Hypoxia enhances differentiation of mouse embryonic stem cells into definitive endoderm and distal lung cells

Stem Cells and Development

Volumn 24, Issue 5, 2015, Pages 663-676

  Pimton, Pimchanok ^a,b   Lecht, Shimon ^b   Stabler, Collin T ^b   Johannes, Gregg ^c   Schulman, Edward S ^c   Lelkes, Peter I ^b  

^a WALAILAK UNIVERSITY   (Thailand)

^b Temple University   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ACTIVIN A; AQUAPORIN 5; CHEMOKINE RECEPTOR CXCR4; HEPATOCYTE NUCLEAR FACTOR 3BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; REACTIVE OXYGEN METABOLITE; SURFACTANT PROTEIN C; TRANSCRIPTION FACTOR SOX17; HIF1A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOPROCESS; CELL DIFFERENTIATION; CELL ENGINEERING; CELL THERAPY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; EPITHELIUM CELL; GENE EXPRESSION; HYPOXIA; IN VITRO STUDY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; MARKER GENE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CELL HYPOXIA; CYTOLOGY; EMBRYOLOGY; LUNG; METABOLISM; MOUSE EMBRYONIC STEM CELL; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL HYPOXIA; CELLS, CULTURED; ENDODERM; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG; MICE; MOUSE EMBRYONIC STEM CELLS; REACTIVE OXYGEN SPECIES;

EID: 84923888289     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0343     Document Type: Article

References (72)

