Protein expression profile of rat type two alveolar epithelial cells during hyperoxic stress and recovery

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 305, Issue 9, 2013, Pages

  Bhargava, Maneesh ^a   Dey, Sanjoy ^b   Becker, Trisha ^a   Steinbach, Michael ^b   Wu, Baolin ^d   Lee, Sang Mee ^d   Higgins, LeeAnn ^c   Kumar, Vipin ^b   Bitterman, Peter B ^a   Ingbar, David H ^a   Wendt, Christine H ^a,c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b University of Minnesota   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acute respiratory distress syndrome; Alveolar epithelial cell proteome; Bioinformatics; Hyperoxia

Indexed keywords

ALKALINE PHOSPHATASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; SURFACTANT PROTEIN A; SURFACTANT PROTEIN B; SURFACTANT PROTEIN C; SURFACTANT PROTEIN D;

ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; HYPEROXIA; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; RAT; TANDEM MASS SPECTROMETRY; UBIQUITINATION;

ACUTE RESPIRATORY DISTRESS SYNDROME; ALVEOLAR EPITHELIAL CELL PROTEOME; BIOINFORMATICS; HYPEROXIA;

ACUTE LUNG INJURY; ALGORITHMS; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HYPEROXIA; MALE; OXIDATIVE STRESS; OXYGEN; PROTEOMICS; PULMONARY ALVEOLI; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUCOSA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSCRIPTOME;

EID: 84886997922     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00079.2013     Document Type: Article

References (61)

