Nuclear reprogramming with c-Myc potentiates glycolytic capacity of derived induced pluripotent stem cells

Journal of Cardiovascular Translational Research

Volumn 6, Issue 1, 2013, Pages 10-21

  Folmes, Clifford D L ^a   Martinez Fernandez, Almudena ^a   Faustino, Randolph S ^a   Yamada, Satsuki ^a   Perez Terzic, Carmen ^a   Nelson, Timothy J ^a   Terzic, Andre ^a,b  

^a Marriott Heart Disease Research Program   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Cardiac differentiation; Cardiogenesis; Glycolysis; iPS cells; Metabolomics; Mitochondria; Oxidative phosphorylation; Stem cell metabolism

Indexed keywords

MYC PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENO1 GENE; FIBROBLAST; GAPDH GENE; GENE; GLYCOLYSIS; HK2 GENE; LDHA GENE; LDHB GENE; METABOLOMICS; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATIVE PHOSPHORYLATION; PDHA1 GENE; PFKM GENE; PGHK1 GENE; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REAL TIME FLUX ANALYSIS; SEGREGATION ANALYSIS;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; GENE EXPRESSION REGULATION; GLYCOLYSIS; INDUCED PLURIPOTENT STEM CELLS; METABOLOMICS; MICE; MITOCHONDRIA; MYOCYTES, CARDIAC; NUCLEAR REPROGRAMMING; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS C-MYC; TIME FACTORS; TRANSFECTION;

IPS;

EID: 84872613340     PISSN: 19375387     EISSN: 19375395     Source Type: Journal    
DOI: 10.1007/s12265-012-9431-2     Document Type: Article

References (85)

