Heterogeneous mixed-lineage differentiation of mouse embryonic stem cells induced by conditioned media from A549 cells

Stem Cells and Development

Volumn 23, Issue 16, 2014, Pages 1923-1936

  Lecht, Shimon ^a   Gerstenhaber, Jonathan A ^a   Stabler, Collin T ^a   Pimton, Pimchanok ^b   Karamil, Seda ^a   Marcinkiewicz, Cezary ^a   Schulman, Edward S ^c   Lelkes, Peter I ^a  

^a Temple University   (United States)

^b WALAILAK UNIVERSITY   (Thailand)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; CLUSTERIN; DICKKOPF 1 PROTEIN; LAMIN A; LAMIN C; LAMININ ALPHA5; MEMBRANE PROTEIN; PROSAPOSIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CULTURE MEDIUM; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CELL LINEAGE; CONDITIONED MEDIA; CONTROLLED STUDY; EMBRYOID BODY; EMBRYONIC STEM CELL; ENRICHMENT CULTURE; GENE ONTOLOGY; GENOTYPE PHENOTYPE CORRELATION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TRANSFORMED CELL LINE; ANIMAL; CULTURE MEDIUM; GENE REGULATORY NETWORK; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; CULTURE MEDIA, CONDITIONED; EMBRYONIC STEM CELLS; GENE ONTOLOGY; GENE REGULATORY NETWORKS; HUMANS; MICE; TRANSCRIPTOME;

EID: 84905651728     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0042     Document Type: Article

References (71)

