Differentiate or die: 3-Bromopyruvate and pluripotency in mouse embryonic stem cells

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Rodrigues, Ana Sofia ^a   Pereira, Sandro L ^a   Correia, Marcelo ^a,b   Gomes, Andreia ^a,b,c   Perestrelo, Tânia ^a,b   Ramalho Santos, João ^a,d  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c Biocant Center of Innovation in Biotechnology   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

3 BROMOPYRUVATE; PYRUVIC ACID DERIVATIVE; UNCLASSIFIED DRUG; BROMOPYRUVATE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DAMAGE; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL METABOLISM; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME SPECIFICITY; EXPERIMENTAL STUDY; GLYCOLYSIS; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; ANIMAL; CYTOLOGY; DRUG EFFECTS; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY;

ANIMALS; CELL DIFFERENTIATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EMBRYONIC STEM CELLS; FLOW CYTOMETRY; GLYCOLYSIS; MICE; PLURIPOTENT STEM CELLS; PYRUVATES;

EID: 84942843640     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135617     Document Type: Article

References (51)

1. Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, Bernard D, et al. A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal. 2007; 9 (3):293-9. Epub 2006/12/23. PMID: 17184172.
2. Cho YM, Kwon S, Pak YK, Seol HW, Choi YM, Park do J, et al. Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun. 2006; 348(4):1472-8. Epub 2006/08/22. S0006-291X(06) 01821-3 [pii] doi: 10.1016/j.bbrc.2006.08.020 PMID: 16920071.
3. St John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY, Navara CS, et al. The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells. 2005; 7(3):141-53. Epub 2005/09/24. doi: 10.1089/clo.2005.7.141 PMID: 16176124.
4. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med. 2007; 4 Suppl 1:S60-7. Epub 2007/01/19. ncpcardio0766 [pii] doi: 10.1038/ncpcardio0766 PMID: 17230217.
5. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells. 2011; 29(3):486-95. Epub 2011/03/23. doi: 10.1002/stem.590 PMID: 21425411.
6. Tamai M, Yamashita A, Tagawa Y. Mitochondrial development of the in vitro hepatic organogenesis model with simultaneous cardiac mesoderm differentiation from murine induced pluripotent stem cells. J Biosci Bioeng. 2011; 112(5):495-500. Epub 2011/08/06. S1389-1723(11)00264-7 [pii] doi: 10.1016/j.jbiosc.2011.07.005 PMID: 21816670.
7. Pereira SL, Rodrigues AS, Sousa MI, Correia M, Perestrelo T, Ramalho-Santos J. From gametogenesis and stem cells to cancer: common metabolic themes. Hum Reprod Update. 2014. Epub 2014/07/12. dmu034 [pii] doi: 10.1093/humupd/dmu034 PMID: 25013216.
8. Pereira SL, Graos M, Rodrigues AS, Anjo SI, Carvalho RA, Oliveira PJ, et al. Inhibition of mitochondrial complex III blocks neuronal differentiation and maintains embryonic stem cell pluripotency. PLoS One. 2013; 8(12):e82095. Epub 2013/12/07. [pii]. PMID: 24312632; PubMed Central PMCID: PMC3847032.
9. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ, Dzeja PP, et al. Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab. 2011; 14(2):264-71. Epub 2011/08/02. S1550-4131(11)00260-9 [pii] doi: 10.1016/j.cmet.2011.06.011 PMID: 21803296; PubMed Central PMCID: PMC3156138.
10. Manganelli G, Fico A, Masullo U, Pizzolongo F, Cimmino A, Filosa S. Modulation of the pentose phosphate pathway induces endodermal differentiation in embryonic stem cells. PLoS One. 2012; 7(1): e29321. Epub 2012/01/19. doi: 10.1371/journal.pone.0029321 PONE-D-11-01982 [pii]. PMID: 22253711; PubMed Central PMCID: PMC3257253.
11. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CAt, Ramalho-Santos J, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One. 2011; 6 (6):e20914. Epub 2011/06/24. doi: 10.1371/journal.pone.0020914 PONE-D-11-02358 [pii]. PMID: 21698063; PubMed Central PMCID: PMC3117868.