1. Takahashi, K; & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126(4), 663-676. (Pubitemid 44233629)
2. Yamanaka, S. (2012). Induced pluripotent stem cells: past, present, and future. Cell Stem Cell, 10(6), 678-684.
3. Yu, J; Vodyanik, M. A; Smuga-Otto, K; Antosiewicz-Bourget, J; Frane, J. L; Tian, S; et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science, 318(5858), 1917-1920.
4. Wernig, M; Meissner, A; Foreman, R; Brambrink, T; Ku, M; Hochedlinger, K; et al. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature, 448(7151), 318-324. (Pubitemid 47080337)
5. Hochedlinger, K; & Plath, K. (2009). Epigenetic reprogramming and induced pluripotency. Development, 136(4), 509-523.
6. Nelson, T. J; & Terzic, A. (2011). Induced pluripotent stem cells: an emerging theranostics platform. Clinical Pharmacology and Therapeutics, 89(5), 648-650.
7. Inoue, H; & Yamanaka, S. (2011). The use of induced pluripotent stem cells in drug development. Clinical Pharmacology and Therapeutics, 89(5), 655-661.
8. Cherry, A. B; & Daley, G. Q. (2012). Reprogramming cellular identity for regenerative medicine. Cell, 148(6), 1110-1122.
9. Daley, G. Q. (2012). The promise and perils of stem cell therapeutics. Cell Stem Cell, 10(6), 740-749.
10. Sun, N; Longaker, M. T; & Wu, J. C. (2010). Human iPS cell-based therapy: considerations before clinical applications. Cell Cycle, 9(5), 880-885.
11. Hussein, S. M; Nagy, K; & Nagy, A. (2011). Human induced pluripotent stem cells: the past, present, and future. Clinical Pharmacology and Therapeutics, 89(5), 741-745.
12. Ghosh, Z; Huang, M; Hu, S; Wilson, K. D; Dey, D; & Wu, J. C. (2011). Dissecting the oncogenic and tumorigenic potential of differentiated human induced pluripotent stem cells and human embryonic stem cells. Cancer Research, 71(14), 5030-5039.
13. Wernig, M; Meissner, A; Cassady, J. P; & Jaenisch, R. (2008). c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell, 2(1), 10-12.
14. Nakagawa, M; Koyanagi, M; Tanabe, K; Takahashi, K; Ichisaka, T; Aoi, T; et al. (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotechnology, 26(1), 101-106.
15. Martinez-Fernandez, A; Nelson, T. J; Yamada, S; Reyes, S; Alekseev, A. E; Perez-Terzic, C; et al. (2009). iPS programmed without c-MYC yield proficient cardiogenesis for functional heart chimerism. Circulation Research, 105(7), 648-656.
16. Martinez-Fernandez, A; Nelson, T. J; & Terzic, A. (2011). Nuclear reprogramming strategy modulates differentiation potential of induced pluripotent stem cells. Journal of Cardiovascular Translational Research, 4(2), 131-137.
17. Martinez-Fernandez, A; Nelson, T. J; Ikeda, Y; & Terzic, A. (2010). c-MYC independent nuclear reprogramming favors cardiogenic potential of induced pluripotent stem cells. Journal of Cardiovascular Translational Research, 3(1), 13-23.
18. Varlakhanova, N. V; Cotterman, R. F; deVries, W. N; Morgan, J; Donahue, L. R; Murray, S; et al. (2010). myc maintains embryonic stem cell pluripotency and self-renewal. Differentiation, 80(1), 9-19.
19. Nakagawa, M; Takizawa, N; Narita, M; Ichisaka, T; & Yamanaka, S. (2010). Promotion of direct reprogramming by transformation-deficient Myc. Proceedings of the National Academy of Sciences of the United States of America, 107(32), 14152-14157.
20. Zhong, W; Mao, S; Tobis, S; Angelis, E; Jordan, M. C; Roos, K. P; et al. (2006). Hypertrophic growth in cardiac myocytes is mediated by Myc through a cyclin D2-dependent pathway. EMBO Journal, 25(16), 3869-3879. (Pubitemid 44300272)
21. Izumo, S; Nadal-Ginard, B; & Mahdavi, V. (1988). Protooncogene induction and reprogramming of cardiac gene expression produced by pressure overload. Proceedings of the National Academy of Sciences of the United States of America, 85(2), 339-343.
22. Xiao, G; Mao, S; Baumgarten, G; Serrano, J; Jordan, M. C; Roos, K. P; et al. (2001). Inducible activation of c-Myc in adult myocardium in vivo provokes cardiac myocyte hypertrophy and reactivation of DNA synthesis. Circulation Research, 89(12), 1122-1129. (Pubitemid 34627869)
