Ascorbic acid-induced cardiac differentiation of murine pluripotent stem cells: Transcriptional profiling and effect of a small molecule synergist of Wnt/β-catenin signaling pathway

Cellular Physiology and Biochemistry

Volumn 36, Issue 2, 2015, Pages 810-830

  Ivanyuk, Dina ^a,b   Budash, Galina ^a   Zheng, Yunjie ^a   Gaspar, John Antony ^a   Chaudhari, Umesh ^a   Fatima, Azra ^a   Bahmanpour, Soghra ^a,c   Grin, Vladislav K ^b   Popandopulo, Andrey G ^b   Sachinidis, Agapios ^a   Hescheler, Jürgen ^a   Šarić, Tomo ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b VK Gusak Institute of Urgent and Recovery Surgery   (Ukraine)

^c SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Cardiomyocytes; Differentiation; ESC; Ipsc; Pluripotent stem cells; Small molecules; Sscorbic acid; Transcriptome; Wnt pathway

Indexed keywords

ALPHA ACTININ; ASCORBIC ACID; BETA CATENIN; CARDIOGENOL C; CDH5 PROTEIN; CYCLIC AMP; CYCLOSPORIN A; DIMETHYL SULFOXIDE; DORSOMORPHIN; ELK3 PROTEIN; ENZYME INHIBITOR; MYOSIN HEAVY CHAIN ALPHA; NPPA PROTEIN; PYRIMIDINE DERIVATIVE; Q11; TEK PROTEIN; TNFAIP2 PROTEIN; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SOX18; TRANSCRIPTOME; TROPONIN T; UNCLASSIFIED DRUG; ANTIOXIDANT; PURINE DERIVATIVE; QS11 COMPOUND;

ACTION POTENTIAL; ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ERYTHROPOIESIS; FLOW CYTOMETRY; GENE ONTOLOGY; HEART MUSCLE CELL; HEMATOPOIESIS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL CULTURE; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; METABOLISM;

MURINAE;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BETA CATENIN; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION PROFILING; MICE; MYOCYTES, CARDIAC; PLURIPOTENT STEM CELLS; PURINES; WNT SIGNALING PATHWAY;

EID: 84930257417     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000430140     Document Type: Article

References (61)

