Efficient derivation of alveolar type ii cells from embryonic stem cells for in vivo application

Tissue Engineering - Part A

Volumn 15, Issue 11, 2009, Pages 3351-3365

  Roszell, Blair ^a,b   Mondrinos, Mark J ^a   Seaton, Ariel ^b   Simons, Donald M ^a   Koutzaki, Sirma H ^a   Fong, Guo Hua ^b   Lelkes, Peter I ^a   Finck, Christine M ^b,c  

^a DREXEL UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c Farmington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL ORGANS; CELL CULTURE; GLYCOPROTEINS; TISSUE;

A549 CELLS; CELL SEEDING; CONDITIONED MEDIUM; CULTURE METHODS; DOSE-DEPENDENT; EMBRYOID BODY; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTOR 2; IN-CELL; IN-VIVO; LUNG CELLS; LUNG EPITHELIAL CELLS; MOUSE EMBRYONIC STEM CELLS; RAPID DIFFERENTIATION; SEEDING METHOD; TYPE II;

CELLS;

ACTIVIN; FIBROBLAST GROWTH FACTOR 2; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOSE RESPONSE; EMBRYONIC STEM CELL; ENDODERM; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LAMELLAR BODY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

MUS;

EID: 72649085849     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0664     Document Type: Article

References (55)

