Hyperoxia stimulates the transdifferentiation of type II alveolar epithelial cells in newborn rats

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 9, 2015, Pages L861-L872

  Hou, Ana ^a   Fu, Jianhua ^a   Yang, Haiping ^a   Zhu, Yuting ^a   Pan, Yuqing ^a   Xu, Shuyan ^a   Xue, Xindong ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Alveolar epithelial cells; Bronchopulmonary dysplasia; Hyperoxia; Transdifferentiation

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AQUAPORIN 5; CASPASE 3; SURFACTANT PROTEIN B; SURFACTANT PROTEIN C; T1 ALPHA PROTEIN; UNCLASSIFIED DRUG; AQP5 PROTEIN, RAT; GP38 PROTEIN, RAT; MEMBRANE PROTEIN; OXYGEN; PEPTIDE; SFTPC PROTEIN, RAT;

ANALYTICAL PARAMETERS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DAMAGE; CELL FATE; CELL FUNCTION; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSDIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HYPEROXIA; IN VIVO STUDY; LUNG ALVEOLUS EPITHELIUM CELL; LUNG DEVELOPMENT; LUNG DYSPLASIA; LUNG EDEMA; LUNG INJURY; LUNG WEIGHT; NEWBORN; NONHUMAN; OXYGEN BREATHING; OXYGEN CONCENTRATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN ISOLATION; RAT; RESPIRATORY FAILURE; SURFACE TENSION; THICKNESS; TIGHT JUNCTION; TISSUE LEVEL; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRONCHOPULMONARY DYSPLASIA; CELL CULTURE; CYTOLOGY; EPITHELIUM CELL; LUNG ALVEOLUS; LUNG GAS EXCHANGE; METABOLISM; PHYSIOLOGY; RANDOMIZATION; RESPIRATORY TRACT MUCOSA; WISTAR RAT;

ANIMALS; APOPTOSIS; AQUAPORIN 5; BLOOD-AIR BARRIER; BRONCHOPULMONARY DYSPLASIA; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; EPITHELIAL CELLS; HYPEROXIA; MEMBRANE GLYCOPROTEINS; OXYGEN; PEPTIDES; PULMONARY ALVEOLI; PULMONARY SURFACTANT-ASSOCIATED PROTEIN B; RANDOM ALLOCATION; RATS; RATS, WISTAR; RESPIRATORY MUCOSA;

EID: 84929670825     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00099.2014     Document Type: Article

References (63)