1. Centers for Disease Control and Prevention: http://www.cdc.gov/nchs/fastats/leading-causes-of-death. htm.
2. Turksen K: Adult stem cells and cardiac regeneration. Stem Cell Rev2013;9:537-540.
3. Koudstaal S, Jansen Of Lorkeers SJ, Gaetani R, Gho JM, van Slochteren FJ, Sluijter JP, Doevendans PA, Ellison GM, Chamuleau SA: Concise review: Heart regeneration and the role of cardiac stem cells. Stem Cell Transl Med 2013;2:434-443.
4. Zwi-Dantsis L, Gepstein L: Induced pluripotent stem cells for cardiac repair.Cell Mol Life Sci 2012;69:3285-3299.
5. Cherry AB, Daley GQ: Reprogrammed cells for disease modeling and regenerative medicine. Annu Rev Med 2013;64:277-290.
6. Mummery CL, Zhang J, Ng ES, Elliott DA, Elefanty AG, Kamp TJ: Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: A methods overview. Circ Res 2012;111:344-358.
7. Cao N, Liu Z, Chen Z, Wang J, Chen T, Zhao X, Ma Y, Qin L, Kang J, Wei B, Wang L, Jin Y, Yang H-T: Ascorbic acid enhances the cardiac differentiation of induced pluripotent stem cells through promoting the proliferation of cardiac progenitor cells. Cell Res 2012;22:219-236.
8. ChenY, Shao JZ, Xiang LX, Guo J, Zhou QJ, Yao X, Dai LC, Lu YL: Cyclic adenosine 3',5'-monophosphate induces differentiation of mouse embryonic stem cells into cardiomyocytes. Cell Biol Int 2006;30:301-307.
9. Hao J, Daleo MA, Murphy CK, Yu PB, Ho JN, Hu J, Peterson RT, Hatzopoulos AK, Hong CC: Dorsomorphin, a selective small molecule inhibitor of bmp signaling, promotes cardiomyogenesis in embryonic stem cells. PLoSOne2008;3:e2904.
10. Naito AT, Akazawa H, Takano H, Minamino T, Nagai T, Aburatani H, Komuro I: Phosphatidylinositol 3-kinase-Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical wnt signaling. Circ Res 2005;97:144-151.
11. RenY, Lee MY, Schliffke S, Paavola J, Amos PJ, Ge X, Ye M, Zhu S, Senyei G, Lum L, Ehrlich BE, Qyang Y: Small molecule wnt inhibitors enhance the efficiency ofBMP-4-directed cardiac differentiation ofhuman pluripotent stem cells. J Mol Cell Cardiol 2011;51:280-287.
12. Tran TH, Wang X, Browne C, Zhang Y, Schinke M, Izumo S, Burcin M: Wnt3a-induced mesoderm formation and cardiomyogenesis in human embryonic stem cells. Stem Cells 2009;27:1869-1878.
13. Ueno S, Weidinger G, Osugi T, KohnAD, Golob JL, Pabon L, Reinecke H, Moon RT, Murry CE: Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc Natl Acad SciUSA 2007;104:9685-9690.
14. Willems E, Spiering S, Davidovics H, Lanier M, Xia Z, Dawson M, Cashman J, Mercola M: Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 2011;109:360-364.
15. Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, Hsiao C, Kamp TJ, Palecek SP: Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions. Nat Protoc 2013;8:162-175.
16. Zhang Q, Major MB, Takanashi S, Camp ND, Nishiya N, Peters EC, Ginsberg MH, Jian X, Randazzo PA, Schultz PG, Moon RT, Ding S: Small-molecule synergist of the Wnt/beta-catenin signaling pathway. Proc Natl Acad SciUSA 2007;104:7444-7448.
17. Kolossov E, Bostani T, Roell W, Breitbach M, Pillekamp F, Nygren JM, Sasse P, Rubenchik O, Fries JW, Wenzel D, Geisen C, Xia Y, Lu Z, Duan Y, Kettenhofen R, Jovinge S, Bloch W, Bohlen H, Welz A, Hescheler J, Jacobsen SE, Fleischmann BK: Engraftment of engineered es cell-derived cardiomyocytes but not BM cells restores contractile functionto the infarcted myocardium. J Exp Med 2006;203:2315-2327.
18. Meissner A, Wernig M, Jaenisch R: Direct reprogramming of genetically unmodified fibroblasts into pluripotentstem cells. NatBiotechnol 2007;25:1177-1181.
19. Gissel C, Voolstra C, Doss MX, Koehler CI, Winkler J, Hescheler J, Sachinidis A: An optimized embryonic stem cell model for consistent gene expression and developmental studies: A fundamental study. Thromb Haemost 2005;94:719-727.
20. Frenzel LP, Abdullah Z, Kriegeskorte AK, Dieterich R, Lange N, Busch DH, Kronke M, Utermohlen O, Hescheler J, Saric T: Role of natural-killer group 2 member d ligands and intercellular adhesion molecule 1 in natural killer cell-mediated lysis of murine embryonic stem cells and embryonic stem cell-derived cardiomyocytes. Stem Cells 2009;27:307-316.
21. Pfannkuche K, Neuss S, Pillekamp F, Frenzel LP, Attia W, Hannes T, Salber J, Hoss M, Zenke M, Fleischmann BK, Hescheler J, Saric T: Fibroblasts facilitate the engraftment of embryonic stem cell-derived cardiomyocytes on three-dimensional collagen matrices and aggregation in hanging drops. Stem Cells Dev 2010;19:1589-1599.