23. Dang, C. V. (2012). MYC on the path to cancer. Cell, 149(1), 22-35.
24. Kim, J. W; Zeller, K. I; Wang, Y; Jegga, A. G; Aronow, B. J; O'Donnell, K. A; et al. (2004). Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Molecular and Cellular Biology, 24(13), 5923-5936. (Pubitemid 38787976)
25. Osthus, R. C; Shim, H; Kim, S; Li, Q; Reddy, R; Mukherjee, M; et al. (2000). Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. Journal of Biological Chemistry, 275(29), 21797-21800. (Pubitemid 30621745)
26. Shim, H; Dolde, C; Lewis, B. C; Wu, C. S; Dang, G; Jungmann, R. A; et al. (1997). c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proceedings of the National Academy of Sciences of the United States of America, 94(13), 6658-6663. (Pubitemid 27281920)
27. Li, F; Wang, Y; Zeller, K. I; Potter, J. J; Wonsey, D. R; O'Donnell, K. A; et al. (2005). Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Molecular and Cellular Biology, 25(14), 6225-6234. (Pubitemid 40946570)
28. Zhang, H; Gao, P; Fukuda, R; Kumar, G; Krishnamachary, B; Zeller, K. I; et al. (2007). HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell, 11(5), 407-420. (Pubitemid 46670080)
29. Gao, P; Tchernyshyov, I; Chang, T. C; Lee, Y. S; Kita, K; Ochi, T; et al. (2009). c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature, 458(7239), 762-765.
30. Liu, W; Le, A; Hancock, C; Lane, A. N; Dang, C. V; Fan, T. W; et al. (2012). Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proceedings of the National Academy of Sciences of the United States of America, 109(23), 8983-8988.
31. Warburg, O. (1956). On the origin of cancer cells. Science, 123(3191), 309-314.
32. Dang, C. V. (2007). The interplay between MYC and HIF in the Warburg effect. Ernst Schering Foundation Symposium Proceedings, 4, 35-53.
33. Folmes, C. D; Nelson, T. J; Martinez-Fernandez, A; Arrell, D. K; Lindor, J. Z; Dzeja, P. P; et al. (2011). Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metabolism, 14(2), 264-271.
34. Panopoulos, A. D; Yanes, O; Ruiz, S; Kida, Y. S; Diep, D; Tautenhahn, R; et al. (2012). The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming. Cell Research, 22(1), 168-177.
35. Zhu, S; Li, W; Zhou, H; Wei, W; Ambasudhan, R; Lin, T; et al. (2010). Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell, 7(6), 651-655.
36. Panopoulos, A. D; & Izpisua Belmonte, J. C. (2011). Anaerobicizing into pluripotency. Cell Metabolism, 14(2), 143-144.
37. Folmes, C. D; Dzeja, P. P; Nelson, T. J; & Terzic, A. (2012). Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell, 11(5), 596-606.
38. Varum, S; Rodrigues, A. S; Moura, M. B; Momcilovic, O; Easley, C. A; Ramalho-Santos, J; et al. (2011). Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One, 6(6), e20914.
39. Prigione, A; Fauler, B; Lurz, R; Lehrach, H; & Adjaye, J. (2010). The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells, 28(4), 721-733.
40. Armstrong, L; Tilgner, K; Saretzki, G; Atkinson, S. P; Stojkovic, M; Moreno, R; et al. (2010). Human induced pluripotent stem cell lines show similar stress defence mechanisms and mitochondrial regulation to human embryonic stem cells. Stem Cells, 28(4), 661-673.
41. Nelson, T. J; Martinez-Fernandez, A; Yamada, S; Mael, A. A; Terzic, A; & Ikeda, Y. (2009). Induced pluripotent reprogramming from promiscuous human stemness-related factors. Clinical and Translational Science, 2(2), 118-126.
42. Nelson, T. J; Martinez-Fernandez, A; Yamada, S; Perez-Terzic, C; Ikeda, Y; & Terzic, A. (2009). Repair of acute myocardial infarction by human stemness factors induced pluripotent stem cells. Circulation, 120(5), 408-416.
43. Zeller, K. I; Jegga, A. G; Aronow, B. J; O'Donnell, K. A; & Dang, C. V. (2003). An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biology, 4(10), R69.
44. Faustino, R. S; Behfar, A; Perez-Terzic, C; & Terzic, A. (2008). Genomic chart guiding embryonic stem cell cardiopoiesis. Genome Biology, 9(1), R6. (Pubitemid 351911941)