12. Ngo H, Tortorella SM, Ververis K, Karagiannis TC. The Warburg effect: molecular aspects and therapeutic possibilities. Mol Biol Rep. 2014. Epub 2014/09/26. doi: 10.1007/s11033-014-3764-7 PMID: 25253100.
13. Peng Q, Zhou J, Zhou Q, Pan F, Zhong D, Liang H. Silencing hexokinase II gene sensitizes human colon cancer cells to 5-fluorouracil. Hepatogastroenterology. 2009; 56(90):355-60. Epub 2009/07/08. PMID: 19579598.
14. Wolf A, Agnihotri S, Micallef J, Mukherjee J, Sabha N, Cairns R, et al. Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J Exp Med. 2011; 208(2):313-26. Epub 2011/01/19. jem.20101470 [pii] doi: 10.1084/jem.20101470 PMID: 21242296; PubMed Central PMCID: PMC3039857.
15. Dang CV, Semenza GL. Oncogenic alterations of metabolism. Trends Biochem Sci. 1999; 24(2):68-72. Epub 1999/03/31. S0968-0004(98)01344-9 [pii]. PMID: 10098401.
16. Prigione A, Rohwer N, Hoffmann S, Mlody B, Drews K, Bukowiecki R, et al. HIF1alpha modulates cell fate reprogramming through early glycolytic shift and upregulation of PDK1-3 and PKM2. Stem Cells. 2014; 32(2):364-76. doi: 10.1002/stem.1552 PMID: 24123565.
17. Pistollato F, Chen HL, Rood BR, Zhang HZ, D'Avella D, Denaro L, et al. Hypoxia and HIF1alpha repress the differentiative effects of BMPs in high-grade glioma. Stem Cells. 2009; 27(1):7-17. Epub 2008/10/04. 2008-0402 [pii] doi: 10.1634/stemcells.2008-0402 PMID: 18832593.
18. Jogi A, Ora I, Nilsson H, Lindeheim A, Makino Y, Poellinger L, et al. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci U S A. 2002; 99(10):7021-6. Epub 2002/05/16. doi: 10.1073/pnas.102660199 99/10/7021 [pii]. PMID: 12011461; PubMed Central PMCID: PMC124521.
19. Folmes CD, Martinez-Fernandez A, Faustino RS, Yamada S, Perez-Terzic C, Nelson TJ, et al. Nuclear reprogramming with c-Myc potentiates glycolytic capacity of derived induced pluripotent stem cells. J Cardiovasc Transl Res. 2013; 6(1):10-21. Epub 2012/12/19. doi: 10.1007/s12265-012-9431-2 PMID: 23247633.
20. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008; 134(5):703-7. Epub 2008/09/09. S0092-8674(08)01066-0 [pii] doi: 10.1016/j.cell.2008.08.021 PMID: 18775299.
21. Glick M, Biddle P, Jantzi J, Weaver S, Schirch D. The antitumor agent 3-bromopyruvate has a short half-life at physiological conditions. Biochem Biophys Res Commun. 2014; 452(1):170-3. doi: 10.1016/j.bbrc.2014.08.066 PMID: 25152397.
22. Pietzke M, Zasada C, Mudrich S, Kempa S. Decoding the dynamics of cellular metabolism and the action of 3-bromopyruvate and 2-deoxyglucose using pulsed stable isotope-resolved metabolomics. Cancer & metabolism. 2014; 2:9. doi: 10.1186/2049-3002-2-9 PMID: 25035808; PubMed Central PMCID: PMC4101711.
23. Ko YH, Smith BL, Wang Y, Pomper MG, Rini DA, Torbenson MS, et al. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem Biophys Res Commun. 2004; 324 (1):269-75. Epub 2004/10/07. S0006-291X(04)02062-5 [pii] doi: 10.1016/j.bbrc.2004.09.047 PMID: 15465013.
24. Isayev O, Rausch V, Bauer N, Liu L, Fan P, Zhang Y, et al. Inhibition of glucose turnover by 3-bromopyruvate counteracts pancreatic cancer stem cell features and sensitizes cells to gemcitabine. Oncotarget. 2014; 5(13):5177-89. PMID: 25015789; PubMed Central PMCID: PMC4148131.
25. Galina A. Mitochondria: 3-bromopyruvate vs. mitochondria? A small molecule that attacks tumors by targeting their bioenergetic diversity. Int J Biochem Cell Biol. 2014; 54:266-71. doi: 10.1016/j.biocel.2014.05.013 PMID: 24842108.
