Human decidua-derived mesenchymal stem cells differentiate into functional alveolar type II-like cells that synthesize and secrete pulmonary surfactant complexes

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Cerrada, Alejandro ^a   De La Torre, Paz ^b   Grande, Jesús ^c   Haller, Thomas ^d   Flores, Ana I ^b   Pérez Gil, Jesús ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b Universidad Complutense   (Spain)

^c HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

LUNG SURFACTANT; PHOSPHOLIPID;

ADSORPTION KINETICS; ARTICLE; BIOACCUMULATION; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL ORGANELLE; CELL STRUCTURE; CONTROLLED STUDY; DECIDUA; EMBRYO; EXOCYTOSIS; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LAMELLAR BODY; LIPID TRANSPORT; LIPOGENESIS; LUNG ALVEOLUS CELL TYPE 2; MESENCHYMAL STEM CELL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LUNG ALVEOLUS CELL; MESENCHYMAL STROMA CELL; METABOLISM; TIME; ULTRASTRUCTURE;

CELL DIFFERENTIATION; DECIDUA; EXOCYTOSIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STROMAL CELLS; PHOSPHOLIPIDS; PNEUMOCYTES; PULMONARY SURFACTANTS; TIME FACTORS;

EID: 84908099221     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110195     Document Type: Article

References (69)