1. Rattue P. (2012). Lung diseases leading cause of death, most people don't know. In: Medical News Today. Hutchings J, ed. MediLexicon, Intl. www.medicalnewstoday.com/articles/247293.php
2. Gibson GJ, R Loddenkemper, Y Sibille and B Lundbäck (eds.). (2014). The European Lung White Book: Ch. 1 - The burden of lung disease. ERS, Sheffield.
3. Jungebluth P and P Macchiarini. (2011). Stem cell-based therapy and regenerative approaches to diseases of the respiratory system. Br Med Bull 99:169-187.
4. Lau AN, M Goodwin, CF Kim and DJ Weiss. (2012). Stem cells and regenerative medicine in lung biology and diseases. Mol Ther 20:1116-1130.
5. Wagner DE, RW Bonvillain, T Jensen, ED Girard, BA Bunnell, CM Finck, AM Hoffman and DJ Weiss. (2013). Can stem cells be used to generate new lungs? Ex vivo lung bioengineering with decellularized whole lung scaffolds. Respirology 18:895-911.
6. Green MD, SX Huang and HW Snoeck. (2013). Stem cells of the respiratory system: from identification to differentiation into functional epithelium. Bioessays 35:261-270.
7. Wong AP and J Rossant. (2013). Generation of lung epithelium from pluripotent stem cells. Curr Pathobiol Rep 1:137-145.
8. Lin YM, A Zhang, HJ Rippon, A Bismarck and AE Bishop. (2010). Tissue engineering of lung: the effect of extracellular matrix on the differentiation of embryonic stem cells to pneumocytes. Tissue Eng Part A 16:1515-1526.
9. Kadzik RS and EE Morrisey. (2012). Directing lung endoderm differentiation in pluripotent stem cells. Cell Stem Cell 10:355-361.
10. Longmire TA, L Ikonomou, F Hawkins, C Christodoulou, Y Cao, JC Jean, LW Kwok, H Mou, J Rajagopal, et al. (2012). Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 10:398-411.
11. Sun H, Y Quan, Q Yan, X Peng, Z Mao, RA Wetsel and D Wang. (2013). Isolation and characterization of alveolar epithelial type II cells derived from mouse embryonic stem cells. Tissue Eng Part C Methods 20:464-472.
12. Roszell B, MJ Mondrinos, A Seaton, DM Simons, SH Koutzaki, GH Fong, PI Lelkes and CM Finck. (2009). Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 15:3351-3365.
13. Lecht S, JA Gerstenhaber, CT Stabler, P Pimton, S Karamil, C Marcinkiewicz, ES Schulman and PI Lelkes. (2014). Heterogeneous mixed-lineage differentiation of mouse embryonic stem cells induced by conditioned media from A549 cells. Stem Cells Dev 23:1923-1936.
14. Kubo A, K Shinozaki, JM Shannon, V Kouskoff, M Kennedy, S Woo, HJ Fehling and G Keller. (2004). Development of definitive endoderm from embryonic stem cells in culture. Development 131:1651-1662.
15. Kim PT and CJ Ong. (2012). Differentiation of definitive endoderm from mouse embryonic stem cells. Results Probl Cell Differ 55:303-319.
16. Dunwoodie SL. (2009). The role of hypoxia in development of the Mammalian embryo. Dev Cell 17:755-773.
17. Patterson AJ and L Zhang. (2010). Hypoxia and fetal heart development. Curr Mol Med 10:653-666.
18. Heinis M, MT Simon, K Ilc, NM Mazure, J Pouyssegur, R Scharfmann and B Duvillie. (2010). Oxygen tension regulates pancreatic beta-cell differentiation through hypoxia-inducible factor 1alpha. Diabetes 59:662-669.
19. Provot S, D Zinyk, Y Gunes, R Kathri, Q Le, HM Kronenberg, RS Johnson, MT Longaker, AJ Giaccia and E Schipani. (2007). Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 177:451-464.
20. van Tuyl M, J Liu, J Wang, M Kuliszewski, D Tibboel and M Post. (2005). Role of oxygen and vascular development in epithelial branching morphogenesis of the developing mouse lung. Am J Physiol Lung Cell Mol Physiol 288:L167-L178.
21. Greer SN, JL Metcalf, Y Wang and M Ohh. (2012). The updated biology of hypoxia-inducible factor. EMBO J 31:2448-2460.
22. Ufer C and CC Wang. (2011). The roles of glutathione peroxidases during embryo development. Front Mol Neurosci 4:12.
23. Hawkins KE, TV Sharp and TR McKay. (2013). The role of hypoxia in stem cell potency and differentiation. Regen Med 8:771-782.
24. Kim TS, S Misumi, CG Jung, T Masuda, Y Isobe, F Furuyama, H Nishino and H Hida. (2008). Increase in dopaminergic neurons from mouse embryonic stem cell-derived neural progenitor/stem cells is mediated by hypoxia inducible factor-1alpha. J Neurosci Res 86:2353-2362.
25. Mondragon-Teran P, GJ Lye and FS Veraitch. (2009). Lowering oxygen tension enhances the differentiation of mouse embryonic stem cells into neuronal cells. Biotechnol Prog 25:1480-1488.
