Surfactant protein-C chromatin-bound green fluorescence protein reporter mice reveal heterogeneity of surfactant protein C-expressing lung cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 3, 2013, Pages 288-298

  Lee, Joo Hyeon ^a,b,c   Kim, Jonghwan ^a   Gludish, David ^a,b,c   Roach, Rebecca R ^a,b,c   Saunders, Arven H ^a,b,c   Barrios, Juliana ^a,b,c   Woo, Andrew Jonghan ^a   Chen, Huaiyong ^d   Conner, David A ^b   Fujiwara, Yuko ^a   Stripp, Barry R ^d   Kim, Carla F ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alveolar Type II cells; Differentiation; Epithelial; GFP; SPC

Indexed keywords

CD74 ANTIGEN; GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN REPORTER; MATRIGEL; SURFACTANT PROTEIN C; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BRONCHIOLE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; LUNG ALVEOLUS CELL; LUNG FIBROBLAST; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; STEM CELL;

ALLELES; ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BRONCHIOLES; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELLS, CULTURED; CHROMATIN; EPITHELIAL CELLS; FEMALE; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; LUNG; LUNG INJURY; MALE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; PULMONARY ALVEOLI; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C; REGENERATION; RESPIRATORY MUCOSA;

EID: 84874899241     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0403OC     Document Type: Article

References (47)