1. Dobbs LG (1989) Pulmonary surfactant. Annu Rev Med 40: 431-446.
2. Gonzalez RF, Dobbs LG (2013) Isolation and culture of alveolar epithelial Type I and Type II cells from rat lungs. Methods Mol Biol 945: 145-159.
3. Fehrenbach H (2012) Alveolar epithelial type II cells from embryonic stem cells: knights in shining armour? Eur Respir J 39: 240-241.
4. Mason RJ (2006) Biology of alveolar type II cells. Respirology 11 Suppl: S12-15.
5. Fehrenbach H (2001) Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2: 33-46.
6. Perez-Gil J (2008) Structure of pulmonary surfactant membranes and films: the role of proteins and lipid-protein interactions. Biochim Biophys Acta 1778: 1676-1695.
7. Serrano AG, Perez-Gil J (2006) Protein-lipid interactions and surface activity in the pulmonary surfactant system. Chem Phys Lipids 141: 105-118.
8. Wright JR (2005) Immunoregulatory functions of surfactant proteins. Nat Rev Immunol 5: 58-68.
9. Hallman M, Glumoff V, Ramet M (2001) Surfactant in respiratory distress syndrome and lung injury. Comp Biochem Physiol A Mol Integr Physiol 129: 287-294.
10. Jennings P, Bertocchi C, Frick M, Haller T, Pfaller W, et al. (2005) Ca2+ induced surfactant secretion in alveolar type II cultures isolated from the H- 2Kb-tsA58 transgenic mouse. Cell Physiol Biochem 15: 159-166.
11. Dobbs LG, Williams MC, Brandt AE (1985) Changes in biochemical characteristics and pattern of lectin binding of alveolar type II cells with time in culture. Biochim Biophys Acta 846: 155-166.
12. Mason RJ, Lewis MC, Edeen KE, McCormick-Shannon K, Nielsen LD, et al. (2002) Maintenance of surfactant protein A and D secretion by rat alveolar type II cells in vitro. Am J Physiol Lung Cell Mol Physiol 282: L249-258.
13. Wong AP, Rossant J (2013) Generation of Lung Epithelium from Pluripotent Stem Cells. Curr Pathobiol Rep 1: 137-145.
14. Ali NN, Edgar AJ, Samadikuchaksaraei A, Timson CM, Romanska HM, et al. (2002) Derivation of type II alveolar epithelial cells from murine embryonic stem cells. Tissue Eng 8: 541-550.
15. Rippon HJ, Polak JM, Qin M, Bishop AE (2006) Derivation of distal lung epithelial progenitors from murine embryonic stem cells using a novel three-step differentiation protocol. Stem Cells 24: 1389-1398.
16. Roszell B, Mondrinos MJ, Seaton A, Simons DM, Koutzaki SH, et al. (2009) Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 15: 3351-3365.
17. Samadikuchaksaraei A, Bishop AE (2006) Derivation and characterization of alveolar epithelial cells from murine embryonic stem cells in vitro. Methods Mol Biol 330: 233-248.
18. Schmeckebier S, Mauritz C, Katsirntaki K, Sgodda M, Puppe V, et al. (2013) Keratinocyte growth factor and dexamethasone plus elevated cAMP levels synergistically support pluripotent stem cell differentiation into alveolar epithelial type II cells. Tissue Eng Part A 19: 938-951.
19. Siti-Ismail N, Samadikuchaksaraei A, Bishop AE, Polak JM, Mantalaris A (1089) Development of a novel three-dimensional, automatable and integrated bioprocess for the differentiation of embryonic stem cells into pulmonary alveolar cells in a rotating vessel bioreactor system. Tissue Eng Part C Methods 18: 263-272.
20. Van Vranken BE, Rippon HJ, Samadikuchaksaraei A, Trounson AO, Bishop AE (2007) The differentiation of distal lung epithelium from embryonic stem cells. Curr Protoc Stem Cell Biol Chapter 1: Unit 1G.1.
21. Winkler ME, Mauritz C, Groos S, Kispert A, Menke S, et al. (2008) Serum-free differentiation of murine embryonic stem cells into alveolar type II epithelial cells. Cloning Stem Cells 10: 49-64.
22. Samadikuchaksaraei A, Cohen S, Isaac K, Rippon HJ, Polak JM, et al. (2006) Derivation of distal airway epithelium from human embryonic stem cells. Tissue Eng 12: 867-875.
23. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel RA (2007) A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A 104: 4449-4454.
24. Knoll A, Brockmeyer T, Chevalier R, Zscheppang K, Nielsen H, et al. (2013) Adult Rat Bone Marrow-Derived Stem Cells Promote Late Fetal Type II Cell Differentiation in a Co-Culture Model. Open Respir Med J 7: 46-53.