1. Weiss DJ, I Bertoncello, Z Borok, C Kim, A Panoskaltsis-Mortari, S Reynolds, M Rojas, B Stripp, D Warburton and DJ Prockop. (2011). Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 8:223-272.
2. Varanou A, CP Page and SL Minger. (2008). Human embryonic stem cells and lung regeneration. Br J Pharmacol 155:316-325.
3. Miller PH, DJ Knapp and CJ Eaves. (2013). Heterogeneity in hematopoietic stem cell populations: implications for transplantation. Curr Opin Hematol 20:257-264.
4. Chetty S, FW Pagliuca, C Honore, A Kweudjeu, A Rezania and DA Melton. (2013). A simple tool to improve pluripotent stem cell differentiation. Nat Methods 10:553-556.
5. Watt FM and WT Huck. (2013). Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 14:467-473.
6. Hawkins KE, TV Sharp and TR McKay. (2013). The role of hypoxia in stem cell potency and differentiation. Regen Med 8:771-782.
7. Zoldan J, ED Karagiannis, CY Lee, DG Anderson, R Langer and S Levenberg. (2011). The influence of scaffold elasticity on germ layer specification of human embryonic stem cells. Biomaterials 32:9612-9621.
8. Hannoun Z, J Fletcher, S Greenhough, C Medine, K Samuel, R Sharma, A Pryde, JR Black, JA Ross, et al. (2010). The comparison between conditioned media and serum-free media in human embryonic stem cell culture and differentiation. Cell Reprogram 12:133-140.
9. Mannello F and GA Tonti. (2007). Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25:1603-1609.
10. Arien-Zakay H, S Lecht, MM Bercu, N Amariglio, G Rechavi, H Galski, P Lazarovici and A Nagler. (2009). Interferon-gamma-induced neuronal differentiation of human umbilical cord blood-derived progenitors. Leukemia 23:1790-1800.
11. Kang Y, JM Nagy, JM Polak and A Mantalaris. (2009). Proteomic characterization of the conditioned media produced by the visceral endoderm-like cell lines HepG2 and END2: toward a defined medium for the osteogenic/ chondrogenic differentiation of embryonic stem cells. Stem Cells Dev 18:77-91.
12. Lu M, MD Kardel, MD O'Connor and CJ Eaves. (2009). Enhanced generation of hematopoietic cells from human hepatocarcinoma cell-stimulated human embryonic and induced pluripotent stem cells. Exp Hematol 37:924-936.
13. 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.
14. Mustafa SA, JD Hoheisel and MS Alhamdani. (2011). Secretome profiling with antibody microarrays. Mol Biosyst 7:1795-1801.
15. Dowling P and M Clynes. (2011). Conditioned media from cell lines: a complementary model to clinical specimens for the discovery of disease-specific biomarkers. Proteomics 11:794-804.
16. Rippon HJ, S Lane, M Qin, NS Ismail, MR Wilson, M Takata and AE Bishop. (2008). Embryonic stem cells as a source of pulmonary epithelium in vitro and in vivo. Proc Am Thorac Soc 5:717-722.
17. Siti-Ismail N, AE Bishop, JM Polak and A Mantalaris. (2008). The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance. Biomaterials 29:3946-3952.
18. Siti-Ismail N, A Samadikuchaksaraei, AE Bishop, JM Polak and A Mantalaris. (2012). 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.
19. 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.
20. Lecht S, H Arien-Zakay, M Kohan, PI Lelkes and P Lazarovici. (2010). Angiostatic effects of K252a, a Trk inhibitor, in murine brain capillary endothelial cells. Mol Cell Biochem 339:201-213.
21. Barnea E, R Sorkin, T Ziv, I Beer and A Admon. (2005). Evaluation of prefractionation methods as a preparatory step for multidimensional based chromatography of serum proteins. Proteomics 5:3367-3375.
22. UniProt Consortium. (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40:D71-D75.
23. Luo X, Y Liu, R Wang, H Hu, R Zeng and H Chen. (2011). A high-quality secretome of A549 cells aided the discovery of C4b-binding protein as a novel serum biomarker for nonsmall cell lung cancer. J Proteomics 74:528-538.
24. Caccia D, L Zanetti Domingues, F Micciche, M De Bortoli, C Carniti, P Mondellini and I Bongarzone. (2011). Secretome compartment is a valuable source of biomarkers for cancer-relevant pathways. J Proteome Res 10:4196-4207.
25. Bidez PR, JY Kresh, Y Wel and PI Lelkes. (2011). Enhanced cardiac differentiation of mouse embryonic stem cells by electrical stimulation. In: Stem Cell Engineering. Artmann GM, S Minger, and J Hescheler, eds. Springer, Berlin, pp 119-141.
26. Narayan K, KE Sylvia, N Malhotra, CC Yin, G Martens, T Vallerskog, H Kornfeld, N Xiong, NR Cohen, et al. (2012). Intrathymic programming of effector fates in three molecularly distinct gammadelta T cell subtypes. Nat Immunol 13:511-518.