26. Wakayama T, Rodriguez I, Perry AC, Yanagimachi R, Mombaerts P. Mice cloned from embryonic stem cells. Proc Natl Acad Sci U S A. 1999; 96(26):14984-9. Epub 1999/12/28. PMID: 10611324; PubMed Central PMCID: PMC24759.
27. Ohtsuka M, Ishii K, Kikuti YY, Warita T, Suzuki D, Sato M, et al. Construction of mouse 129/Ola BAC library for targeting experiments using E14 embryonic stem cells. Genes Genet Syst. 2006; 81(2):143-6. Epub 2006/06/07. JST.JSTAGE/ggs/81.143 [pii]. PMID: 16755138.
28. Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev. 2005; 11:127-52. Epub 2005/10/12. S1387-2656(05)11004-7 [pii] doi: 10.1016/S1387-2656(05)11004-7 PMID: 16216776.
29. O'Connor MD, Kardel MD, Eaves CJ. Functional assays for human embryonic stem cell pluripotency. Methods Mol Biol. 2011; 690:67-80. Epub 2010/11/03. doi: 10.1007/978-1-60761-962-8-4 PMID: 21042985.
30. Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. Mitochondrial membrane potential probesand the proton gradient: a practical usage guide. Biotechniques. 2011; 50(2):98-115. Epub 2011/04/14. 000113610 [pii] doi: 10.2144/000113610 PMID: 21486251; PubMed Central PMCID: PMC3115691.
31. Schieke SM, Ma M, Cao L, McCoy JP Jr., Liu C, Hensel NF, et al. Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells. J Biol Chem. 2008; 283 (42):28506-12. Epub 2008/08/21. M802763200 [pii] doi: 10.1074/jbc.M802763200 PMID: 18713735; PubMed Central PMCID: PMC2568919.
32. Floryk D, Houstek J. Tetramethyl rhodamine methyl ester (TMRM) is suitable for cytofluorometric measurements of mitochondrial membrane potential in cells treated with digitonin. Biosci Rep. 1999; 19 (1):27-34. Epub 1999/06/24. PMID: 10379904.
33. Mukhopadhyay P, Rajesh M, Hasko G, Hawkins BJ, Madesh M, Pacher P. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc. 2007; 2(9):2295-301. Epub 2007/09/15. nprot.2007.327 [pii] doi: 10.1038/nprot.2007.327 PMID: 17853886; PubMed Central PMCID: PMC2225540.
34. Lee S, Van Remmen H, Csete M. Sod2 overexpression preserves myoblast mitochondrial mass and function, but not muscle mass with aging. Aging Cell. 2009; 8(3):296-310. Epub 2009/07/25. ACE477 [pii] doi: 10.1111/j.1474-9726.2009.00477.x PMID: 19627269.
35. Dingley S, Chapman KA, Falk MJ. Fluorescence-activated cell sorting analysis of mitochondrial content, membrane potential, and matrix oxidant burden in human lymphoblastoid cell lines. Methods Mol Biol. 2012; 837:231-9. Epub 2012/01/05. doi: 10.1007/978-1-61779-504-6-16 PMID: 22215552; PubMed Central PMCID: PMC3590112.
36. Mahler M, Miyachi K, Peebles C, Fritzler MJ. The clinical significance of autoantibodies to the proliferating cell nuclear antigen (PCNA). Autoimmun Rev. 2012; 11(10):771-5. Epub 2012/03/03. S1568-9972 (12)00040-7 [pii] doi: 10.1016/j.autrev.2012.02.012 PMID: 22381917.
37. Nair RP, Krishnan LK. Identification of p63+ keratinocyte progenitor cells in circulation and their matrixdirected differentiation to epithelial cells. Stem Cell Res Ther. 2013; 4(2):38. Epub 2013/04/13. scrt186 [pii] doi: 10.1186/scrt186 PMID: 23578397.
38. Amaral S, Mota PC, Lacerda B, Alves M, Pereira Mde L, Oliveira PJ, et al. Testicular mitochondrial alterations in untreated streptozotocin-induced diabetic rats. Mitochondrion. 2009; 9(1):41-50. Epub 2008/12/23. S1567-7249(08)00106-2 [pii] doi: 10.1016/j.mito.2008.11.005 PMID: 19100345.
