithelial barrier function in the lung. Ann N Y Acad Sci 2012;1257:175-183.
10. Niimi T, Nagashima K, Ward JM, Minoo P, Zimonjic DB, Popescu NC, Kimura S. Claudin-18, a novel downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor, encodes lungand stomach-specific isoforms through alternative splicing. Mol Cell Biol 2001;21:7380-7390.
11. LaFemina MJ, Rokkam D, Chandrasena A, Pan J, Bajaj A, Johnson M, Frank JA. Keratinocyte growth factor enhances barrier function without altering claudin expression in primary alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2010;299:L724-L734.
12. Fang X, Neyrinck AP, Matthay MA, Lee JW. Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. J Biol Chem 2010;285:26211-26222.
13. Daugherty BL, Mateescu M, Patel AS, Wade K, Kimura S, Gonzales LW, Guttentag S, Ballard PL, Koval M. Developmental regulation of claudin localization by fetal alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004;287:L1266-L1273.
14. Frank J, Roux J, Kawakatsu H, Su G, Dagenais A, Berthiaume Y, Howard M, Canessa CM, Fang X, Sheppard D, et al. Transforming growth factor-beta1 decreases expression of the epithelial sodium channel alphaENaC and alveolar epithelial vectorial sodium and fluid transport via an ERK1/2-dependent mechanism. J Biol Chem 2003;278:43939-43950.
15. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol 1990;258:L134-L147.
16. Wray C, Mao Y, Pan J, Chandrasena A, Piasta F, Frank JA. Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. Am J Physiol Lung Cell Mol Physiol 2009;297: L219-L227.
17. Balasubramaniam V, Tang JR, Maxey A, Plopper CG, Abman SH. Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol 2003; 284:L964-L971.
18. Thurlbeck WM. The internal surface area of nonemphysematous lungs. Am Rev Respir Dis 1967;95:765-773.
19. Thurlbeck WM. Measurement of pulmonary emphysema. Am Rev Respir Dis 1967;95:752-764.
20. Mund SI, Stampanoni M, Schittny JC. Developmental alveolarization of the mouse lung. Dev Dyn 2008;237:2108-2116.
21. Bland RD, Xu L, Ertsey R, Rabinovitch M, Albertine KH, Wynn KA, Kumar VH, Ryan RM, Swartz DD, Csiszar K, et al. Dysregulation of pulmonary elastin synthesis and assembly in preterm lambs with chronic lung disease. Am J Physiol Lung Cell Mol Physiol 2007;292: L1370-L1384.
22. Thebaud B, Abman SH. Bronchopulmonary dysplasia: where have all the vessels gone? Roles of angiogenic growth factors in chronic lung disease. Am J Respir Crit Care Med 2007;175:978-985.
23. McElroy MC, Pittet JF, Hashimoto S, Allen L, Wiener-Kronish JP, Dobbs LG. A type I cell-specific protein is a biochemical marker of epithelial injury in a rat model of pneumonia. Am J Physiol 1995;268:L181-L186.
24. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349.
25. Schneeberger EE, Lynch RD. The tight junction: A multifunctional complex. Am J Physiol Cell Physiol 2004;286:C1213-C1228.
26. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol 2006;68:403-429.
27. Hadj-Rabia S, Baala L, Vabres P, Hamel-Teillac D, Jacquemin E, Fabre M, Lyonnet S, De Prost Y, Munnich A, Hadchouel M, et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: A tight junction disease. Gastroenterology 2004;127: 1386-1390.
28. Wilcox ER, Burton QL, Naz S, Riazuddin S, Smith TN, Ploplis B, Belyantseva I, Ben-Yosef T, Liburd NA, Morell RJ, et al. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell 2001;104:165-172.
29. Hou J, Renigunta A, Gomes AS, Hou M, Paul DL, Waldegger S, Goodenough DA. Claudin-16 and claudin-19 interaction is required for their assembly into tight junctions and for renal reabsorption of magnesium. Proc Natl Acad Sci USA 2009;106:15350-15355.
30. Rokkam D, Lafemina MJ, Lee JW, Matthay MA, Frank JA. Claudin-4 levels are associated with intact alveolar fluid clearance in human lungs. Am J Pathol 2011;179:1081-1087.
31. Ohta H, Chiba S, Ebina M, Furuse M, Nukiwa T. Altered expression of tight junction molecules in alveolar septa in lung injury and fibrosis. Am J Physiol Lung Cell Mol Physiol 2012;302:L193-L205.
32. Dobbs LG, Johnson MD, Vanderbilt J, Allen L, Gonzalez R. The great big alveolar TI cell: evolving concepts and paradigms. Cell Physiol Biochem 2010;25:55-62.
33. Li G, Flodby P, Luo J, Kage H, Sipos A, Gao D, Ji Y, Beard LL, Marconett CN, Demaio L, et al. Knockout mice reveal key roles for claudin 18 in alveolar barrier properties and fluid homeostasis. Am J Respir Cell Mol Biol (In press).
34. Jobe AH. The new bronchopulmonary dysplasia. Curr Opin Pediatr 2011;23:167-172.
35. Buczynski BW, Maduekwe ET, O'Reilly MA. The role of hyperoxia in the pathogenesis of experimental BPD. Semin Perinatol 2013;37:69-78.
36. Velten M, Heyob KM, Rogers LK, Welty SE. Deficits in lung alveolarization and function after systemic maternal inflammation and neonatal hyperoxia exposure. J Appl Physiol (1985) 2010;108: 1347-1356.
37. Bland RD, Mokres LM, Ertsey R, Jacobson BE, Jiang S, Rabinovitch M, Xu L, Shinwell ES, Zhang F, Beasley MA. Mechanical ventilation with 40% oxygen reduces pulmonary expression of genes that regulate lung development and impairs alveolar septation in newborn mice. Am J Physiol Lung Cell Mol Physiol 2007;293:L1099-L1110.
38. Weinstein M, Xu X, Ohyama K, Deng CX. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 1998;125:3615-3623.
39. Wan H, Kaestner KH, Ang SL, Ikegami M, Finkelman FD, Stahlman MT, Fulkerson PC, Rothenberg ME, Whitsett JA. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 2004;131: 953-964.
40. Young LR, Gulleman PM, Bridges JP, Weaver TE, Deutsch GH, Blackwell TS, McCormack FX. The alveolar epithelium determines susceptibility to lung fibrosis in Hermansky-Pudlak syndrome. Am J Respir Crit Care Med 2012;186:1014-1024.
41. King TE Jr, Pardo A, Selman M. Idiopathic pulmonary fibrosis. Lancet 2011;378:1949-1961.
42. Srisuma S, Bhattacharya S, Simon DM, Solleti SK, Tyagi S, Starcher B, Mariani TJ. Fibroblast growth factor receptors control epithelial-mesenchymal interactions necessary for alveolar elastogenesis. Am J Respir Crit Care Med 2010;181:838-850.