1. Compernolle, V., Brusselmans, K., Acker, T., Hoet, P., Tjwa, M., Beck, H., Plaisance, S., Dor, Y., Keshet, E., Lupu, F., Nemery, B., Dewerchin, M., Van Veldhoven, P., Plate, K., Moons, L., Collen, D., and Carmeliet, P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8, 702, 2002.
2. Halvorsen, T., Skadberg, B.T., Eide, G.E., Roksund, O.D., and Markestad, T. Better care of immature infants; has it influenced long-term pulmonary outcome? Acta Paediatr 95, 547, 2006.
3. Doyle, L.W., Faber, B., Callanan, C., Freezer, N., Ford, G.W., and Davis, N.M. Bronchopulmonary dysplasia in very low birth weight subjects and lung function in late adolescence. Pediatrics 118, 108, 2006.
4. Vento, G., Matassa, P.G., Ameglio, F., Capoluongo, E., Tor-torolo, L., and Romagnoli, C. Effects of early dexamethasone therapy on pulmonary fibrogenic mediators and respiratory mechanicsinpreterminfants.EurCytokineNetw13,207,2002.
5. Jobe, A.H. Animal models of antenatal corticosteroids: clinical implications. Clin Obstet Gynecol 46, 174, 2003.
6. Yamanaka, S., Li, J., Kania, G., Elliott, S., Wersto, R.P., Van Eyk, J., Wobus, A.M., and Boheler, K.R. Pluripotency of embryonic stem cells. Cell Tissue Res 2007.
7. Fehrenbach, H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2, 33, 2001.
8. Gadue, P., Huber, T.L., Paddison, P.J., and Keller, G.M. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 103, 16806, 2006.
9. Yasunaga, M., Tada, S., Torikai-Nishikawa, S., Nakano, Y., Okada, M., Jakt, L.M., Nishikawa, S., Chiba, T., Era, T., and Nishikawa, S. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat Biotechnol 23, 1542, 2005.
10. Tada, S., Era, T., Furusawa, C., Sakurai, H., Nishikawa, S., Kinoshita, M., Nakao, K., Chiba, T., and Nishikawa, S. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132, 4363, 2005.
11. Morrison, G.M., Oikonomopoulou, I., Migueles, R.P., Soneji, S., Livigni, A., Enver, T., and Brickman, J.M. Anterior definitive endoderm from ESCs reveals a role for FGF signaling. Cell Stem Cell 3, 402, 2008.
12. Rippon, H.J., Polak, J.M., Qin, M., and Bishop, A.E. Derivation of distal lung epithelial progenitors from murine embryonic stem cells using a novel three-step differentiation protocol. Stem Cells 24, 1389, 2006.
13. Samadikuchaksaraei, A., and Bishop, A.E. Derivation and characterization of alveolar epithelial cells from murine embryonic stem cells in vitro. Methods Mol Biol 330, 233, 2006.
14. Samadikuchaksaraei, A., and Bishop, A.E. Effects of growth factors on the differentiation of murine ESC into type II pneumocytes. Cloning Stem Cells 9, 407, 2007.
15. Denham, M., Cole, T.J., and Mollard, R. Embryonic stem cells form glandular structures and express surfactant protein C following culture with dissociated fetal respiratory tissue. Am J Physiol Lung Cell Mol Physiol 290, L1210, 2006.
16. Wang, D., Haviland, D.L., Burns, A.R., Zsigmond, E., and Wetsel, R.A. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 104, 4449, 2007.
17. Van Vranken, B.E., Romanska, H.M., Polak, J.M., Rippon, H.J., Shannon, J.M., and Bishop, A.E. Coculture of embryonic stem cells with pulmonary mesenchyme: a microenvi-ronment that promotes differentiation of pulmonary epithelium. Tissue Eng 11, 1177, 2005.
18. Ali, N.N., Edgar, A.J., Samadikuchaksaraei, A., Timson, C.M., Romanska, H.M., Polak, J.M., and Bishop, A.E. Derivation of type II alveolar epithelial cells from murine embryonic stem cells. Tissue Eng 8, 541, 2002.
19. Winkler, M.E., Mauritz, C., Groos, S., Kispert, A., Menke, S., Hoffmann, A., Gruh, I., Schwanke, K., Haverich, A., and Martin, U. Serum-free differentiation of murine embryonic stem cells into alveolar type II epithelial cells. Cloning Stem Cells 10, 49, 2008.
20. Baum, C. What are the consequences of the fourth case? Mol Ther 15, 1401, 2007.
21. Bottcher, R.T., and Niehrs, C. Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26, 63, 2005.
22. Dessimoz, J., Opoka, R., Kordich, J.J., Grapin-Botton, A., and Wells, J.M. FGF signaling is necessary for establishing gut tube domains along the anterior-posterior axis in vivo. Mech Dev 123, 42, 2006.
23. Jung, J., Zheng, M., Goldfarb, M., and Zaret, K.S. Initiation of mammalian liver development from endoderm by fibro-blast growth factors. Science 284, 1998, 1999.
24. Serls, A.E., Doherty, S., Parvatiyar, P., Wells, J.M., and Deutsch, G.H. Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. Development 132, 35, 2005.
25. Mondrinos, M.J., Koutzaki, S., Lelkes, P.I., and Finck, C.M. A tissue-engineered model of fetal distal lung tissue. Am J Physiol Lung Cell Mol Physiol 293, L639, 2007.
26. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402, 2001.
27. Compernolle, V., Brusselmans, K., Acker, T., Hoet, P., Tjwa, M., Beck, H., Plaisance, S., Dor, Y., Keshet, E., Lupu, F., Nemery, B., Dewerchin, M., Van Veldhoven, P., Plate, K., Moons, L., Collen, D., and Carmeliet, P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8, 702, 2002.
28. Crisanti, M.C., Koutzaki, S.H., Mondrinos, M.J., Lelkes, P.I., and Finck, C.M. Novel methods for delivery of cell-based therapies. J Surg Res 146, 3, 2008.
29. D'Amour, K.A., Agulnick, A.D., Eliazer, S., Kelly, O.G., Kroon, E., and Baetge, E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23, 1534, 2005.