25. Ma N, Gai H, Mei J, Ding FB, Bao CR, et al. (2011) Bone marrow mesenchymal stem cells can differentiate into type II alveolar epithelial cells in vitro. Cell Biol Int 35: 1261-1266.
26. Wang G, Bunnell BA, Painter RG, Quiniones BC, Tom S, et al. (2005) Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis. Proc Natl Acad Sci U S A 102: 186-191.
27. Carraro G, Perin L, Sedrakyan S, Giuliani S, Tiozzo C, et al. (2008) Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells 26: 2902-2911.
28. Moodley Y, Ilancheran S, Samuel C, Vaghjiani V, Atienza D, et al. (2010) Human amnion epithelial cell transplantation abrogates lung fibrosis and augments repair. Am J Respir Crit Care Med 182: 643-651.
29. Berger MJ, Adams SD, Tigges BM, Sprague SL, Wang XJ, et al. (2006) Differentiation of umbilical cord blood-derived multilineage progenitor cells into respiratory epithelial cells. Cytotherapy 8: 480-487.
30. Macias MI, Grande J, Moreno A, Dominguez I, Bornstein R, et al. (2010) Isolation and characterization of true mesenchymal stem cells derived from human term decidua capable of multilineage differentiation into all 3 embryonic layers. Am J Obstet Gynecol 203: 8.
31. Hemberger M, Yang W, Natale D, Brown TL, Dunk C, et al. (2008) Stem cells from fetal membranes - a workshop report. Placenta 29: 21.
32. Marcus AJ, Woodbury D (2008) Fetal stem cells from extra-embryonic tissues: do not discard. J Cell Mol Med 12: 730-742.
33. Bornstein R, Macias MI, de la Torre P, Grande J, Flores AI (2012) Human decidua-derived mesenchymal stromal cells differentiate into hepatic-like cells and form functional three-dimensional structures. Cytotherapy 14: 1182-1192.
34. Canals D, Mormeneo D, Fabrias G, Llebaria A, Casas J, et al. (2009) Synthesis and biological properties of Pachastrissamine (jaspine B) and diastereoisomeric jaspines. Bioorg Med Chem 17: 235-241.
35. Haller T, Dietl P, Stockner H, Frick M, Mair N, et al. (2004) Tracing surfactant transformation from cellular release to insertion into an air-liquid interface. Am J Physiol Lung Cell Mol Physiol 286: 2.
36. Rouser G, Fkeischer S, Yamamoto A (1970) Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5: 494-496.
37. Taeusch HW, Bernardino de la Serna J, Perez-Gil J, Alonso C, Zasadzinski JA (2005) Inactivation of pulmonary surfactant due to serum-inhibited adsorption and reversal by hydrophilic polymers: experimental. Biophys J 89: 1769-1779.
38. Haller T, Ortmayr J, Friedrich F, Volkl H, Dietl P (1998) Dynamics of surfactant release in alveolar type II cells. Proc Natl Acad Sci U S A 95: 1579-1584.
39. Ravasio A, Cruz A, Perez-Gil J, Haller T (2008) High-throughput evaluation of pulmonary surfactant adsorption and surface film formation. J Lipid Res 49: 2479-2488.
40. Ravasio A, Olmeda B, Bertocchi C, Haller T, Perez-Gil J (2010) Lamellar bodies form solid three-dimensional films at the respiratory air-liquid interface. J Biol Chem 285: 28174-28182.
41. Perez-Gil J, Weaver TE (2010) Pulmonary surfactant pathophysiology: current models and open questions. Physiology 25: 132-141.
42. Mendelson CR, Boggaram V (1990) Hormonal and developmental regulation of pulmonary surfactant synthesis in fetal lung. Baillieres Clin Endocrinol Metab 4: 351-378.
43. Mendelson CR, Boggaram V (1991) Hormonal control of the surfactant system in fetal lung. Annu Rev Physiol 53: 415-440.
44. Pryhuber GS, Hull WM, Fink I, McMahan MJ, Whitsett JA (1991) Ontogeny of surfactant proteins A and B in human amniotic fluid as indices of fetal lung maturity. Pediatr Res 30: 597-605.
45. Bohinski RJ, Di Lauro R, Whitsett JA (1994) The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol Cell Biol 14: 5671-5681.
46. Wan H, Xu Y, Ikegami M, Stahlman MT, Kaestner KH, et al. (2004) Foxa2 is required for transition to air breathing at birth. Proc Natl Acad Sci U S A 101: 14449-14454.
47. Kalin TV, Wang IC, Meliton L, Zhang Y, Wert SE, et al. (2008) Forkhead Box m1 transcription factor is required for perinatal lung function. Proc Natl Acad Sci U S A 105: 19330-19335.