27. Paquette J and T Tokuyasu. (2010). EGAN: exploratory gene association networks. Bioinformatics 26:285-286.
28. Kestler HA, A Muller, JM Kraus, M Buchholz, TM Gress, H Liu, DW Kane, BR Zeeberg and JN Weinstein. (2008). VennMaster: area-proportional Euler diagrams for functional GO analysis of microarrays. BMC Bioinformatics 9:67.
29. Jackson M, AH Taylor, EA Jones and LM Forrester. (2010). The culture of mouse embryonic stem cells and formation of embryoid bodies. Methods Mol Biol 633:1-18.
30. Pal R, S Totey, MK Mamidi and VS Bhat. (2009). Propensity of human embryonic stem cell lines during early stage of lineage specification controls their terminal differentiation into mature cell types. Exp Biol Med (Maywood) 234:1230-1243.
31. Osafune K, L Caron, M Borowiak, RJ Martinez, CS Fitz-Gerald, Y Sato, CA Cowan, KR Chien and DA Melton. (2008). Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26:313-315.
32. Pal R, MK Mamidi, AK Das, PK Gupta and R Bhonde. (2012). A simple and economical route to generate functional hepatocyte-like cells from hESCs and their application in evaluating alcohol induced liver damage. J Cell Biochem 113:19-30.
33. Hwang YS, WL Randle, RC Bielby, JM Polak and A Mantalaris. (2006). Enhanced derivation of osteogenic cells from murine embryonic stem cells after treatment with HepG2-conditioned medium and modulation of the embryoid body formation period: application to skeletal tissue engineering. Tissue Eng 12:1381-1392.
34. Kadzik RS and EE Morrisey. (2012). Directing lung endoderm differentiation in pluripotent stem cells. Cell Stem Cell 10:355-361.
35. Ali NN, AJ Edgar, A Samadikuchaksaraei, CM Timson, HM Romanska, JM Polak and AE Bishop. (2002). Derivation of type II alveolar epithelial cells from murine embryonic stem cells. Tissue Eng 8:541-550.
36. Cardoso WV. (2004). Lung morphogenesis, role of growth factors and transcription factors. In: The Lung: Development, Aging and the Environment. Harding R, KE Pinkerton, CG Plopper, eds. Elsevier Ltd., Oxford, UK, pp 3-12.
37. 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.
38. Huang SX, MN Islam, J O'Neill, Z Hu, YG Yang, YW Chen, M Mumau, MD Green, G Vunjak-Novakovic, J Bhattacharya and HW Snoeck. (2014). Efficient generation of lung and airway epithelial cells from human pluripotent stem cells. Nat Biotechnol 32:84-91.
39. Ulloa-Montoya F, BL Kidder, KA Pauwelyn, LG Chase, A Luttun, A Crabbe, M Geraerts, AA Sharov, Y Piao, et al. (2007). Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity. Genome Biol 8:R163.
40. Prakash YS and KR Stenmark. (2012). Bioengineering the lung: molecules, materials, matrix, morphology, and mechanics. Am J Physiol Lung Cell Mol Physiol 302:L361-L362.
41. Tu ML, HQ Wang, LJ Chen, JC Lu, F Jiang, JH Liang, G Xu da and DS Li. (2009). Involvement of Akt1/protein kinase Balpha in tumor conditioned medium-induced endothelial cell migration and survival in vitro. J Cancer Res Clin Oncol 135:1543-1550.
42. Nguyen NM, JH Miner, RA Pierce and RM Senior. (2002). Laminin alpha 5 is required for lobar septation and visceral pleural basement membrane formation in the developing mouse lung. Dev Biol 246:231-244.
43. Kadoya Y, M Mochizuki, M Nomizu, L Sorokin and S Yamashina. (2003). Role for laminin-alpha5 chain LG4 module in epithelial branching morphogenesis. Dev Biol 263:153-164.
44. Nguyen NM and RM Senior. (2006). Laminin isoforms and lung development: all isoforms are not equal. Dev Biol 294:271-279.
45. Colland F, X Jacq, V Trouplin, C Mougin, C Groizeleau, A Hamburger, A Meil, J Wojcik, P Legrain and JM Gauthier. (2004). Functional proteomics mapping of a human signaling pathway. Genome Res 14:1324-1332.
46. Leonova T, X Qi, A Bencosme, E Ponce, Y Sun and GA Grabowski. (1996). Proteolytic processing patterns of prosaposin in insect and mammalian cells. J Biol Chem 271:17312-17320.
47. Wang X, J Venable, P LaPointe, DM Hutt, AV Koulov, J Coppinger, C Gurkan, W Kellner, J Matteson, et al. (2006). Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127:803-815.
48. Lee YS, PW Chen, PJ Tsai, SH Su and PC Liao. (2006). Proteomics analysis revealed changes in rat bronchoalveolar lavage fluid proteins associated with oil mist exposure. Proteomics 6:2236-2250.
49. Choi J, SY Park, F Costantini, EH Jho and CK Joo. (2004). Adenomatous polyposis coli is down-regulated by the ubiquitin-proteasome pathway in a process facilitated by Axin. J Biol Chem 279:49188-49198.