26. Niebruegge S, CL Bauwens, R Peerani, N Thavandiran, S Masse, E Sevaptisidis, K Nanthakumar, K Woodhouse, M Husain, E Kumacheva and PW Zandstra. (2009). Generation of human embryonic stem cell-derived mesoderm and cardiac cells using size-specified aggregates in an oxygencontrolled bioreactor. Biotechnol Bioeng 102:493-507.
27. Purpura KA, SH George, SM Dang, K Choi, A Nagy and PW Zandstra. (2008). Soluble Flt-1 regulates Flk-1 activation to control hematopoietic and endothelial development in an oxygen-responsive manner. Stem Cells 26:2832-2842.
28. Koay EJ and KA Athanasiou. (2008). Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. Osteoarthritis Cartilage 16:1450-1456.
29. Garita-Hernandez M, F Diaz-Corrales, D Lukovic, I Gonzalez-Guede, A Diez-Lloret, ML Valdes-Sanchez, S Massalini, S Erceg and SS Bhattacharya. (2013). Hypoxia increases the yield of photoreceptors differentiating from mouse embryonic stem cells and improves the modeling of retinogenesis in vitro. Stem Cells 31:966-978.
30. Jarecki J, E Johnson and MA Krasnow. (1999). Oxygen regulation of airway branching in Drosophila is mediated by branchless FGF. Cell 99:211-220.
31. Morrisey EE and BL Hogan. (2010). Preparing for the first breath: genetic and cellular mechanisms in lung development. Dev Cell 18:8-23.
32. Tam PP and RR Behringer. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech Dev 68:3-25.
33. Gebb SA and PL Jones. (2003). Hypoxia and lung branching morphogenesis. Adv Exp Med Biol 543:117-125.
34. Lim HJ, J Han, DH Woo, SE Kim, SK Kim, HG Kang and JH Kim. (2011). Biochemical and morphological effects of hypoxic environment on human embryonic stem cells in long-term culture and differentiating embryoid bodies. Mol Cells 31:123-132.
35. Katsuda T, T Teratani, MM Chowdhury, T Ochiya and Y Sakai. (2013). Hypoxia efficiently induces differentiation of mouse embryonic stem cells into endodermal and hepatic progenitor cells. Biochem Eng J 74:95-101.
36. Gadue P, V Gouon-Evans, X Cheng, E Wandzioch, KS Zaret, M Grompe, PR Streeter and GM Keller. (2009). Generation of monoclonal antibodies specific for cell surface molecules expressed on early mouse endoderm. Stem Cells 27:2103-2113.
37. Bidez PRI, YJ Kresh, Y Wei and PI Lelkes. (2011). Enhanced cardiac differentiation of mouse embryonic stem cells by electrical stimulation. In: Stem Cell Engineering. Artmann G, J Hecheler, S Minger, eds. Springer, Heidelberg, pp 119-142.
38. Carmeliet P, Y Dor, JM Herbert, D Fukumura, K Brusselmans, M Dewerchin, M Neeman, F Bono, R Abramovitch, et al. (1998). Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485-490.
39. Pimton P, S Sarkar, N Sheth, A Perets, C Marcinkiewicz, P Lazarovici and PI Lelkes. (2011). Fibronectin-mediated upregulation of alpha5beta1 integrin and cell adhesion during differentiation of mouse embryonic stem cells. Cell Adh Migr 5:73-82.
40. Lee SW, HK Jeong, JY Lee, J Yang, EJ Lee, SY Kim, SW Youn, J Lee, WJ Kim, et al. (2012). Hypoxic priming of mESCs accelerates vascular-lineage differentiation through HIF1-mediated inverse regulation of Oct4 and VEGF. EMBO Mol Med 4:924-938.
41. Hu CJ, S Iyer, A Sataur, KL Covello, LA Chodosh and MC Simon. (2006). Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Mol Cell Biol 26:3514-3526.
42. Chang DJ, SH Oh, N Lee, C Choi, I Jeon, HS Kim, DA Shin, SE Lee, D Kim and J Song. (2013). Contralaterally transplanted human embryonic stem cell-derived neural precursor cells (ENStem-A) migrate and improve brain functions in stroke-damaged rats. Exp Mol Med 45:e53.
43. Giaccia AJ, MC Simon and R Johnson. (2004). The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev 18:2183-2194.
44. Wang K, T Zhang, Q Dong, EC Nice, C Huang and Y Wei. (2013). Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis 4:e537.
45. Jones R and LM Reid. (2004). Development of the pulmonary vasculature. In: The Lung: Development, Aging and the Environment. Harding R, KE Pinkerton, and CG Plopper, eds. Elsevier Ltd, Oxford, United Kingdom, pp 81-104.
46. Fischer B and BD Bavister. (1993). Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99:673-679.
47. Gassmann M, J Fandrey, S Bichet, M Wartenberg, HH Marti, C Bauer, RH Wenger and H Acker. (1996). Oxygen supply and oxygen-dependent gene expression in differentiating embryonic stem cells. Proc Natl Acad Sci U S A 93:2867-2872.
48. Jauniaux E, AL Watson, J Hempstock, YP Bao, JN Skepper and GJ Burton. (2000). Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 157:2111-2122.