45. + Biomarkers select a cardiopoietic lineage from embryonic stem cells. Stem Cells, 26(14), 1464-1473.
46. Perez-Terzic, C; Faustino, R. S; Boorsma, B. J; Arrell, D. K; Niederlander, N. J; Behfar, A; et al. (2007). Stem cells transform into a cardiac phenotype with remodeling of the nuclear transport machinery. Nature Clinical Practice. Cardiovascular Medicine, 4(Suppl 1), S68-76. (Pubitemid 46151907)
47. Turner, W. S; Seagle, C; Galanko, J. A; Favorov, O; Prestwich, G. D; Macdonald, J. M; et al. (2008). Nuclear magnetic resonance metabolomic footprinting of human hepatic stem cells and hepatoblasts cultured in hyaluronan-matrix hydrogels. Stem Cells, 26(6), 1547-1555.
48. Shao, G; Kautz, R; Peng, S; Cui, G; & Giese, R. W. (2007). Calibration by NMR for quantitative analysis: p-toluenesulfonic acid as a reference substance. Journal of Chromatography. A, 1138(1-2), 305-308. (Pubitemid 44908336)
49. Govindaraju, V; Young, K; & Maudsley, A. A. (2000). Proton NMR chemical shifts and coupling constants for brain metabolites. NMR in Biomedicine, 13(3), 129-153. (Pubitemid 30414704)
50. Wishart, D. S; Knox, C; Guo, A. C; Eisner, R; Young, N; Gautam, B; et al. (2009). HMDB: a knowledgebase for the human metabolome. Nucleic Acids Research, 37(Database issue), D603-610.
51. Wu, M; Neilson, A; Swift, A. L; Moran, R; Tamagnine, J; Parslow, D; et al. (2007). Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. American Journal of Physiology. Cell Physiology, 292(1), C125-136. (Pubitemid 46115126)
52. Zhang, J; Nuebel, E; Wisidagama, D. R; Setoguchi, K; Hong, J. S; Van Horn, C. M; et al. (2012). Measuring energy metabolism in cultured cells, including human pluripotent stem cells and differentiated cells. Nature Protocols, 7(6), 1068-1085.
53. Xia, J; Psychogios, N; Young, N; & Wishart, D. S. (2009). MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Research, 37(Web Server issue), W652-660.
54. Xia, J; Mandal, R; Sinelnikov, I. V; Broadhurst, D; & Wishart, D. S. (2012). MetaboAnalyst 2.0 - a comprehensive server for metabolomic data analysis. Nucleic Acids Research, 40(Web Server issue), W127-133.
55. Lindon, J. C; & Nicholson, J. K. (2008). Spectroscopic and statistical techniques for information recovery in metabonomics and metabolomics. Annual Review of Analytical Chemistry, 1, 45-69.
56. Folmes, C. D; Nelson, T. J; Dzeja, P. P; & Terzic, A. (2012). Energy metabolism plasticity enables stemness programs. Annals of the New York Academy of Sciences, 1254(1), 82-89.
57. Prigione, A; Lichtner, B; Kuhl, H; Struys, E. A; Wamelink, M; Lehrach, H; et al. (2011). Human induced pluripotent stem cells harbor homoplasmic and heteroplasmic mitochondrial DNA mutations while maintaining human embryonic stem cell-like metabolic reprogramming. Stem Cells, 29(9), 1338-1348.
58. Zeuschner, D; Mildner, K; Zaehres, H; & Scholer, H. R. (2010). Induced pluripotent stem cells at nanoscale. Stem Cells and Development, 19(5), 615-620.
59. Suhr, S. T; Chang, E. A; Tjong, J; Alcasid, N; Perkins, G. A; Goissis, M. D; et al. (2010). Mitochondrial rejuvenation after induced pluripotency. PLoS One, 5(11), e14095.
60. Yoshida, Y; Takahashi, K; Okita, K; Ichisaka, T; & Yamanaka, S. (2009). Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell, 5(3), 237-241.
61. Kawamura, T; Suzuki, J; Wang, Y. V; Menendez, S; Morera, L. B; Raya, A; et al. (2009). Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature, 460(7259), 1140-1144.
62. Banito, A; Rashid, S. T; Acosta, J. C; Li, S; Pereira, C. F; Geti, I; et al. (2009). Senescence impairs successful reprogramming to pluripotent stem cells. Genes & Development, 23(18), 2134-2139.
63. Bensaad, K; Tsuruta, A; Selak, M. A; Vidal, M. N; Nakano, K; Bartrons, R; et al. (2006). TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell, 126(1), 107-120. (Pubitemid 44040989)
64. Hong, H; Takahashi, K; Ichisaka, T; Aoi, T; Kanagawa, O; Nakagawa, M; et al. (2009). Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature, 460(7259), 1132-1135.
