Inhibition of mitochondrial complex III blocks neuronal differentiation and maintains embryonic stem cell pluripotency

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Pereira, Sandro L ^a,b   Grãos, Mário ^c   Rodrigues, Ana Sofia ^a,b   Anjo, Sandra I ^a,b   Carvalho, Rui A ^a,b   Oliveira, Paulo J ^a,b   Arenas, Ernest ^d   Ramalho Santos, João ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c Biocant Technology Transfer Association   (Portugal)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; ANTIMYCIN A1; CASPASE 3; CASPASE 7; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OCTAMER TRANSCRIPTION FACTOR 4; REACTIVE OXYGEN METABOLITE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL LOSS; CELL PROLIFERATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYONIC STEM CELL; ENZYME INHIBITION; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NONHUMAN; PLURIPOTENT STEM CELL; UPREGULATION;

ADENINE NUCLEOTIDES; ANIMALS; ANTIMYCIN A; CELL DIFFERENTIATION; CELL LINE; ELECTRON TRANSPORT COMPLEX III; EMBRYONIC STEM CELLS; ENZYME INHIBITORS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MITOCHONDRIA; NEURONS; PLURIPOTENT STEM CELLS; REACTIVE OXYGEN SPECIES;

EID: 84891590984     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082095     Document Type: Article

References (64)