50. Ho CY, DE Jaalouk, MK Vartiainen and J Lammerding. (2013). Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497:507-511.
51. Chamorro MN, DR Schwartz, A Vonica, AH Brivanlou, KR Cho and HE Varmus. (2005). FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. EMBO J 24:73-84.
52. Shu W, S Guttentag, Z Wang, T Andl, P Ballard, MM Lu, S Piccolo, W Birchmeier, JA Whitsett, SE Millar and EE Morrisey. (2005). Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximaldistal patterning in the lung. Dev Biol 283:226-239.
53. De Langhe SP, FG Sala, PM Del Moral, TJ Fairbanks, KM Yamada, D Warburton, RC Burns and S Bellusci. (2005). Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev Biol 277:316-331.
54. Chen F, Y Cao, J Qian, F Shao, K Niederreither and WV Cardoso. (2010). A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J Clin Invest 120:2040-2048.
55. Watanabe K, D Kamiya, A Nishiyama, T Katayama, S Nozaki, H Kawasaki, Y Watanabe, K Mizuseki and Y Sasai. (2005). Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288-296.
56. Kong XB and C Zhang. (2009). Dickkopf (Dkk) 1 promotes the differentiation of mouse embryonic stem cells toward neuroectoderm. In Vitro Cell Dev Biol Anim 45:185-193.
57. Verani R, I Cappuccio, P Spinsanti, R Gradini, A Caruso, MC Magnotti, M Motolese, F Nicoletti and D Melchiorri. (2007). Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid. J Neurochem 100:242-250.
58. Rai M, JM Walthall, J Hu and AK Hatzopoulos. (2012). Continuous antagonism by Dkk1 counter activates canonical Wnt signaling and promotes cardiomyocyte differentiation of embryonic stem cells. Stem Cells Dev 21:54-66.
59. Reddy KB, MC Karode, AK Harmony and PH Howe. (1996). Interaction of transforming growth factor beta receptors with apolipoprotein J/clusterin. Biochemistry 35:309-314.
60. French LE, A Chonn, D Ducrest, B Baumann, D Belin, A Wohlwend, JZ Kiss, AP Sappino, J Tschopp and JA Schifferli. (1993). Murine clusterin: molecular cloning and mRNA localization of a gene associated with epithelial differentiation processes during embryogenesis. J Cell Biol 122:1119-1130.
61. Higashino A and T Kageyama. (2008). Developmentdependent expression of calreticulin in the brain and other tissues of the Japanese monkey, Macaca fuscata. J Med Primatol 37:303-310.
62. Faustino RS, A Chiriac, NJ Niederlander, TJ Nelson, A Behfar, PK Mishra, S Macura, M Michalak, A Terzic and C Perez-Terzic. (2010). Decoded calreticulin-deficient embryonic stem cell transcriptome resolves latent cardiophenotype. Stem Cells 28:1281-1291.
63. Perrone L, G Tell and R Di Lauro. (1999). Calreticulin enhances the transcriptional activity of thyroid transcription factor-1 by binding to its homeodomain. J Biol Chem 274:4640-4645.
64. Moodley Y, P Thompson and D Warburton. (2013). Stem cells: a recapitulation of development. Respirology 18: 1167-1176.
65. 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.
66. Chen CY, LM Chi, HC Chi, MM Tsai, CY Tsai, YH Tseng, YH Lin, WJ Chen, YH Huang and KH Lin. (2012). Stable isotope labeling with amino acids in cell culture (SILAC)- based quantitative proteomics study of a thyroid hormoneregulated secretome in human hepatoma cells. Mol Cell Proteomics 11:M111011270.
67. Slany A, VJ Haudek, H Zwickl, NC Gundacker, M Grusch, TS Weiss, K Seir, C Rodgarkia-Dara, C Hellerbrand and C Gerner. (2010). Cell characterization by proteome profiling applied to primary hepatocytes and hepatocyte cell lines Hep-G2 and Hep-3B. J Proteome Res 9:6-21.
68. Makawita S, C Smith, I Batruch, Y Zheng, F Ruckert, R Grutzmann, C Pilarsky, S Gallinger and EP Diamandis. (2011). Integrated proteomic profiling of cell line conditioned media and pancreatic juice for the identification of pancreatic cancer biomarkers. Mol Cell Proteomics 10:M111 008599.
69. Ogawa T, K Takayama, N Takakura, S Kitano and H Ueno. (2002). Anti-tumor angiogenesis therapy using soluble receptors: enhanced inhibition of tumor growth when soluble fibroblast growth factor receptor-1 is used with soluble vascular endothelial growth factor receptor. Cancer Gene Ther 9:633-640.
70. Fox AJ, HJ Patel, PJ Barnes and MG Belvisi. (2001). Release of nerve growth factor by human pulmonary epithelial cells: role in airway inflammatory diseases. Eur J Pharmacol 424:159-162.
71. Katzir I, J Shani, K Regev, D Shabashov and P Lazarovici. (2002). A quantitative bioassay for nerve growth factor, using PC12 clones expressing different levels of trkA receptors. J Mol Neurosci 18:251-264.