65. Li, H; Collado, M; Villasante, A; Strati, K; Ortega, S; Canamero, M; et al. (2009). The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature, 460(7259), 1136-1139.
66. Marion, R. M; Strati, K; Li, H; Murga, M; Blanco, R; Ortega, S; et al. (2009). A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature, 460(7259), 1149-1153.
67. Folmes, C. D. L; Dzeja, P. P; Nelson, T. J; & Terzic, A. (2012). Mitochondria in control of cell fate. Circulation Research, 110(4), 526-529.
68. Chung, S; Arrell, D. K; Faustino, R. S; Terzic, A; & Dzeja, P. P. (2010). Glycolytic network restructuring integral to the energetics of embryonic stem cell cardiac differentiation. Journal of Molecular and Cellular Cardiology, 48(4), 725-734.
69. Chung, S; Dzeja, P. P; Faustino, R. S; Perez-Terzic, C; Behfar, A; & Terzic, A. (2007). Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nature Clinical Practice. Cardiovascular Medicine, 4(Suppl 1), S60-67. (Pubitemid 46151906)
70. Folmes, C. D; Nelson, T. J; & Terzic, A. (2011). Energy metabolism in nuclear reprogramming. Biomarkers in Medicine, 5(6), 715-729.
71. Dzeja, P. P; Chung, S; Faustino, R. S; Behfar, A; & Terzic, A. (2011). Developmental enhancement of adenylate kinase-AMPK metabolic signaling axis supports stem cell cardiac differentiation. PLoS One, 6(4), e19300.
72. St John, J. C; Ramalho-Santos, J; Gray, H. L; Petrosko, P; Rawe, V. Y; Navara, C. S; et al. (2005). The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning and Stem Cells, 7(3), 141-153. (Pubitemid 43150270)
73. Cho, Y. M; Kwon, S; Pak, Y. K; Seol, H. W; Choi, Y. M; do Park, J; et al. (2006). Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochemical and Biophysical Research Communications, 348(4), 1472-1478. (Pubitemid 44291363)
74. Facucho-Oliveira, J. M; Alderson, J; Spikings, E. C; Egginton, S; & St John, J. C. (2007). Mitochondrial DNA replication during differentiation of murine embryonic stem cells. Journal of Cell Science, 120(Pt 22), 4025-4034. (Pubitemid 350269408)
75. Facucho-Oliveira, J. M; & St John, J. C. (2009). The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Reviews and Reports, 5(2), 140-158.
76. Hom, J. R; Quintanilla, R. A; Hoffman, D. L; de Mesy Bentley, K. L; Molkentin, J. D; Sheu, S. S; et al. (2011). The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Developmental Cell, 21(3), 469-478.
77. Bracha, A. L; Ramanathan, A; Huang, S; Ingber, D. E; & Schreiber, S. L. (2010). Carbon metabolism-mediated myogenic differentiation. Nature Chemical Biology, 6(3), 202-204.
78. Zhang, J; Khvorostov, I; Hong, J. S; Oktay, Y; Vergnes, L; Nuebel, E; et al. (2011). UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO Journal, 30(24), 4860-4873.
79. Tormos, K. V; Anso, E; Hamanaka, R. B; Eisenbart, J; Joseph, J; Kalyanaraman, B; et al. (2011). Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metabolism, 14(4), 537-544.
80. Varum, S; Momcilovic, O; Castro, C; Ben-Yehudah, A; Ramalho-Santos, J; & Navara, C. S. (2009). Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem Cell Research, 3(2-3), 142-156.
81. Lonergan, T; Brenner, C; & Bavister, B. (2006). Differentiation- related changes in mitochondrial properties as indicators of stem cell competence. Journal of Cellular Physiology, 208(1), 149-153. (Pubitemid 43848999)
82. San Martin, N; Cervera, A. M; Cordova, C; Covarello, D; McCreath, K. J; & Galvez, B. G. (2011). Mitochondria determine the differentiation potential of cardiac mesoangioblasts. Stem Cells, 29(7), 1064-1074.
83. Schieke, S. M; Ma, M; Cao, L; McCoy, J. P; Jr; Liu, C; Hensel, N. F; et al. (2008). Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells. Journal of Biological Chemistry, 283(42), 28506-28512.
84. Brambrink, T; Foreman, R; Welstead, G. G; Lengner, C. J; Wernig, M; Suh, H; et al. (2008). Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell, 2(2), 151-159. (Pubitemid 351168714)
85. Sommer, C. A; Sommer, A. G; Longmire, T. A; Christodoulou, C; Thomas, D. D; Gostissa, M; et al. (2010). Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells, 28(1), 64-74.