1. Adamson IY, Bowden DH. The type 2 cell as progenitor of alveolar epithelial regeneration. A cytodynamic study in mice after exposure to oxygen. Lab Invest 30: 35-42, 1974.
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. Akkina SK, Zhang Y, Nelsestuen GL, Oetting WS, Ibrahlm HN. Temporal stability of the urinary proteome after kidney transplant: more sensitive than protein composition? J Proteome Res 8: 94-103, 2009.
4. Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet 2: 319-323, 1967.
5. Barazzone C, Donati Y, Boccard J, Rochat A, Vestin C, Kan C, Piguet P. CD40-CD40 ligand disruption does not prevent hyperoxia-induced injury. Am J Pathol 160: 67-71, 2002.
6. Barazzone C, Horowitz S, Donati YR, Rodriguez I, Piguet PF. Oxygen toxicity in mouse lung: pathways to cell death. Am J Respir Cell Mol Biol 19: 573-581, 1998.
7. Barazzone C, Tacchini-Cottier F, Vesin C, Rochat AF, Piguet PF. Hyperoxia induces platelet activation and lung sequestration: an event dependent on tumor necrosis factor-alpha and CD11a. Am J Respir Cell Mol Biol 15: 107-114, 1996.
8. Barber RE, Lee J, Hamilton WK. Oxygen toxicity in man. A prospective study in patients with irreversible brain damage. N Engl J Med 283: 1478-1484, 1970.
9. Benjamini Y. Discovering the false discovery rate. J R Statist Soc B 72: 405-416, 2010.
10. Bhargava M, Runyon MR, Smirnov D, Lei J, Groppoli TJ, Mariash CN, Wangensteen OD, Ingbar DH. Triiodo-L-thyronine rapidly stimulates alveolar fluid clearance in normal and hyperoxia-injured lungs. Am J Respir Crit Care Med 178: 506-512, 2008.
11. Bitterman PB, Polunovsky VA, Ingbar DH. Repair after acute lung injury. Chest 105: 118S-121S, 1994.
12. Budinger GR, Mutlu GM, Urich D, Soberanes S, Buccellato LJ, Hawkins K, Chiarella SE, Radigan KA, Eisenbart J, Agrawal H, Berkelhamer S, Hekimi S, Zhang J, Perlman H, Schumacker PT, Jain M, Chandel NS. Epithelial cell death is an important contributor to oxidant-mediated acute lung injury. Am J Respir Crit Care Med 183: 1043-1054, 2011.
13. Carter EP, Wangensteen OD, O'Grady SM, Ingbar DH. Effects of hyperoxia on type II cell Na-K-ATPase function and expression. Am J Physiol Lung Cell Mol Physiol 272: L542-L551, 1997.
14. Cha S, Imielinski MB, Rejtar T, Richardson EA, Thakur D, Sgroi DC, Karger BL. In situ proteomic analysis of human breast cancer epithelial cells using laser capture microdissection: annotation by protein set enrichment analysis and gene ontology. Mol Cell Proteomics 9: 2529-2544, 2010.
15. Chambrion C, Le Naour F. The tetraspanins CD9 and CD81 regulate CD9P1-induced effects on cell migration. PLoS One 5: e11219, 2010.
16. Chen Z, Chintagari NR, Guo Y, Bhaskaran M, Chen J, Gao L, Jin N, Weng T, Liu L. Gene expression of rat alveolar type II cells during hyperoxia exposure and early recovery. Free Radic Biol Med 43: 628-642, 2007.
17. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL2 family reunion. Mol Cell 37: 299-310, 2010.
18. Comellas AP, Dada LA, Lecuona E, Pesce LM, Chandel NS, Quesada N, Budinger GR, Strous GJ, Ciechanover A, Sznajder JI. Hypoxiamediated degradation of Na, K-ATPase via mitochondrial reactive oxygen species and the ubiquitin-conjugating system. Circ Res 98: 1314-1322, 2006.
19. Crapo JD. Morphologic changes in pulmonary oxygen toxicity. Annu Rev Physiol 48: 721-731, 1986.
20. 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.
21. Crosby LM, Waters CM. Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol 298: L715-L731, 2010.
22. D'Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, Pipeling MR, Brower RG, Tuder RM, McDyer JF, King LS. CD4 CD25 Foxp3 Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 119: 2898-2913, 2009.
23. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 116: 205-219, 2004.
24. Davis WB, Rennard SI, Bitterman PB, Crystal RG. Pulmonary oxygen toxicity. Early reversible changes in human alveolar structures induced by hyperoxia. N Engl J Med 309: 878-883, 1983.
25. De Paepe ME, Mao Q, Chao Y, Powell JL, Rubin LP, Sharma S. Hyperoxia-induced apoptosis and Fas/FasL expression in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 289: L647-L659, 2005.
26. Dobbs LG. Isolation and culture of alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 258: L134-L147, 1990.
27. Ernst J, Bar-Joseph Z. STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7: 191, 2006.
28. Factor P, Dumasius V, Saldias F, Brown LA, Sznajder JI. Adenovirusmediated transfer of an Na/K-ATPase beta1 subunit gene improves alveolar fluid clearance and survival in hyperoxic rats. Hum Gene Ther 11: 2231-2242, 2000.
29. Helenius IT, Dada LA, Sznajder JI. Role of ubiquitination in Na, KATPase regulation during lung injury. Proc Am Thorac Soc 7: 65-70, 2010.
30. Hemler ME. Targeting of tetraspanin proteins-potential benefits and strategies. Nat Rev Drug Discov 7: 747-758, 2008.
31. Holm BA, Matalon S, Finkelstein JN, Notter RH. Type II pneumocyte changes during hyperoxic lung injury and recovery. J Appl Physiol 65: 2672-2678, 1988.
32. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.
33. Kapanci Y, Tosco R, Eggermann J, Gould VE. Oxygen pneumonitis in man. Light-and electron-microscopic morphometric studies. Chest 62: 162-169, 1972.
