Directed Differentiation of Embryonic Stem Cells into Cardiomyocytes by Bacterial Injection of Defined Transcription Factors

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bai, Fang ^a,b   Ho Lim, Chae ^b,d   Jia, Jingyue ^a,b   Santostefano, Katherine ^b   Simmons, Chelsey ^c   Kasahara, Hideko ^b   Wu, Weihui ^a   Terada, Naohiro ^b   Jin, Shouguang ^a,b  

^a NANKAI UNIVERSITY   (China)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GATA4 PROTEIN, MOUSE; MEF2C PROTEIN, MOUSE; MYOCYTE ENHANCER FACTOR 2; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4;

ANIMAL; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOUSE; MOUSE EMBRYONIC STEM CELL; PROCEDURES; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME FACTOR; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION; HELA CELLS; HUMANS; MEF2 TRANSCRIPTION FACTORS; MICE; MICROSCOPY, FLUORESCENCE; MOUSE EMBRYONIC STEM CELLS; MYOCYTES, CARDIAC; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-BOX DOMAIN PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84944096799     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep15014     Document Type: Article

References (66)

1. Chambers, S. M. & Studer, L. Cell fate plug and play: direct reprogramming and induced pluripotency. Cell 145, 827-830 (2011).
2. Cherry, A. B. & Daley, G. Q. Reprogramming cellular identity for regenerative medicine. Cell 148, 1110-1122 (2012).
3. Yamanaka, S. & Blau, H. M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704-712 (2010).
4. Khan, M. et al. Delivery of reprogramming factors into fibroblasts for generation of non-genetic induced pluripotent stem cells using a cationic bolaamphiphile as a non-viral vector. Biomaterials 34, 5336-5343 (2013).
5. Zhou, H. et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381-384 (2009).
6. Gellatly, S. L. & Hancock, R. E. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67, 159-173 (2013).
7. Hauser, A. R. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7, 654-665 (2009).
8. Rangel, S. M., Logan, L. K. & Hauser, A. R. The ADP-ribosyltransferase domain of the effector protein ExoS inhibits phagocytosis of Pseudomonas aeruginosa during pneumonia. MBio 5, e01080-14 (2014).
9. Bichsel, C. et al. Bacterial delivery of nuclear proteins into pluripotent and differentiated cells. PLoS One 6, e16465 (2011).
10. Jia, J. et al. Bacterial delivery of TALEN proteins for human genome editing. PLoS One 9, e91547 (2014).
11. Bichsel, C. et al. Direct reprogramming of fibroblasts to myocytes via bacterial injection of MyoD protein. Cell Reprogram 15, 117-125 (2013).
12. Ford, E. S. et al. Explaining the decrease in U.S. deaths from coronary disease, 1980-2000. N Engl J Med 356, 2388-2398 (2007).
13. Levy, D. et al. Long-term trends in the incidence of and survival with heart failure. N Engl J Med 347, 1397-1402 (2002).
14. Lloyd-Jones, D. M. et al. Prediction of lifetime risk for cardiovascular disease by risk factor burden at 50 years of age. Circulation 113, 791-798 (2006).
15. Burridge, P. W., Keller, G., Gold, J. D. & Wu, J. C. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 10, 16-28 (2012).
16. Mummery, C. L. et al. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ Res 111, 344-358 (2012).
17. Buikema, J. W., Van Der Meer, P., Sluijter, J. P. & Domian, I. J. Concise review: Engineering myocardial tissue: the convergence of stem cells biology and tissue engineering technology. Stem Cells 31, 2587-2598 (2013).
18. Inagawa, K. & Ieda, M. Direct reprogramming of mouse fibroblasts into cardiac myocytes. J Cardiovasc Transl Res 6, 37-45 (2013).
19. Ieda, M. et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142, 375-386 (2010).
20. Qian, L. et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485, 593-598 (2012).
21. Song, K. et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485, 599-604 (2012).
22. Protze, S. et al. A new approach to transcription factor screening for reprogramming of fibroblasts to cardiomyocyte-like cells. J Mol Cell Cardiol 53, 323-332 (2012).
23. Fu, J. D. et al. Direct reprogramming of human fibroblasts toward a cardiomyocyte-like state. Stem Cell Reports 1, 235-247 (2013).
24. Wada, R. et al. Induction of human cardiomyocyte-like cells from fibroblasts by defined factors. Proc Natl Acad Sci USA 110, 12667-12672 (2013).
25. Olson, E. N. Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927 (2006).
26. Zhao, R. et al. Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Dev Biol 317, 614-619 (2008).
27. Bruneau, B. G. et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106, 709-721 (2001).
28. Garg, V. et al. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424, 443-447 (2003).
29. Ghosh, T. K. et al. Physical interaction between TBX5 and MEF2C is required for early heart development. Mol Cell Biol 29, 2205-2218 (2009).
30. Neeld, D. et al. Pseudomonas aeruginosa injects NDK into host cells through a type III secretion system. Microbiology 160, 1417-1426 (2014).
31. Durand, E. et al. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J Bacteriol 185, 2749-2758 (2003).
