Neonatal hyperoxia stimulates the expansion of alveolar epithelial type II cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 4, 2014, Pages 757-766

  Yee, Min ^a   Buczynski, Bradley W ^a   O'Reilly, Michael A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Bronchopulmonary dysplasia; Neonatal hyperoxia; Persistent pulmonary disease; Proliferation; Type II epithelial cells

Indexed keywords

AQUAPORIN 5; CD31 ANTIGEN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA;

ADULT; AMBIENT AIR; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRDU ASSAY; CELL EXPANSION; CELL FATE; CELL LABELING; CELL POPULATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HYPEROXIA; LUNG ALVEOLUS EPITHELIUM; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION;

ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HYPEROXIA; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; PNEUMOCYTES; PROMOTER REGIONS, GENETIC; PULMONARY ALVEOLI; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; RNA, MESSENGER; TIME FACTORS; UTEROGLOBIN;

EID: 84896126300     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0207OC     Document Type: Article

References (57)

1. Eber E, Zach MS. Long term sequelae of bronchopulmonary dysplasia (chronic lung disease of infancy). Thorax 2001;56:317-323. (Pubitemid 32269815)
2. Bhatt AJ, Pryhuber GS, Huyck H, Watkins RH, Metlay LA, Maniscalco WM. Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and TIE-2 in human infants dying with bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;164:1971-1980. (Pubitemid 33152338)
3. Coalson JJ, Winter VT, Gerstmann DR, Idell S, King RJ, Delemos RA. Pathophysiologic, morphometric, and biochemical studies of the premature baboon with bronchopulmonary dysplasia. Am Rev Respir Dis 1992;145:872-881.
4. Maniscalco WM, Watkins RH, O'Reilly MA, Shea CP. Increased epithelial cell proliferation in very premature baboons with chronic lung disease. Am J Physiol Lung Cell Mol Physiol 2002;283:L991-L1001. (Pubitemid 35204891)
5. Warner BB, Stuart LA, Papes RA, Wispé JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol 1998;275:L110-L117.
6. 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 1975;32:619-635.
7. Thébaud 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. (Pubitemid 46741748)
8. Balasubramaniam V, Mervis CF, Maxey AM, Markham NE, Abman SH. Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: implications for the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2007;292:L1073-L1084. (Pubitemid 47084852)
9. 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 2006;118:108-113. (Pubitemid 46071153)
10. Robin B, Kim YJ, Huth J, Klocksieben J, Torres M, Tepper RS, Castile RG, Solway J, Hershenson MB, Goldstein-Filbrun A. Pulmonary function in bronchopulmonary dysplasia. Pediatr Pulmonol 2004;37:236-242. (Pubitemid 38326373)
11. Smith VC, Zupancic JA, McCormick MC, Croen LA, Greene J, Escobar GJ, Richardson DK. Rehospitalization in the first year of life among infants with bronchopulmonary dysplasia. J Pediatr 2004;144:799-803. (Pubitemid 38858099)
12. Weisman LE. Populations at risk for developing respiratory syncytial virus and risk factors for respiratory syncytial virus severity: infants with predisposing conditions. Pediatr Infect Dis J 2003;22:S33-S37; discussion S37-S39.
13. Doyle LW, Faber B, Callanan C, Morley R. Blood pressure in late adolescence and very low birth weight. Pediatrics 2003;111:252-257. (Pubitemid 36177140)
14. Cutz E, Chiasson D. Chronic lung disease after premature birth. N Engl J Med 2008;358:743-745, author reply 745-746.
15. Yee M, Vitiello PF, Roper JM, Staversky RJ, Wright TW, McGrath-Morrow SA, Maniscalco WM, Finkelstein JN, O'Reilly MA. Type II epithelial cells are critical target for hyperoxia-mediated impairment of postnatal lung development. Am J Physiol Lung Cell Mol Physiol 2006;291:L1101-L1111. (Pubitemid 44772072)