1. Adamson IY, Bowden DH. Derivation of type 1 epithelium from type 2 cells in the developing rat lung. Lab Invest 32: 736–745, 1975.
2. Adamson IY, Bowden DH, Wyatt JP. Oxygen poisoning in mice. Ultrastructural and surfactant studies during exposure and recovery. Arch Pathol 90: 463–472, 1970.
3. Alejandre-Alcazar MA, Kwapiszewska G, Reiss I, Amarie OV, Marsh LM, Sevilla-Perez J, Wygrecka M, Eul B, Kobrich S, Hesse M, Schermuly RT, Seeger W, Eickelberg O, Morty RE. Hyperoxia modulates TGF-α/BMP signaling in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 292: L537–L549, 2007.
4. Anderson PJ, Doyle LW. Neurodevelopmental outcome of bronchopulmonary dysplasia. Semin Perinatol 30: 227–232, 2006.
5. Bancalari E, Claure N. Definitions and diagnostic criteria for bronchopulmonary dysplasia. Semin Perinatol 30: 164–170, 2006.
6. Bhandari A, McGrath-Morrow S. Long-term pulmonary outcomes of patients with bronchopulmonary dysplasia. Semin Perinatol 37: 132–137, 2013.
7. Bhaskaran M, Kolliputi N, Wang Y, Gou D, Chintagari NR, Liu L. Trans-differentiation of alveolar epithelial type II cells to type I cells involves autocrine signaling by transforming growth factor beta 1 through the Smad pathway. J Biol Chem 282: 3968–3976, 2007.
8. Bonikos DS, Bensch KG, Ludwin SK, Northway WH Jr. Oxygen toxicity in the newborn. The effect of prolonged 100 per cent O2 exposure on the lungs of newborn mice. Lab Invest 32: 619–635, 1975.
9. Borok Z, Liebler JM, Lubman RL, Foster MJ, Zhou B, Li X, Zabski SM, Kim KJ, Crandall ED. Na transport proteins are expressed by rat alveolar epithelial type I cells. Am J Physiol Lung Cell Mol Physiol 282: L599–L608, 2002.
10. Borok Z, Lubman RL, Danto SI, Zhang XL, Zabski SM, King LS, Lee DM, Agre P, Crandall ED. Keratinocyte growth factor modulates alveolar epithelial cell phenotype in vitro: expression of aquaporin 5. Am J Respir Cell Mol Biol 18: 554–561, 1998.
11. Bostrom H, Willetts K, Pekny M, Leveen P, Lindahl P, Hedstrand H, Pekna M, Hellstrom M, Gebre-Medhin S, Schalling M, Nilsson M, Kurland S, Tornell J, Heath JK, Betsholtz C. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85: 863–873, 1996.
12. Burri PH. Structural aspects of postnatal lung development - alveolar formation and growth. Biol Neonate 89: 313–322, 2006.
13. Cao YX, Ramirez MI, Williams MC. Enhanced binding of Sp1/Sp3 transcription factors mediates the hyperoxia-induced increased expression of the lung type I cell gene T1alpha. J Cell Biochem 89: 887–901, 2003.
14. Capoluongo E, Ameglio F, Zuppi C. Insulin-like growth factor-I and complications of prematurity: a focus on bronchopulmonary dysplasia. Clin Chem Lab Med 46: 1061–1066, 2008.
15. Chen Y, Chang L, Li W, Rong Z, Liu W, Shan R, Pan R. Thioredoxin protects fetal type II epithelial cells from hyperoxia-induced injury. Pediatr Pulmonol 45: 1192–1200, 2010.
16. Chen Y, Legan SK, Mahan A, Thornton J, Xu H, Schwarz MA. Endothelial-monocyte activating polypeptide II disrupts alveolar epithelial type II to type I cell transdifferentiation. Respir Res 13: 1, 2012.
17. Chetty A, Andersson S, Lassus P, Nielsen HC. Insulin-like growth factor-1 (IGF-1) and IGF-1 receptor (IGF-1R) expression in human lung in RDS and BPD. Pediatr Pulmonol 37: 128–136, 2004.
18. Crapo JD, Barry BE, Foscue HA, Shelburne J. Structural and biochemical changes in rat lungs occurring during exposures to lethal and adaptive doses of oxygen. Am Rev Respir Dis 122: 123–143, 1980.
19. Dahlin K, Mager EM, Allen L, Tigue Z, Goodglick L, Wadehra M, Dobbs L. Identification of genes differentially expressed in rat alveolar type I cells. Am J Respir Cell Mol Biol 31: 309–316, 2004.
20. Danan C, Franco ML, Jarreau PH, Dassieu G, Chailley-Heu B, Bourbon J, Delacourt C. High concentrations of keratinocyte growth factor in airways of premature infants predicted absence of bronchopulmonary dysplasia. Am J Respir Crit Care Med 165: 1384–1387, 2002.