30. Kubo, A., Shinozaki, K., Shannon, J.M., Kouskoff, V., Kennedy, M., Woo, S., Fehling, H.J., and Keller, G. Development of definitive endoderm from embryonic stem cells in culture. Development 131, 1651, 2004.
31. Lieber, M., Smith, B., Szakal, A., Nelson-Rees, W., and To-daro, G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 17, 62, 1976.
32. Katoh, M. Molecular cloning and characterization of human WNT3. Int J Oncol 19, 977, 2001.
33. Duncan, S.A., Manova, K., Chen, W.S., Hoodless, P., Wein-stein, D.C., Bachvarova, R.F., and Darnell, J.E., Jr. Expression of transcription factor HNF-4 in the extraembryonic endo-derm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst. Proc Natl Acad Sci USA 91, 7598, 1994.
34. Morrisey, E.E., Ip, H.S., Lu, M.M., and Parmacek, M.S. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev Biol 177, 309, 1996.
35. Hou, J., Charters, A.M., Lee, S.C., Zhao, Y., Wu, M.K., Jones, S.J., Marra, M.A., and Hoodless, P.A. A systematic screen for genes expressed in definitive endoderm by serial analysis of gene expression (SAGE). BMC Dev Biol 7, 92, 2007.
36. Ang, S.L., Wierda, A., Wong, D., Stevens, K.A., Cascio, S., Rossant, J., and Zaret, K.S. The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119, 1301, 1993.
37. Sasaki, H., and Hogan, B.L. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47, 1993.
38. Izzi, L., Silvestri, C., von Both, I., Labbe, E., Zakin, L., Wrana, J.L., and Attisano, L. Foxh1 recruits Gsc to negatively regulate Mixl1 expression during early mouse development. EMBO J 26, 3132, 2007.
39. Cardoso, W.V., and Lu, J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 133, 1611, 2006.
40. Wunderlich, S., Gruh, I., Winkler, M.E., Beier, J., Radtke, K., Schmiedl, A., Groos, S., Haverich, A., and Martin, U. Type II pneumocyte-restricted green fluorescent protein expression after lentiviral transduction of lung epithelial cells. Hum Gene Ther 19, 39, 2008.
41. Eswarakumar, V.P., Lax, I., and Schlessinger, J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16, 139, 2005.
42. Phelps, D.S., and Floros, J. Localization of pulmonary surfactant proteins using immunohistochemistry and tissue in situ hybridization. Exp Lung Res 17, 985, 1991.
43. Gardai, S.J., Xiao, Y.Q., Dickinson, M., Nick, J.A., Voelker, D.R., Greene, K.E., and Henson, P.M. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13, 2003.
44. Compernolle, V., Brusselmans, K., Acker, T., Hoet, P., Tjwa, M., Beck, H., Plaisance, S., Dor, Y., Keshet, E., Lupu, F., Nemery, B., Dewerchin, M., Van Veldhoven, P., Plate, K., Moons, L., Collen, D., and Carmeliet, P. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8, 702, 2002.
45. Qin, M., Tai, G., Collas, P., Polak, J.M., and Bishop, A.E. Cell extract-derived differentiation of embryonic stem cells. Stem Cells 23, 712, 2005.
46. Zhang, Y., Goss, A.M., Cohen, E.D., Kadzik, R., Lepore, J.J., Muthukumaraswamy, K., Yang, J., DeMayo, F.J., Whitsett, J.A., Parmacek, M.S., and Morrisey, E.E. A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nat Genet 40, 862, 2008.
47. Van Vranken, B.E., Rippon, H.J., Samadikuchaksaraei, A., Trounson, A.O., and Bishop, A.E. The differentiation of distal lung epithelium from embryonic stem cells. Curr Protoc Stem Cell Biol, 1G, July 2007.
48. Andrade, C.F., Wong, A.P., Waddell, T.K., Keshavjee, S., and Liu, M. Cell-based tissue engineering for lung regeneration. Am J Physiol Lung Cell Mol Physiol 292, L510, 2007.
49. Kenzaki, K., Sakiyama, S., Kondo, K., Yoshida, M., Kawa-kami, Y., Takehisa, M., Takizawa, H., Miyoshi, T., Bando, Y., Tangoku, A., and Liu, M. Lung regeneration: implantation of fetal rat lung fragments into adult rat lung parenchyma. J Thorac Cardiovasc Surg 131, 1148, 2006.
50. Carraro, G., Perin, L., Sedrakyan, S., Giuliani, S., Tiozzo, C., Lee, J., Turcatel, G., De Langhe, S.P., Driscoll, B., Bellusci, S., Minoo, P., Atala, A., De Filippo, R.E., and Warburton, D. Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells 26, 2902, 2008.
51. Cortiella, J., Nichols, J.E., Kojima, K., Bonassar, L.J., Dargon, P., Roy, A.K., Vacant, M.P., Niles, J.A., and Vacanti, C.A. Tissue-engineered lung: an in vivo and in vitro comparison of polyglycolic acid and pluronic F-127 hydrogel/somatic lung progenitor cell constructs to support tissue growth. Tissue Eng 12, 1213, 2006.
52. Cecilia, C.M., Koutzaki, S.H., Mondrinos, M.J., Lelkes, P.I., and Finck, C.M. Novel methods for delivery of cell-based therapies. J Surg Res 146, 3, 2007.
53. Kuang, P.P., Lucey, E., Rishikof, D.C., Humphries, D.E., Bronsnick, D., and Goldstein, R.H. Engraftment of neonatal lung fibroblasts into the normal and elastase-injured lung. Am J Respir Cell Mol Biol 33, 371, 2005.
54. Serrano-Mollar, A., Nacher, M., Gay-Jordi, G., Closa, D., Xaubet, A., and Bulbena, O. Intratracheal transplantation of alveolar type II cells reverses bleomycin-induced lung fi-brosis. Am J Respir Crit Care Med 176, 1261, 2007.
55. Bruder, D., Westendorf, A.M., Geffers, R., Gruber, A.D., Gereke, M., Enelow, R.I., and Buer, J. CD4 T Lymphocyte-mediated lung disease: steady state between pathological and tolerogenic immune reactions. Am J Respir Crit Care Med 170, 1145, 2004