16. Schulman SR, Canada AT, Fryer AD, Winsett DW, Costa DL. Airway hyperreactivity produced by short-term exposure to hyperoxia in neonatal guinea pigs. Am J Physiol 1997;272:L1211-L1216.
17. McGrath-Morrow SA, Cho C, Soutiere S, Mitzner W, Tuder R. The effect of neonatal hyperoxia on the lung of p21Waf1/Cip1/Sdi1-deficient mice. Am J Respir Cell Mol Biol 2004;30:635-640. (Pubitemid 38591214)
18. Denis D, Fayon MJ, Berger P, Molimard M, De Lara MT, Roux E, Marthan R. Prolonged moderate hyperoxia induces hyperresponsiveness and airway inflammation in newborn rats. Pediatr Res 2001;50:515-519. (Pubitemid 32911343)
19. 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 2003;123:530-538. (Pubitemid 36269441)
20. Yee M, Chess PR, McGrath-Morrow SA, Wang Z, Gelein R, Zhou R, Dean DA, Notter RH, O'Reilly MA. Neonatal oxygen adversely affects lung function in adult mice without altering surfactant composition or activity. Am J Physiol Lung Cell Mol Physiol 2009;297:L641-L649.
21. Buczynski BW, Yee M, Paige Lawrence B, O'Reilly MA. Lung development and the host response to influenza A virus are altered by different doses of neonatal oxygen in mice. Am J Physiol Lung Cell Mol Physiol 2012;302:L1078- L1087.
22. Yee M, White RJ, Awad HA, Bates WA, McGrath-Morrow SA, O'Reilly MA. Neonatal hyperoxia causes pulmonary vascular disease and shortens life span in aging mice. Am J Pathol 2011;178:2601-2610.
23. O'Reilly MA, Marr SH, Yee M, McGrath-Morrow SA, Lawrence BP. Neonatal hyperoxia enhances the inflammatory response in adult mice infected with influenza A virus. Am J Respir Crit Care Med 2008;177:1103-1110. (Pubitemid 351717569)
24. Giannandrea M, Yee M, O'Reilly MA, Lawrence BP. Memory CD8+ T cells are sufficient to alleviate impaired host resistance to influenza A virus infection caused by neonatal oxygen supplementation. Clin Vaccine Immunol 2012;19:1432-1441.
25. 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 1980;122:123-143. (Pubitemid 10073551)
26. Lo B, Hansen S, Evans K, Heath JK, Wright JR. Alveolar epithelial type II cells induce T cell tolerance to specific antigen. J Immunol 2008;180:881-888.
27. Perl AK, Tichelaar JW, Whitsett JA. Conditional gene expression in the respiratory epithelium of the mouse. Transgenic Res 2002;11:21-29. (Pubitemid 34152360)
28. Kolla V, Gonzales LW, Gonzales J, Wang P, Angampalli S, Feinstein SI, Ballard PL. Thyroid transcription factor in differentiating type II cells: regulation, isoforms, and target genes. Am J Respir Cell Mol Biol 2007;36:213-225. (Pubitemid 46233475)
29. Liu CW, Corboy MJ, DeMartino GN, Thomas PJ. Endoproteolytic activity of the proteasome. Science 2003;299:408-411. (Pubitemid 36120047)
30. Amy RW, Bowes D, Burri PH, Haines J, Thurlbeck WM. Postnatal growth of the mouse lung. J Anat 1977;124:131-151. (Pubitemid 8187543)
31. Kauffman SL, Burri PH, Weibel ER. The postnatal growth of the rat lung. II. Autoradiography. Anat Rec 1974;180:63-76.
32. Perl AK, Wert SE, Loudy DE, Shan Z, Blair PA, Whitsett JA. Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. Am J Respir Cell Mol Biol 2005;33:455-462. (Pubitemid 41572688)
33. Yi M, Jankov RP, Belcastro R, Humes D, Copland I, Shek S, Sweezey NB, Post M, Albertine KH, Auten RL, et al. Opposing effects of 60% oxygen and neutrophil influx on alveologenesis in the neonatal rat. Am J Respir Crit Care Med 2004;170:1188-1196. (Pubitemid 39577377)
34. Sisson TH, Hansen JM, Shah M, Hanson KE, Du M, Ling T, Simon RH, Christensen PJ. Expression of the reverse tetracycline-transactivator gene causes emphysema-like changes in mice. Am J Respir Cell Mol Biol 2006;34:552-560.