21. Dauger S, Ferkdadji L, Saumon G, Vardon G, Peuchmaur M, Gaultier C, Gallego J. Neonatal exposure to 65% oxygen durably impairs lung architecture and breathing pattern in adult mice. Chest 123: 530–538, 2003.
22. Dobbs LG, Gonzalez R, Matthay MA, Carter EP, Allen L, Verkman AS. Highly water-permeable type I alveolar epithelial cells confer high water permeability between the airspace and vasculature in rat lung. Proc Natl Acad Sci USA 95: 2991–2996, 1998.
23. Doyle LW, Faber B, Callanan C, Freezer N, Ford GW, Davis NM. Bronchopulmonary dysplasia in very low birth weight subjects and lung function in late adolescence. Pediatrics 118: 108–113, 2006.
24. Evans MJ, Cabral LJ, Stephens RJ, Freeman G. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO 2. Exp Mol Pathol 22: 142–150, 1975.
25. Franco-Montoya ML, Bourbon JR, Durrmeyer X, Lorotte S, Jarreau PH, Delacourt C. Pulmonary effects of keratinocyte growth factor in newborn rats exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 297: L965–L976, 2009.
26. Ghosh MC, Gorantla V, Makena PS, Luellen C, Sinclair SE, Schwingshackl A, Waters CM. Insulin-like growth factor-I stimulates differentiation of ATII cells to ATI-like cells through activation of Wnt5a. Am J Physiol Lung Cell Mol Physiol 305: L222–L228, 2013.
27. Han S, Tie X, Meng L, Wang Y, Wu A. PMA and ionomycin induce glioblastoma cell death: activation-induced cell-death-like phenomena occur in glioma cells. PLoS One 8: e76717, 2013.
28. Han S, Xia J, Qin X, Han S, Wu A. Phosphorylated SATB1 is associated with the progression and prognosis of glioma. Cell Death Dis 4: e901, 2013.
29. Harbeck RJ, Gegen NW, Struhar D, Mason R. Class II molecules on rat alveolar type II epithelial cells. Cell Immunol 111: 139–147, 1988.
30. Hellstrom A, Engstrom E, Hard AL, Albertsson-Wikland K, Carlsson B, Niklasson A, Lofqvist C, Svensson E, Holm S, Ewald U, Holmstrom G, Smith LE. Postnatal serum insulin-like growth factor I deficiency is associated with retinopathy of prematurity and other complications of premature birth. Pediatrics 112: 1016–1020, 2003.
31. Hilgendorff A, Reiss I, Ehrhardt H, Eickelberg O, Alvira CM. Chronic lung disease in the preterm infant. Lessons learned from animal models. Am J Respir Cell Mol Biol 50: 233–245, 2014.
32. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 279: L600–L607, 2000.
33. Ji W, Fu J, Nie H, Xue X. Expression and activity of epithelial sodium channel in hyperoxia-induced bronchopulmonary dysplasia in neonatal rats. Pediatr Int 54: 735–742, 2012.
34. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163: 1723–1729, 2001.
35. Kim JH, Jang YS, Eom KS, Hwang YI, Kang HR, Jang SH, Kim CH, Park YB, Lee MG, Hyun IG, Jung KS, Kim DG. Transforming growth factor beta1 induces epithelial-to-mesenchymal transition of A549 cells. J Korean Med Sci 22: 898–904, 2007.
36. Li T, Koshy S, Folkesson HG. Involvement of αENaC and Nedd4-2 in the conversion from lung fluid secretion to fluid absorption at birth in the rat as assayed by RNA interference analysis. Am J Physiol Lung Cell Mol Physiol 293: L1069–L1078, 2007.
37. Liu DY, Wu J, Zhang XY, Feng ZC. [Expression of IL-8, SP-A and TGF-beta1 in bronchoalveolar lavage fluid of neonates with bronchopulmonary dysplasia]. Zhongguo Dang Dai Er Ke Za Zhi 12: 444–446, 2010.
38. Lofqvist C, Hellgren G, Niklasson A, Engstrom E, Ley D, Hansen- Pupp I, Consortium W. Low postnatal serum IGF-I levels are associated with bronchopulmonary dysplasia (BPD). Acta Paediatr 101: 1211–1216, 2012.
39. Lu HY, Shao GB, Li WB, Wang H. Effects of hyperoxia on transdifferentiation of primary cultured type II alveolar epithelial cells from premature rats. In Vitro Cell Dev Biol Anim 47: 64–72, 2011.
40. Madurga A, Mizikova I, Ruiz-Camp J, Morty RE. Recent advances in late lung development and the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 305: L893–L905, 2013.
41. McGrath-Morrow SA, Stahl J. Apoptosis in neonatal murine lung exposed to hyperoxia. Am J Respir Cell Mol Biol 25: 150–155, 2001.