49. Kocabas F, AI Mahmoud, D Sosic, ER Porrello, R Chen, JA Garcia, RJ DeBerardinis and HA Sadek. (2012). The hypoxic epicardial and subepicardial microenvironment. J Cardiovasc Transl Res 5:654-665.
50. Oliver JA, O Maarouf, FH Cheema, TP Martens and Q Al-Awqati. (2004). The renal papilla is a niche for adult kidney stem cells. J Clin Invest 114:795-804.
51. Parmar K, P Mauch, JA Vergilio, R Sackstein and JD Down. (2007). Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 104:5431-5436.
52. Fynes K, R Tostoes, L Ruban, B Weil, C Mason and FS Veraitch. (2014). The Differential effects of 2% oxygen preconditioning on the subsequent differentiation of mouse and human pluripotent stem cells. Stem Cells Dev 23: 1910-1922.
53. 2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102:4783-4788.
54. Forristal CE, DR Christensen, FE Chinnery, R Petruzzelli, KL Parry, T Sanchez-Elsner and FD Houghton. (2013). Environmental oxygen tension regulates the energy metabolism and self-renewal of human embryonic stem cells. PLoS One 8:e62507.
55. Bae D, P Mondragon-Teran, D Hernandez, L Ruban, C Mason, SS Bhattacharya and FS Veraitch. (2012). Hypoxia enhances the generation of retinal progenitor cells from human induced pluripotent and embryonic stem cells. Stem Cells Dev 21:1344-1355.
56. Si-Tayeb K, FK Noto, M Nagaoka, J Li, MA Battle, C Duris, PE North, S Dalton and SA Duncan. (2010). Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51:297-305.
57. Hakim F, T Kaitsuka, JM Raeed, FY Wei, N Shiraki, T Akagi, T Yokota, S Kume and K Tomizawa. (2014). High oxygen condition facilitates the differentiation of mouse and human pluripotent stem cells into pancreatic progenitors and insulin-producing cells. J Biol Chem 289:9623-9638.
58. Giordano FJ. (2005). Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115:500-508.
59. Gu YZ, SM Moran, JB Hogenesch, L Wartman and CA Bradfield. (1998). Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3alpha. Gene Expr 7:205-213.
60. Forristal CE, KL Wright, NA Hanley, RO Oreffo and FD Houghton. (2010). Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139:85-97.
61. Hinck AP. (2012). Structural studies of the TGF-betas and their receptors - insights into evolution of the TGF-beta superfamily. FEBS Lett 586:1860-1870.
62. Jain M, S Rivera, EA Monclus, L Synenki, A Zirk, J Eisenbart, C Feghali-Bostwick, GM Mutlu, GR Budinger and NS Chandel. (2013). Mitochondrial reactive oxygen species regulate transforming growth factor-beta signaling. J Biol Chem 288:770-777.
63. Ji AR, SY Ku, MS Cho, YY Kim, YJ Kim, SK Oh, SH Kim, SY Moon and YM Choi. (2010). Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp Mol Med 42:175-186.
64. Wen JW, JT Hwang and GM Kelly. (2012). Reactive oxygen species and Wnt signalling crosstalk patterns mouse extraembryonic endoderm. Cell Signal 24:2337-2348.
65. Sandieson L, JT Hwang and GM Kelly. (2014). Redox regulation of canonical Wnt signaling affects extraembryonic endoderm formation. Stem Cells Dev 23:1037-1049.
66. Shimoda LA and GL Semenza. (2011). HIF and the lung: role of hypoxia-inducible factors in pulmonary development and disease. Am J Respir Crit Care Med 183:152-156.
67. Van Haute L, G De Block, I Liebaers, K Sermon and M De Rycke. (2009). Generation of lung epithelial-like tissue from human embryonic stem cells. Respir Res 10:105.
68. Matthay MA, P Anversa, J Bhattacharya, BK Burnett, HA Chapman, JM Hare, DJ Hei, AM Hoffman, S Kourembanas, et al. (2013). Cell therapy for lung diseases. Report from an NIH-NHLBI workshop, November 13-14, 2012. Am J Respir Crit Care Med 188:370-375.
69. Lecht S, CT Stabler, AL Rylander, R Chiaverelli, ES Schulman, C Marcinkiewicz and PI Lelkes. (2014). Enhanced reseeding of decellularized rodent lungs with mouse embryonic stem cells. Biomaterials 35:3252-3262.
70. Crisanti MC, SH Koutzaki, MJ Mondrinos, PI Lelkes and CM Finck. (2008). Novel methods for delivery of cell-based therapies. J Surg Res 146:3-10.
71. Mondrinos MJ, S Koutzaki, E Jiwanmall, M Li, JP Dechadarevian, PI Lelkes and CM Finck. (2006). Engineering three-dimensional pulmonary tissue constructs. Tissue Eng 12:717-728.
72. Mondrinos MJ, PL Jones, CM Finck and PI Lelkes. (2014). Engineering de novo assembly of fetal pulmonary organoids. Tissue Eng Part A. [Epub ahead of print]; DOI: 10.1089/ten.tea.2014.0085.