35. Otto-Verberne CJ, Ten Have-Opbroek AA, Willems LN, Franken C, Kramps JA, Dijkman JH. Lack of type ii cells and emphysema in human lungs. Eur Respir J 1991;4:316-323.
36. McCormack FX, Whitsett JA. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J Clin Invest 2002;109:707-712. (Pubitemid 34263144)
37. Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2001;2:33-46. (Pubitemid 34187905)
38. Yee M, Buczynski BW, Lawrence BP, O'Reilly MA. Neonatal hyperoxia increases sensitivity of adult mice to bleomycin-induced lung fibrosis. Am J Respir Cell Mol Biol 2013;48:258-266.
39. O'Reilly MA, Yee M, Buczynski BW, Vitiello PF, Keng PC, Welle SL, Finkelstein JN, Dean DA, Lawrence BP. Neonatal oxygen increases sensitivity to influenza A virus infection in adult mice by suppressing epithelial expression of Ear1. Am J Pathol 2012;181:441-451.
40. Auten RL, Mason SN, Auten KM, Brahmajothi M. Hyperoxia impairs postnatal alveolar epithelial development via NADPH oxidase in newborn mice. Am J Physiol Lung Cell Mol Physiol 2009;297:L134-L142.
41. O'Reilly MA. DNA damage and cell cycle checkpoints in hyperoxic lung injury: braking to facilitate repair. Am J Physiol Lung Cell Mol Physiol 2001;281:L291-L305.
42. Auten RL, Whorton MH, Nicholas Mason S. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol 2002;26:391-397. (Pubitemid 34253922)
43. Lee PJ, Choi AM. Pathways of cell signaling in hyperoxia. Free Radic Biol Med 2003;35:341-350. (Pubitemid 37289165)
44. Maniscalco WM, Watkins RH, Finkelstein JN, Campbell MH. Vascular endothelial growth factor mRNA increases in alveolar epithelial cells during recovery from oxygen injury. Am J Respir Cell Mol Biol 1995;13:377-386.
45. Kauffman SL. Kinetics of pulmonary epithelial proliferation during prenatal growth of the mouse lung. Anat Rec 1975;183:393-403.
46. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, Wang F, Hogan BL. The role of Scgb1a11 Clara cells in the long-term maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 2009;4:525-534.
47. Rancourt RC, Hayes DD, Chess PR, Keng PC, O'Reilly MA. Growth arrest in G1 protects against oxygen-induced DNA damage and cell death. J Cell Physiol 2002;193:26-36. (Pubitemid 34969125)
48. Zuzarte-Luis V, Hurle JM. Programmed cell death in the embryonic vertebrate limb. Semin Cell Dev Biol 2005;16:261-269. (Pubitemid 40432127)
49. Vanderhaeghen P, Cheng HJ. Guidance molecules in axon pruning and cell death. Cold Spring Harb Perspect Biol 2010;2:a001859.
50. Watson CJ, Kreuzaler PA. Remodeling mechanisms of the mammary gland during involution. Int J Dev Biol 2011;55:757-762.
51. Jenkinson SG. Oxygen toxicity. New Horiz 1993;1:504-511.
52. Schittny JC, Djonov V, Fine A, Burri PH. Programmed cell death contributes to postnatal lung development. Am J Respir Cell Mol Biol 1998;18:786-793. (Pubitemid 128358425)
53. Minoo P, Segura L, Coalson JJ, King RJ, DeLemos RA. Alterations in surfactant protein gene expression associated with premature birth and exposure to hyperoxia. Am J Physiol 1991;261:L386-L392.
54. Awasthi S, Coalson JJ, Crouch E, Yang F, King RJ. Surfactant proteins A and D in premature baboons with chronic lung injury (Bronchopulmonary dysplasia): evidence for an inhibition of secretion. Am J Respir Crit Care Med 1999;160:942-949. (Pubitemid 29442035)
55. White CW, Greene KE, Allen CB, Shannon JM. Elevated expression of surfactant proteins in newborn rats during adaptation to hyperoxia. Am J Respir Cell Mol Biol 2001;25:51-59. (Pubitemid 32682705)
56. Woods E, Ohashi T, Polk D, Ikegami M, Ueda T, Jobe AH. Surfactant treatment and ventilation effects on surfactant SP-A, SP-B, and SP-C mRNA levels in preterm lamb lungs. Am J Physiol 1995;269:L209-L214.
57. Boggaram V. Regulation of surfactant protein gene expression by hyperoxia in the lung. Antioxid Redox Signal 2004;6:185-190. (Pubitemid 38063990)