42. O’Reilly MA, Staversky RJ, Finkelstein JN, Keng PC. Activation of the G2 cell cycle checkpoint enhances survival of epithelial cells exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 284: L368–L375, 2003.
43. Perez-Gil J, Weaver TE. Pulmonary surfactant pathophysiology: current models and open questions. Physiology 25: 132–141, 2010.
44. Qiao R, Yan W, Clavijo C, Mehrian-Shai R, Zhong Q, Kim KJ, Ann D, Crandall ED, Borok Z. Effects of KGF on alveolar epithelial cell transdifferentiation are mediated by JNK signaling. Am J Respir Cell Mol Biol 38: 239–246, 2008.
45. Randell SH, Mercer RR, Young SL. Neonatal hyperoxia alters the pulmonary alveolar and capillary structure of 40-day-old rats. Am J Pathol 136: 1259–1266, 1990.
46. Roper JM, Mazzatti DJ, Watkins RH, Maniscalco WM, Keng PC, O’Reilly MA. In vivo exposure to hyperoxia induces DNA damage in a population of alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 286: L1045–L1054, 2004.
47. Schneeberger EE, Lynch RD. Structure, function, and regulation of cellular tight junctions. Am J Physiol 262: L647–L661, 1992.
48. Schneider JP, Ochs M. Alterations of mouse lung tissue dimensions during processing for morphometry: a comparison of methods. Am J Physiol Lung Cell Mol Physiol 306: L341–L350, 2014.
49. Stone KC, Mercer RR, Freeman BA, Chang LY, Crapo JD. Distribution of lung cell numbers and volumes between alveolar and nonalveolar tissue. Am Rev Respir Dis 146: 454–456, 1992.
50. Subramaniam M, Bausch C, Twomey A, Andreeva S, Yoder BA, Chang L, Crapo JD, Pierce RA, Cuttitta F, Sunday ME. Bombesin-like peptides modulate alveolarization and angiogenesis in bronchopulmonary dysplasia. Am J Respir Crit Care Med 176: 902–912, 2007.
51. Sun H, Choo-Wing R, Fan J, Leng L, Syed MA, Hare AA, Jorgensen WL, Bucala R, Bhandari V. Small molecular modulation of macrophage migration inhibitory factor in the hyperoxia-induced mouse model of bronchopulmonary dysplasia. Respir Res 14: 27, 2013.
52. Vicencio AG, Lee CG, Cho SJ, Eickelberg O, Chuu Y, Haddad GG, Elias JA. Conditional overexpression of bioactive transforming growth factor-beta1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia? Am J Respir Cell Mol Biol 31: 650–656, 2004.
53. Warburton D, Bellusci S. The molecular genetics of lung morphogenesis and injury repair. Paediatr Respir Rev 5, Suppl A: S283–S287, 2004.
54. Wikenheiser KA, Wert SE, Wispe JR, Stahlman M, D’Amore-Bruno M, Singh G, Katyal SL, Whitsett JA. Distinct effects of oxygen on surfactant protein B expression in bronchiolar and alveolar epithelium. Am J Physiol 262: L32–L39, 1992.
55. Willis BC, duBois RM, Borok Z. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc Am Thorac Soc 3: 377–382, 2006.
56. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, Borok Z. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 166: 1321–1332, 2005.
57. Wright JR, Hawgood S. Pulmonary surfactant metabolism. Clin Chest Med 10: 83–93, 1989.
58. Xu W, Yang N, Pan L, Fu J, Xue X. The expression of HoxB5 and its role in neonatal rats with chronic lung disease. Fetal Pediatr Pathol 31: 11–20, 2012.
59. Yang H, Fu J, Xue X, Yao L, Qiao L, Hou A, Jin L, Xing Y. Epithelial-mesenchymal transitions in bronchopulmonary dysplasia of newborn rats. Pediatr Pulmonol 49: 1112–1123, 2014.
60. Yee M, Buczynski BW, O’Reilly MA. Neonatal Hyperoxia Stimulates the Expansion of Alveolar Epithelial Type II Cells. Am J Respir Cell Mol Biol 50: 757–766, 2014.
61. You K, Xu X, Fu J, Xu S, Yue X, Yu Z, Xue X. Hyperoxia disrupts pulmonary epithelial barrier in newborn rats via the deterioration of occludin and ZO-1. Respir Res 13: 36, 2012.
62. Yue X, Fu J, Xue X, Gao H, Liu D, Zong Z, Wang W, Li H, Yuan Z. Detection of p16 promoter methylation in premature rats with chronic lung disease induced by hyperoxia. Pediatr Int 52: 520–526, 2010.
63. Zhao L, Yee M, O’Reilly MA. Transdifferentiation of alveolar epithelial type II to type I cells is controlled by opposing TGF-β and BMP signaling. Am J Physiol Lung Cell Mol Physiol 305: L409–L418, 2013.