22. Takahashi T, Lord B, Schulze PC, Fryer RM, Sarang SS, Gullans SR, Lee RT: Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 2003;107:1912-1916.
23. Jasmin, Spray DC, Campos de Carvalho AC, Mendez-Otero R: Chemical induction of cardiac differentiation in p19 embryonal carcinoma stem cells. Stem Cells Dev 2010;19:403-412.
24. Sachinidis A, Schwengberg S, Hippler-Altenburg R, Mariappan D, Kamisetti N, Seelig B, Berkessel A, Hescheler J: Identification of small signalling molecules promoting cardiac-specific differentiation of mouse embryonic stem cells. Cell Physiol Biochem 2006;18:303-314.
25. Yan P, Nagasawa A, Uosaki H, Sugimoto A, Yamamizu K, Teranishi M, Matsuda H, Matsuoka S, Ikeda T, Komeda M, Sakata R, Yamashita JK: Cyclosporin-A potently induces highly cardiogenic progenitors from embryonic stem cells. Biochem Biophys Res Commun 2009;379:115-120.
26. Schulz H, Kolde R, Adler P, Aksoy I, Anastassiadis K, Bader M, Billon N, Boeuf H, Bourillot PY, Buchholz F, Dani C, Doss MX, Forrester L, Gitton M, Henrique D, Hescheler J, Himmelbauer H, Hubner N, Karantzali E, Kretsovali A, Lubitz S, Pradier L, Rai M, Reimand J, Rolletschek A, Sachinidis A, Savatier P, Stewart F, Storm MP, Trouillas M, Vilo J, Welham MJ, Winkler J, Wobus AM, Hatzopoulos AK: The fungenes database: A genomics resource for mouse embryonic stem cell differentiation. PLoS One 2009;4:e6804.
27. Gaspar JA DM, Winkler J, Wagh V, Hescheler J, Kolde R, Vilo J, Schulz H, Sachinidis A.: Gene expression signatures defining fundamental biological processes in pluripotent, early and late differentiated embryonic stem cells. Stem Cells Dev 2012;21:2471-2484.
28. Bolstad BM, Irizarry RA, Astrand M, Speed TP: A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003;19:185-193.
29. Johnson WE, Li C, Rabinovic A: Adjusting batch effects in microarray expression data using empirical bayes methods. Biostatistics 2007;8:118-127.
30. Dennis G, Jr., Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA: David: Database for annotation, visualization, and integrated discovery. Genome Biol 2003;4:P3.
31. Huang da W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: Tool for the unification of biology. The gene ontology consortium. Nature Genet 2000;25:25-29.
33. Kanehisa M, Goto S: Kegg: Kyoto encyclopedia of genes and genomes. Nuclei Acids Res 2000;28:27-30.
34. Fujiwara M, Yan P, Otsuji TG, Narazaki G, Uosaki H, Fukushima H, Kuwahara K, Harada M, Matsuda H, Matsuoka S, Okita K, Takahashi K, Nakagawa M, Ikeda T, Sakata R, Mummery CL, Nakatsuji N, Yamanaka S, Nakao K, Yamashita JK: Induction and enhancement of cardiac cell differentiation from mouse and human induced pluripotent stem cells with cyclosporin-A. PLoS One 2011;6:el6734.
35. Jasmin, Spray DC, Campos de Carvalho AC, Mendez-Otero R: Chemical induction of cardiac differentiation in p19 embryonal carcinoma stem cells. Stem Cells Dev 2010;19:403-412.
36. Wu X, Ding S, Ding Q, Gray NS, Schultz PG: Small molecules that induce cardiomyogenesis in embryonic stem cells. J Am Chem Soc 2004;126:1590-1591.
37. Bartsch C, Bekhite MM, Wolheim A, Richter M, Ruhe C, Wissuwa B, Marciniak A, Muller J, Heller R, Figulla HR, Sauer H, Wartenberg M: NADPH oxidase and ENOS control cardiomyogenesis in mouse embryonic stem cells on ascorbic acid treatment. Free Radic Biol Med 2011;51:432-443.
38. Sato H, Takahashi M, Ise H, Yamada A, Hirose S, Tagawa Y, Morimoto H, Izawa A, Ikeda U: Collagen synthesis is required for ascorbic acid-enhanced differentiation of mouse embryonic stem cells into cardiomyocytes. Biochem Biophys Res Commun 2006;342:107-112.
39. Kinney MA, Sargent CY, McDevitt TC: Temporal modulation of beta-catenin signaling by multicellular aggregation kinetics impacts embryonic stem cell cardiomyogenesis. Stem Cells Dev 2013;22:2665-2677.
40. Minami I, Yamada K, Otsuji TG, Yamamoto T, Shen Y, Otsuka S, Kadota S, Morone N, Barve M, Asai Y, Tenkova-Heuser T, Heuser JE, Uesugi M, Aiba K, Nakatsuji N: A small molecule that promotes cardiac differentiation ofhuman pluripotent stem cells under defined, cytokine-and xeno-free conditions. Cell Rep 2012;2:1448-1460.