32. Rumbaugh, K. P., Griswold, J. A. & Hamood, A. N. The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect 2, 1721-1731 (2000).
33. Wu, H. et al. Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147, 1105-1113 (2001).
34. Sundin, C., Thelaus, J., Broms, J. E. & Forsberg, A. Polarisation of type III translocation by Pseudomonas aeruginosa requires PcrG, PcrV and PopN. Microb Pathog 37, 313-322 (2004).
35. Yang, H. et al. Regulatory role of PopN and its interacting partners in type III secretion of Pseudomonas aeruginosa. J Bacteriol 189, 2599-2609 (2007).
36. Yahr, T. L. & Wolfgang, M. C. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 62, 631-640 (2006).
37. Schoehn, G. et al. Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas. EMBO J 22, 4957-4967 (2003).
38. Creighton, T. E. Proteins: Structures and Molecular Properties 2nd edn, Ch. 10, 463-473 (W H Freeman and Company, 1993).
39. Takahashi, T. et al. Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107, 1912-1916 (2003).
40. Box, G. E. P. & Draper, N. R. Response surfaces, mixtures, and ridge analysis 2nd edn, Ch. 1, 1-14 (John Wiley & Sons, 2007).
41. Kishore, D. & Kayastha, A. M. Optimisation of immobilisation conditions for chick pea beta-galactosidase (CpGAL) to alkylamine glass using response surface methodology and its applications in lactose hydrolysis. Food Chem 134, 1650-1657 (2012).
42. Cornell, J. A. Experiments with mixtures: designs, models, and the analysis of mixture data 3th edn, Ch. 5, 223-277 (John Wiley & Sons, 2002).
43. Kishore, D., Talat, M., Srivastava, O. N. & Kayastha, A. M. Immobilization of beta-galactosidase onto functionalized graphene nano-sheets using response surface methodology and its analytical applications. PLoS One 7, e40708 (2012).
44. Boheler, K. R. et al. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 91, 189-201 (2002).
45. Murry, C. E. & Keller, G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680 (2008).
46. Kubo, A. et al. Development of definitive endoderm from embryonic stem cells in culture. Development 131, 1651-1662 (2004).
47. Singh, A. M. & Terada, N. Bypassing heterogeneity: the road to embryonic stem cell-derived cardiomyocyte specification. Trends Cardiovasc Med 17, 96-101 (2007).
48. Guan, K. et al. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ Res 100, 1615-1625 (2007).
49. Reppel, M., Boettinger, C. & Hescheler, J. Beta-adrenergic and muscarinic modulation of human embryonic stem cell-derived cardiomyocytes. Cell Physiol Biochem 14, 187-196 (2004).
50. Makkerh, J. P., Dingwall, C. & Laskey, R. A. Comparative mutagenesis of nuclear localization signals reveals the importance of neutral and acidic amino acids. Curr Biol 6, 1025-1027 (1996).
51. Cansizoglu, A. E., Lee, B. J., Zhang, Z. C., Fontoura, B. M. & Chook, Y. M. Structure-based design of a pathway-specific nuclear import inhibitor. Nat Struct Mol Biol 14, 452-454 (2007).
52. Lee, B. J. et al. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 126, 543-558 (2006).
53. Hirel, P. H., Schmitter, M. J., Dessen, P., Fayat, G. & Blanquet, S. Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc Natl Acad Sci USA 86, 8247-8251 (1989).
54. Zhang, Y., Deng, Q. & Barbieri, J. T. Intracellular localization of type III-delivered Pseudomonas ExoS with endosome vesicles. J Biol Chem 282, 13022-13032 (2007).
55. Rajala, K., Pekkanen-Mattila, M. & Aalto-Setala, K. Cardiac differentiation of pluripotent stem cells. Stem Cells Int 2011, 383709-383721 (2011).
56. Gadue, P., Huber, T. L., Paddison, P. J. & 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, 16806-16811 (2006).
57. Lindsley, R. C., Gill, J. G., Kyba, M., Murphy, T. L. & Murphy, K. M. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133, 3787-96 (2006).
58. Fox, I. J. et al. Stem cell therapy. Use of differentiated pluripotent stem cells as replacement therapy for treating disease. Science 345, 1247391 (2014).
59. Yang, X., Pabon, L. & Murry, C. E. Engineering adolescence: maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Res 114, 511-523 (2014).
60. Fehling, H. J. et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130, 4217-4227 (2003).
61. Zhang, Y. H., Wang, Y., Yusufali, A. H. & Ling, C. Cytotoxic genes from traditional Chinese medicine inhibit tumor growth both in vitro and in vivo. Journal of integrative medicine 12, 483-494 (2014).
62. Hamazaki, T., Oka, M., Yamanaka, S. & Terada, N. Aggregation of embryonic stem cells induces Nanog repression and primitive endoderm differentiation. J Cell Sci 117, 5681-5686 (2004).
63. Santiago, J. G., Wereley, S. T., Meinhart, C. D., Beebe, D. J. & Adrian, R. J. A particle image velocimetry system for microfluidics. Experiments in Fluids 25, 316-319 (1998).
64. Navarrete, E. G. et al. Screening drug-induced arrhythmia [corrected] using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 128, S3-13 (2013).
65. West, S. E., Schweizer, H. P., Dall, C., Sample, A. K. & Runyen-Janecky, L. J. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148, 81-86 (1994).
66. Ha, U. & Jin, S. Growth phase-dependent invasion of Pseudomonas aeruginosa and its survival within HeLa cells. Infect Immun 69, 4398-4406 (2001).