48. Fuchs S, Hollins AJ, Laue M, Schaefer UF, Roemer K, et al. (2003) Differentiation of human alveolar epithelial cells in primary culture: morphological characterization and synthesis of caveolin-1 and surfactant protein-C. Cell Tissue Res 311: 31-45.
49. Steimer A, Laue M, Franke H, Haltner-Ukomado E, Lehr CM (2006) Porcine alveolar epithelial cells in primary culture: morphological, bioelectrical and immunocytochemical characterization. Pharm Res 23: 2078-2093.
50. Stahlman MT, Besnard V, Wert SE, Weaver TE, Dingle S, et al. (2007) Expression of ABCA3 in developing lung and other tissues. J Histochem Cytochem 55: 71-83.
51. Stahlman MT, Gray ME, Whitsett JA (1992) The ontogeny and distribution of surfactant protein B in human fetuses and newborns. J Histochem Cytochem 40: 1471-1480.
52. Zhou L, Lim L, Costa RH, Whitsett JA (1996) Thyroid transcription factor-1, hepatocyte nuclear factor-3beta, surfactant protein B, C, and Clara cell secretory protein in developing mouse lung. J Histochem Cytochem 44: 1183-1193.
53. Miyamura K, Malhotra R, Hoppe HJ, Reid KB, Phizackerley PJ, et al. (1994) Surfactant proteins A (SP-A) and D (SP-D): levels in human amniotic fluid and localization in the fetal membranes. Biochim Biophys Acta 20: 303-307.
54. Sun K, Brockman D, Campos B, Pitzer B, Myatt L (2006) Induction of surfactant protein A expression by cortisol facilitates prostaglandin synthesis in human chorionic trophoblasts. J Clin Endocrinol Metab 91: 4988-4994.
55. Newman GE, Phizackerley PJ, Lopez Bernal A, Noble GR, Willis AC (1991) Adsorption of fetal surfactant protein SP-B on the human amnion at term and on amniocytes incubated with fetal surfactant in vitro. Reprod Fertil Dev 3: 421-430.
56. Sati L, Seval-Celik Y, Demir R (2007) Lung surfactant proteins in the early human placenta. Histochem Cell Biol 133: 85-93.
57. Frick M, Bertocchi C, Jennings P, Haller T, Mair N, et al. (2004) Ca2+ entry is essential for cell strain-induced lamellar body fusion in isolated rat type II pneumocytes. Am J Physiol Lung Cell Mol Physiol 286: 22.
58. Frick M, Eschertzhuber S, Haller T, Mair N, Dietl P (2001) Secretion in alveolar type II cells at the interface of constitutive and regulated exocytosis. Am J Respir Cell Mol Biol 25: 306-315.
59. Miklavc P, Mair N, Wittekindt OH, Haller T, Dietl P, et al. (1073) Fusionactivated Ca2+ entry via vesicular P2X4 receptors promotes fusion pore opening and exocytotic content release in pneumocytes. Proc Natl Acad Sci U S A 108: 14503-14508.
60. Okamoto K, Miyoshi S, Toyoda M, Hida N, Ikegami Y, et al. (2007) 'Working' cardiomyocytes exhibiting plateau action potentials from human placentaderived extraembryonic mesodermal cells. Exp Cell Res 313: 2550-2562.
61. Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, et al. (2006) Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 194: 664-673.
62. Soncini M, Vertua E, Gibelli L, Zorzi F, Denegri M, et al. (2007) Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 1: 296-305.
63. Cargnoni A, Gibelli L, Tosini A, Signoroni PB, Nassuato C, et al. (2009) Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 18: 405-422.
64. Duchesneau P, Wong AP, Waddell TK (1830) Optimization of targeted cell replacement therapy: a new approach for lung disease. Mol Ther 18: 1830-1836.
65. Spitalieri P, Quitadamo MC, Orlandi A, Guerra L, Giardina E, et al. (1183) Rescue of murine silica-induced lung injury and fibrosis by human embryonic stem cells. Eur Respir J 39: 446-457.
66. Wang YY, Li XZ, Wang LB (2013) Therapeutic implications of mesenchymal stem cells in acute lung injury/acute respiratory distress syndrome. Stem Cell Res Ther 4: 45.
67. Wong AP, Dutly AE, Sacher A, Lee H, Hwang DM, et al. (2007) Targeted cell replacement with bone marrow cells for airway epithelial regeneration. Am J Physiol Lung Cell Mol Physiol 293: 6.
68. Wong AP, Keating A, Lu WY, Duchesneau P, Wang X, et al. (2009) Identification of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J Clin Invest 119: 336-348.
69. Vegh I, Grau M, Gracia M, Grande J, de la Torre P, et al. (2013) Decidua mesenchymal stem cells migrated toward mammary tumors in vitro and in vivo affecting tumor growth and tumor development. Cancer Gene Ther 20: 8-16.