41. RenY, Lee MY, Schliffke S, Paavola J, Amos PJ, Ge X, Ye M, Zhu S, Senyei G, Lum L, Ehrlich BE, Qyang Y: Small molecule wnt inhibitors enhance the efficiency ofBMP-4-directed cardiac differentiation ofhuman pluripotent stem cells. J Mol Cell Cardiol 2011;51:280-287.
42. Willems E, Spiering S, Davidovics H, Lanier M, Xia Z, Dawson M, Cashman J, Mercola M: Small-molecule inhibitors of the WNT pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 2011;109:360-364.
43. Ao A, Hao J, Hopkins CR, Hong CC: Dmhl, a novel BMP small molecule inhibitor, increases cardiomyocyte progenitors and promotes cardiac differentiation in mouse embryonic stem cells. PLoS One 2012;7:e41627.
44. Crescini E, Gualandi L, Uberti D, Prandelli C, Presta M, Dell'Era P: Ascorbic acid rescues cardiomyocyte development in FGFR1(-/-) murine embryonic stem cells. Biochim Biophys Acta 2013;1833:140-147.
45. Chen K, Bai H, Arzigian M, Gao YX, Bao J, Wu WS, Shen WF, Wu L, Wang ZZ: Endothelial cells regulate cardiomyocyte developmentfrom embryonic stem cells. J Cell Biochem 2010;111:29-39.
46. Buggisch M, Ateghang B, Ruhe C, Strobel C, Lange S, Wartenberg M, Sauer H: Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and nadph oxidase. J CellSci2007;120:885-894.
47. Chung T-L, Brena RM, Kolle G, Grimmond SM, Berman BP, Laird PW, Pera MF, Wolvetang EJ: Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. StemCells2010;28:1848.
48. Chung T-L, Turner JP, Thaker NY, Kolle G, Cooper-White JJ, Grimmond SM, Pera MF, Wolvetang EJ: Ascorbate promotes epigenetic activation of cd30 in human embryonic stem cells. Stem Cells 2010;28:1782-1793.
49. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, Li W, Weng Z, Chen J, Ni S, Chen K, Li Y, Liu X, Xu J, Zhang S, Li F, He W, Labuda K, Song Y, Peterbauer A, Wolbank S, Redl H, Zhong M, Cai D, Zeng L, Pei D: Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 2010;6:71-79.
50. Wang T, Chen K, Zeng X, Yang J, Wu Y, Shi X, Qin B, Zeng L, Esteban MiguelA A, Pan G, Pei D: The histone demethylases jhdm1a/1b enhance somatic cell reprogramming in a vitamin-c-dependent manner. Cell Stem Cell 2011;9:575-587.
51. Blaschke K, Ebata KT, Karimi MM, Zepeda-Martinez JA, Goyal P, Mahapatra S, Tam A, Laird DJ, Hirst M, Rao A, Lorincz MC, Ramalho-Santos M: Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in es cells. Nature 2013;500:222-226.
52. Yamashita JK, Takano M, Hiraoka-Kanie M, Shimazu C, Peishi Y, Yanagi K, Nakano A, Inoue E, Kita F, Nishikawa S: Prospective identification of cardiac progenitors by a novel single cell-based cardiomyocyte induction. FASEB J 2005;19:1534-1536.
53. Qyang Y, Martin-Puig S, Chiravuri M, Chen S, Xu H, Bu L, Jiang X, Lin L, Granger A, Moretti A, Caron L, Wu X, Clarke J, Taketo MM, Laugwitz KL, Moon RT, Gruber P, Evans SM, Ding S, Chien KR: The renewal and differentiation of isll+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 2007;1:165-179.
54. Naito AT, Shiojima I, Akazawa H, Hidaka K, Morisaki T, Kikuchi A, Komuro I: Developmental stage-specific biphasic roles ofWnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U SA2006;103:19812-19817.
55. Nakamura T, Sano M, Songyang Z, Schneider MD: AWnt-and beta-catenin-dependent pathway for mammalian cardiac myogenesis. Proc Natl Acad Sci U S A2003;100:5834-5839.
56. David R, Brenner C, Stieber J, Schwarz F, Brunner S, Vollmer M, Mentele E, Muller-Hocker J, Kitajima S, Lickert H, Rupp R, Franz WM: Mespl drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade ofWnt-signalling. Nat Cell Biol 2008;10:338-345.
57. Willems E, Spiering S, Davidovics H, Lanier M, Xia Z, Dawson M, Cashman J, Mercola M: Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ Res 2011;109:360-364.
58. Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, Hsiao C, Kamp TJ, Palecek SP: Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions. Nat Protoc 2013;8:162-175.
59. Chung T-L, Brena RM, Kolle G, Grimmond SM, Berman BP, Laird PW, Pera MF, Wolvetang EJ: Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells 2010;28:1848-1855.
60. Gessert S, Kuhl M: The multiple phases and faces ofWnt signaling during cardiac differentiation and development. Circ Res 2010;107:186-199.
61. Xing W, Pourteymoor S, Mohan S: Ascorbic acid regulates osterix expression in osteoblasts by activation of prolyl hydroxylase and ubiquitination-mediated proteosomal degradation pathway. Physiol Genomics 2011;43:749-757.