39. Stocchi V, Cucchiarini L, Magnani M, Chiarantini L, Palma P, Crescentini G. Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal Biochem. 1985; 146(1):118-24. Epub 1985/04/01. 0003-2697(85)90405-1 [pii]. PMID: 3993925.
40. Varum S, Momcilovic O, Castro C, Ben-Yehudah A, Ramalho-Santos J, Navara CS. Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem Cell Res. 2009; 3(2-3):142-56. Epub 2009/09/01. S1873-5061(09)00085-3 [pii] doi: 10.1016/j.scr.2009.07.002 PMID: 19716358; PubMed Central PMCID: PMC2837416.
41. Ko YH, Verhoeven HA, Lee MJ, Corbin DJ, Vogl TJ, Pedersen PL. A translational study "case report" on the small molecule "energy blocker" 3-bromopyruvate (3BP) as a potent anticancer agent: from bench side to bedside. J Bioenerg Biomembr. 2012; 44(1):163-70. Epub 2012/02/14. doi: 10.1007/s10863-012-9417-4 PMID: 22328020.
42. O'Connor MD, Kardel MD, Iosfina I, Youssef D, Lu M, Li MM, et al. Alkaline phosphatase-positive colony formation is a sensitive, specific, and quantitative indicator of undifferentiated human embryonic stem cells. Stem Cells. 2008; 26(5):1109-16. Epub 2008/02/16. 2007-0801 [pii] doi: 10.1634/stemcells.2007-0801 PMID: 18276800.
43. Macchioni L, Davidescu M, Sciaccaluga M, Marchetti C, Migliorati G, Coaccioli S, et al. Mitochondrial dysfunction and effect of antiglycolytic bromopyruvic acid in GL15 glioblastoma cells. J Bioenerg Biomembr. 2011; 43(5):507-18. Epub 2011/08/13. doi: 10.1007/s10863-011-9375-2 PMID: 21833601.
44. Rodrigues JR-SaAS. From Oocytes and Pluripotent Stem Cells to Fully Differentiated Fates: (Also) a Mitochondrial Odyssey. In: John JCS, editor. Mitochondrial DNA, Mitochondria, Disease and Stem Cells: Humana Press; 2012. p. 69-86.
45. Qin JZ, Xin H, Nickoloff BJ. 3-Bromopyruvate induces necrotic cell death in sensitive melanoma cell lines. Biochem Biophys Res Commun. 2010; 396(2):495-500. Epub 2010/05/01. S0006-291X(10) 00819-3 [pii] doi: 10.1016/j.bbrc.2010.04.126 PMID: 20430010.
46. Zhang Q, Zhang Y, Zhang P, Chao Z, Xia F, Jiang C, et al. Hexokinase II inhibitor, 3-BrPA induced autophagy by stimulating ROS formation in human breast cancer cells. Genes & cancer. 2014; 5(3-4):100-12. PMID: 25053988; PubMed Central PMCID: PMC4091531.
47. Kim JS, Ahn KJ, Kim JA, Kim HM, Lee JD, Lee JM, et al. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells: ROS-mediated cell death by 3-BrPA. J Bioenerg Biomembr. 2008; 40(6):607-18. Epub 2008/12/11. doi: 10.1007/s10863-008-9188-0 PMID: 19067133.
48. Xu RH, Pelicano H, Zhou Y, Carew JS, Feng L, Bhalla KN, et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 2005; 65(2):613-21. Epub 2005/02/08. 65/2/613 [pii]. PMID: 15695406.
49. Kreis NN, Louwen F, Yuan J. Less understood issues: p21 in mitosis and its therapeutic potential. Oncogene. 2014; 0. Epub 2014/05/27. onc2014133 [pii] doi: 10.1038/onc.2014.133 PMID: 24858045.
50. Strzalka W, Ziemienowicz A. Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Annals of botany. 2011; 107(7):1127-40. doi: 10.1093/aob/mcq243 PMID: 21169293; PubMed Central PMCID: PMC3091797.
51. Zhou W, Choi M, Margineantu D, Margaretha L, Hesson J, Cavanaugh C, et al. HIF1α induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J. 2012 May 2; 31(9):2103-16. doi: 10.1038/emboj.2012.71 Epub 2012 Mar 23. PMID: 22446391.