1. Stripp BR, Reynolds SD. Maintenance and repair of the bronchiolar epithelium. Proc Am Thorac Soc 2008;5:328-333.
2. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. In vivo differentiation potential of tracheal basal cells: evidence for multipotent and unipotent subpopulations. Am J Physiol Lung Cell Mol Physiol 2004;286:L643-L649.
3. Hong KU, Reynolds SD, Watkins S, Fuchs E, Stripp BR. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am J Pathol 2004;164:577-588.
4. Rawlins EL, Okubo T, Xue Y, Brass DM, Auten RL, Hasegawa H, Wang F, Hogan BL. The role of SCGB1A11 Clara cells in the longterm maintenance and repair of lung airway, but not alveolar, epithelium. Cell Stem Cell 2009;4:525-534.
5. Reynolds SD, Hong KU, Giangreco A, Mango GW, Guron C, Morimoto Y, Stripp BR. Conditional Clara cell ablation reveals a self-renewing progenitor function of pulmonary neuroendocrine cells. Am J Physiol Lung Cell Mol Physiol 2000;278:L1256-L1263.
6. Hong KU, Reynolds SD, Giangreco A, Hurley CM, Stripp BR. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 2001;24:671-681.
7. Reynolds SD, Giangreco A, Power JH, Stripp BR. Neuroepithelial bodies of pulmonary airways serve as a reservoir of progenitor cells capable of epithelial regeneration. Am J Pathol 2000;156:269-278.
8. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 2011;108:E1475-E1483.
9. Tropea KA, Leder E, Aslam M, Lau AN, Raiser DM, Lee JH, Balasubramaniam V, Fredenburgh LE, Mitsialis SA, Kourembanas S, et al. Bronchioalveolar stem cells increase after mesenchymal stromal cell treatment in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2012;302:L829-L837.
10. Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-835.
11. Williams MC. Alveolar Type I cells: molecular phenotype and development. Annu Rev Physiol 2003;65:669-695.
12. Gonzalez RF, Allen L, Dobbs LG. Rat alveolar Type I cells proliferate, express OCT-4, and exhibit phenotypic plasticity in vitro. Am J Physiol Lung Cell Mol Physiol 2009;297:L1045-L1055.
13. Fehrenbach H. Alveolar epithelial Type II cell: defender of the alveolus revisited. Respir Res 2001;2:33-46.
14. 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 1974;30:35-42.
15. Evans MJ, Cabral LJ, Stephens RJ, Freeman G. Transformation of alveolar Type 2 cells to Type 1 cells following exposure to NO2. Exp Mol Pathol 1975;22:142-150.
16. Brody JS, Burki R, Kaplan N. Deoxyribonucleic acid synthesis in lung cells during compensatory lung growth after pneumonectomy. Am Rev Respir Dis 1978;117:307-316.
17. Reddy R, Buckley S, Doerken M, Barsky L,Weinberg K, Anderson KD, Warburton D, Driscoll B. Isolation of a putative progenitor subpopulation of alveolar epithelial Type 2 cells. Am J Physiol Lung Cell Mol Physiol 2004;286:L658-L667.
18. Adamson IY, Bowden DH. Derivation of Type 1 epithelium from Type 2 cells in the developing rat lung. Lab Invest 1975;32:736-745.
19. Reynolds SD, Giangreco A, Hong KU, McGrath KE, Ortiz LA, Stripp BR. Airway injury in lung disease pathophysiology: selective depletion of airway stem and progenitor cell pools potentiates lung inflammation and alveolar dysfunction. Am J Physiol Lung Cell Mol Physiol 2004;287:L1256-L1265.
20. Londhe VA, Maisonet TM, Lopez B, Jeng JM, Li C, Minoo P. A subset of epithelial cells with CCSP promoter activity participates in alveolar development. Am J Respir Cell Mol Biol 2011;44:804-812.
21. Chapman HA, Li X, Alexander JP, Brumwell A, Lorizio W, Tan K, Sonnenberg A, Wei Y, Vu TH. Integrin alpha6beta4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Invest 2011;121:2855-2862.
22. Leary JF, Finkelstein JN, Notter RH, Shapiro DL. Isolation of Type II pneumocytes by laser flow cytometry. Am Rev Respir Dis 1982;125: 326-330.
23. Wilson JS, Steinkamp JA, Lehnert BE. Isolation of viable Type II alveolar epithelial cells by flow cytometry. Cytometry 1986;7:157-162.
24. Funkhouser JD, Cheshire LB, Ferrara TB, Peterson RD. Monoclonal antibody identification of a Type II alveolar epithelial cell antigen and expression of the antigen during lung development. Dev Biol 1987; 119:190-198.
25. Harrison JH Jr., Porretta CP, Leming K. Purification of murine pulmonary Type II cells for flow cytometric cell cycle analysis. Exp Lung Res 1995;21:407-421.
26. CortiM, Brody AR, Harrison JH. Isolation and primary culture of murine alveolar Type II cells. Am J Respir Cell Mol Biol 1996;14:309-315.
27. Roper JM, Staversky RJ, Finkelstein JN, Keng PC, O'Reilly MA. Identification and isolation of mouse Type II cells on the basis of intrinsic expression of enhanced green fluorescent protein. Am J Physiol Lung Cell Mol Physiol 2003;285:L691-L700.
28. 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.
29. Teisanu RM, Chen H, Matsumoto K, McQualter JL, Potts E, Foster WM, Bertoncello I, Stripp BR. Functional analysis of two distinct bronchiolar progenitors during lung injury and repair. Am J Respir Cell Mol Biol 2011;44:794-803.
30. Glasser SW, Burhans MS, Eszterhas SK, Bruno MD, Korfhagen TR. Human SP-C gene sequences that confer lung epithelium-specific expression in transgenic mice. Am J Physiol Lung Cell Mol Physiol 2000;278:L933-L945.
31. Glasser SW, Korfhagen TR, Wert SE, Bruno MD, McWilliams KM, Vorbroker DK, Whitsett JA. Genetic element from human surfactant protein SP-C gene confers bronchiolar-alveolar cell specificity in transgenic mice. Am J Physiol 1991;261:L349-L356.
32. Glasser SW, Eszterhas SK, Detmer EA,MaxfieldMD, Korfhagen TR. The murine SP-C promoter directs Type II cell-specific expression in transgenic mice. Am J Physiol Lung Cell Mol Physiol 2005;288:L625-L632.
33. Leslie CC, McCormick-Shannon K, Robinson PC, Mason RJ. Stimulation of DNA synthesis in cultured rat alveolar Type II cells. Exp Lung Res 1985;8:53-66.
34. Leslie CC, McCormick-Shannon K, Mason RJ, Shannon JM. Proliferation of rat alveolar epithelial cells in low density primary culture. Am J Respir Cell Mol Biol 1993;9:64-72.
35. Uhal BD, Flowers KM, Rannels DE. Type II pneumocyte proliferation in vitro: problems and future directions. Am J Physiol 1991; 261(4, Suppl)110-117.
36. Sugahara K, Mason RJ, Shannon JM. Effects of soluble factors and extracellular matrix on DNA synthesis and surfactant gene expression in primary cultures of rat alveolar Type II cells. Cell Tissue Res 1998; 291:295-303.
37. Shannon JM, Jennings SD, Nielsen LD. Modulation of alveolar Type II cell differentiated function in vitro. Am J Physiol 1992;262:L427-L436.
38. Diglio CA, Kikkawa Y. The Type II epithelial cells of the lung: IV. Adaption and behavior of isolated Type II cells in culture. Lab Invest 1977;37:622-631.
39. Mason RJ, Dobbs LG. Synthesis of phosphatidylcholine and phosphatidylglycerol by alveolar Type II cells in primary culture. J Biol Chem 1980;255:5101-5107.
40. Dobbs LG, Williams MC, Brandt AE. Changes in biochemical characteristics and pattern of lectin binding of alveolar Type II cells with time in culture. Biochim Biophys Acta 1985;846:155-166.
41. Mason RJ, Dobbs LG, Greenleaf RD, Williams MC. Alveolar Type II cells. Fed Proc 1977;36:2697-2702.
42. Copeland NG, Jenkins NA, Court DL. Recombineering: a powerful new tool for mouse functional genomics. Nat Rev Genet 2001;2:769-779.
43. Kanda T, Sullivan KF, Wahl GM. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr Biol 1998;8:377-385.
44. McQualter JL, Yuen K, Williams B, Bertoncello I. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 2011;107:1414-1419.
45. Gonzalez R, Yang YH, Griffin C, Allen L, Tigue Z, Dobbs L. Freshly isolated rat alveolar Type I cells, Type II cells, and cultured Type II cells have distinct molecular phenotypes. Am J Physiol Lung Cell Mol Physiol 2005;288:L179-L189.
46. Rawlins EL. Lung epithelial progenitor cells: lessons from development. Proc Am Thorac Soc 2008;5:675-681.
47. Marsh LM, Cakarova L, Kwapiszewska G, von Wulffen W, Herold S, Seeger W, Lohmeyer J. Surface expression of CD74 by Type II alveolar epithelial cells: a potential mechanism for macrophage migration inhibitory factor-induced epithelial repair. Am J Physiol Lung Cell Mol Physiol 2009;296:L442-L452.