34. Kapanci Y, Weibel ER, Kaplan HP, Robinson FR. Pathogenesis and reversibility of the pulmonary lesions of oxygen toxicity in monkeys. II. Ultrastructural and morphometric studies. Lab Invest 20: 101-118, 1969.
35. Kotha J, Zhang C, Longhurst CM, Lu Y, Jacobs J, Cheng Y, Jennings LK. Functional relevance of tetraspanin CD9 in vascular smooth muscle cell injury phenotypes: a novel target for the prevention of neointimal hyperplasia. Atherosclerosis 203: 377-386, 2009.
36. Lecuona E, Sun H, Vohwinkel C, Ciechanover A, Sznajder JI. Ubiquitination participates in the lysosomal degradation of Na, K-ATPase in steady-state conditions. Am J Respir Cell Mol Biol 41: 671-679, 2009.
37. Lesur O, Arsalane K, Lane D. Lung alveolar epithelial cell migration in vitro: modulators and regulation processes. Am J Physiol Lung Cell Mol Physiol 270: L311-L319, 1996.
38. Li Z, Choo-Wing R, Sun H, Sureshbabu A, Sakurai R, Rehan VK, Bhandari V. A potential role of the JNK pathway in hyperoxia-induced cell death, myofibroblast transdifferentiation and TGF-beta1-mediated injury in the developing murine lung. BMC Cell Biol 12: 54, 2011.
39. Longhurst CM, Jacobs JD, White MM, Crossno JT Jr, Fitzgerald DA, Bao J, Fitzgerald TJ, Raghow R, Jennings LK. Chinese hamster ovary cell motility to fibronectin is modulated by the second extracellular loop of CD9. Identification of a putative fibronectin binding site. J Biol Chem 277: 32445-32452, 2002.
40. Mangeat P, Roy C, Martin M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol 9: 187-192, 1999.
41. Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295: L379-L399, 2008.
42. McCulloch CE, Shayle Searle R, Nehaus John M. Generalized, Linear, and Mixed Models. Hoboken, NJ: Wiley Interscience, 2008.
43. Morris PE, Glass J, Cross R, Cohen DA. Role of T-lymphocytes in the resolution of endotoxin-induced lung injury. Inflammation 21: 269-278, 1997.
44. 2-terminal kinase signaling pathway confers susceptibility to hyperoxic lung injury in mice. Am J Physiol Lung Cell Mol Physiol 285: L250-L257, 2003.
45. Niggli V, Rossy J. Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton. Int J Biochem Cell Biol 40: 344-349, 2008.
46. Nogee LM, Wispe JR, Clark JC, Weaver TE, Whitsett JA. Increased expression of pulmonary surfactant proteins in oxygen-exposed rats. Am J Respir Cell Mol Biol 4: 102-107, 1991.
47. O'Brien-Ladner AR, Nelson ME, Cowley BD Jr, Bailey K, Wesselius LJ. Hyperoxia amplifies TNF-alpha production in LPS-stimulated human alveolar macrophages. Am J Respir Cell Mol Biol 12: 275-279, 1995.
48. Okayama T, Kikuchi S, Ochiai T, Ikoma H, Kubota T, Ichikawa D, Fujiwara H, Okamoto K, Sakakura C, Sonoyama T, Kokuba Y, Doi Y, Tsukita S, Bissell DM, Otsuji E. Attenuated response to liver injury in moesin-deficient mice: impaired stellate cell migration and decreased fibrosis. Biochim Biophys Acta 1782: 542-548, 2008.
49. Rotin D, Staub O. Role of the ubiquitin system in regulating ion transport. Pflügers Arch 461: 1-21, 2011.
50. Sala-Valdes M, Ursa A, Charrin S, Rubinstein E, Hemler ME, Sanchez-Madrid F, Yanez-Mo M. EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrinradixin-moesin proteins. J Biol Chem 281: 19665-19675, 2006.
51. Shaw AR, Domanska A, Mak A, Gilchrist A, Dobler K, Visser L, Poppema S, Fliegel L, Letarte M, Willett BJ. Ectopic expression of human and feline CD9 in a human B cell line confers beta 1 integrindependent motility on fibronectin and laminin substrates and enhanced tyrosine phosphorylation. J Biol Chem 270: 24092-24099, 1995.
52. Shea LM, Beehler C, Schwartz M, Shenkar R, Tuder R, Abraham E. Hyperoxia activates NF-kappaB and increases TNF-alpha and IFN-gamma gene expression in mouse pulmonary lymphocytes. J Immunol 157: 3902-3908, 1996.
53. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 6: 1638-1655, 2007.
54. Staub O, Dho S, Henry P, Correa J, Ishikawa T, McGlade J, Rotin D. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na channel deleted in Liddle's syndrome. EMBO J 15: 2371-2380, 1996.
55. Staub O, Rotin D. Role of ubiquitylation in cellular membrane transport. Physiol Rev 86: 669-707, 2006.
56. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550, 2005.
57. Taylor CF, Paton NW, Lilley KS, Binz PA, Julian RK Jr, Jones AR, Zhu W, Apweiler R, Aebersold R, Deutsch EW, Dunn MJ, Heck AJ, Leitner A, Macht M, Mann M, Martens L, Neubert TA, Patterson SD, Ping P, Seymour SL, Souda P, Tsugita A, Vandekerckhove J, Vondriska TM, Whitelegge JP, Wilkins MR, Xenarios I, Yates JR, 3rd, Hermjakob H. The minimum information about a proteomics experiment (MIAPE). Nat Biotechnol 25: 887-893, 2007.
58. Thet LA, Parra SC, Shelburne JD. Sequential changes in lung morphology during the repair of acute oxygen-induced lung injury in adult rats. Exp Lung Res 11: 209-228, 1986.
59. Vadasz I, Weiss CH, Sznajder JI. Ubiquitination and proteolysis in acute lung injury. Chest 141: 763-771, 2012.
60. Vosa U, Vooder T, Kolde R, Fischer K, Valk K, Tonisson N, Roosipuu R, Vilo J, Metspalu A, Annilo T. Identification of miR-374a as a prognostic marker for survival in patients with early-stage nonsmall cell lung cancer. Genes Chromosomes Cancer 50: 812-822, 2011.
61. Zhang Y, Wendt CH, Hertz MI, Nelsestuen GL. Identification and validation of proteinase-3 and latent matrix-metalloproteinase 9 as potential biomarkers for chronic lung transplant rejection. Clin Proteomics 3: 3-12, 2007.