1. Lonergan T, Bavister B, Brenner C (2007) Mitochondria in stem cells. Mitochondrion 7: 289-296. doi:10.1016/j.mito.2007.05.002. PubMed: 17588828.
2. Nesti C, Pasquali L, Vaglini F, Siciliano G, Murri L (2007) The role of mitochondria in stem cell biology. Biosci Rep 27: 165-171. doi:10.1007/s10540- 007-9044-1. PubMed: 17484045.
3. Parker GC, Acsadi G, Brenner CA (2009) Mitochondria: determinants of stem cell fate? Stem Cells Dev 18: 803-806. doi:10.1089/scd.2009.1806.edi. PubMed: 19563264.
4. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP et al. (2009) Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15: 553-572. doi:10.1093/humupd/ dmp016. PubMed: 19414527.
5. Schieke SM, Ma M, Cao L, McCoy JP, Liu C et al. (2008) Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells. J Biol Chem 283: 28506-28512. doi:10.1074/jbc.M802763200. PubMed: 18713735.
6. Folmes CD, Nelson TJ, Terzic A (2011) Energy metabolism in nuclear reprogramming. Biomark Med 5: 715-729. doi:10.2217/bmm.11.87. PubMed: 22103608.
7. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147. doi:10.1126/science.282.5391.1145. PubMed: 9804556.
8. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156. doi:10.1038/292154a0. PubMed: 7242681.
9. Fischer B, Bavister BD (1993) Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99: 673-679. doi:10.1530/jrf.0.0990673. PubMed: 8107053.
10. Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102: 4783-4788. doi:10.1073/pnas.0501283102. PubMed: 15772165.
11. Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M et al. (2007) A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9: 293-299. doi:10.1089/ars.2006.1467. PubMed: 17184172.
12. Kondoh H, Lleonart ME, Gil J, Wang J, Degan P et al. (2005) Glycolytic enzymes can modulate cellular life span. Cancer Res 65: 177-185. PubMed: 15665293.
13. Armstrong L, Tilgner K, Saretzki G, Atkinson SP, Stojkovic M et al. (2010) Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells 28: 661-673. doi:10.1002/stem.307. PubMed: 20073085.
14. Prigione A, Adjaye J (2010) Modulation of mitochondrial biogenesis and bioenergetic metabolism upon in vitro and in vivo differentiation of human ES and iPS cells. Int J Dev Biol 54: 1729-1741. doi:10.1387/ijdb.103198ap. PubMed: 21305470.
15. Suhr ST, Chang EA, Tjong J, Alcasid N, Perkins GA et al. (2010) Mitochondrial rejuvenation after induced pluripotency. PLOS ONE 5: e14095. doi:10.1371/journal.pone.0014095. PubMed: 21124794.
16. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA et al. (2011) Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLOS ONE 6: e20914. doi:10.1371/journal.pone.0020914. PubMed: 21698063.
17. Folmes CD, Nelson TJ, Martinez-Fernandez A, Arrell DK, Lindor JZ et al. (2011) Somatic oxidative bioenergetics transitions into pluripotency-dependent glycolysis to facilitate nuclear reprogramming. Cell Metab 14: 264-271. doi:10.1016/j.cmet.2011.06.011. PubMed: 21803296.
18. Yoshida Y, Takahashi K, Okita K, Ichisaka T, Yamanaka S (2009) Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell 5: 237-241. doi:10.1016/j.stem.2009.08.001. PubMed: 19716359.
19. Warburg O (1956) On the origin of cancer cells. Science 123: 309-314. doi:10.1126/science.123.3191.309. PubMed: 13298683.
20. Chen CT, Hsu SH, Wei YH (2010) Upregulation of mitochondrial function and antioxidant defense in the differentiation of stem cells. Biochim Biophys Acta 1800: 257-263. doi:10.1016/j.bbagen.2009.09.001. PubMed: 19747960.
21. Feron O (2009) Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol 92: 329-333. doi:10.1016/j.radonc.2009.06.025. PubMed: 19604589.
22. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033. doi:10.1126/science.1160809. PubMed: 19460998.
23. Lonergan T, Brenner C, Bavister B (2006) Differentiation-related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol 208: 149-153. doi:10.1002/jcp.20641. PubMed: 16575916.
24. St John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY et al. (2005) The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7: 141-153. doi:10.1089/clo.2005.7.141. PubMed: 16176124.
25. Cho YM, Kwon S, Pak YK, Seol HW, Choi YM et al. (2006) Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 348: 1472-1478. doi:10.1016/j.bbrc.2006.08.020. PubMed: 16920071.
26. Chung S, Arrell DK, Faustino RS, Terzic A, Dzeja PP (2010) Glycolytic network restructuring integral to the energetics of embryonic stem cell cardiac differentiation. J Mol Cell Cardiol 48: 725-734. doi:10.1016/j.yjmcc.2009.12. 014. PubMed: 20045004.
27. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A et al. (2007) Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 4 Suppl 1: S60-S67. doi:10.1038/ncpcardio0775. PubMed: 17230217.
28. Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC (2007) Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 120: 4025-4034. doi:10.1242/jcs.016972. PubMed: 17971411.
29. Spitkovsky D, Sasse P, Kolossov E, Böttinger C, Fleischmann BK et al. (2004) Activity of complex III of the mitochondrial electron transport chain is essential for early heart muscle cell differentiation. FASEB J 18: 1300-1302. PubMed: 15180963.
30. Birket MJ, Orr AL, Gerencser AA, Madden DT, Vitelli C et al. (2011) A reduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. J Cell Sci 124: 348-358. doi:10.1242/jcs.072272. PubMed: 21242311.
31. Kirby DM, Rennie KJ, Smulders-Srinivasan TK, Acin-Perez R, Whittington M et al. (2009) Transmitochondrial embryonic stem cells containing pathogenic mtDNA mutations are compromised in neuronal differentiation. Cell Prolif 42: 413-424. doi:10.1111/j.1365-2184.2009.00612.x. PubMed: 19552636.
32. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U (2011) Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 29: 486-495. doi:10.1002/stem.590. PubMed: 21425411.
33. Varum S, Momcilović; O, Castro C, Ben-Yehudah A, Ramalho-Santos J et al. (2009) Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem. Cell Res 3: 142-156.
34. Vayssière JL, Cordeau-Lossouarn L, Larcher JC, Basseville M, Gros F et al. (1992) Participation of the mitochondrial genome in the differentiation of neuroblastoma cells. In Vitro Cell Dev Biol 28A: 763-772. PubMed: 1483966.
35. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE (2009) Mitochondria and reactive oxygen species. Free Radic Biol Med 47: 333-343. doi:10.1016/j.freeradbiomed.2009.05.004. PubMed: 19427899.
36. Hooper M, Hardy K, Handyside A, Hunter S, Monk M (1987) HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 326: 292-295. doi:10.1038/326292a0. PubMed: 3821905.
37. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 90: 8424-8428. doi:10.1073/pnas.90.18.8424. PubMed: 8378314.
38. Barberi T, Klivenyi P, Calingasan NY, Lee H, Kawamata H et al. (2003) Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 21: 1200-1207. doi:10.1038/nbt870. PubMed: 14502203.
39. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y et al. (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28: 31-40. doi:10.1016/S0896-6273(00)00083-0. PubMed: 11086981.
40. Cajánek L, Ribeiro D, Liste I, Parish CL, Bryja V et al. (2009) Wnt/beta-catenin signaling blockade promotes neuronal induction and dopaminergic differentiation in embryonic stem cells. Stem Cells 27: 2917-2927. PubMed: 19725118.
41. Ying QL, Stavridis M, Griffiths D, Li M, Smith A (2003) Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21: 183-186. doi:10.1038/nbt780. PubMed: 12524553.
42. Parnas D, Linial M (1998) Highly sensitive ELISA-based assay for quantifying protein levels in neuronal cultures. Brain Res Brain Res Protoc 2: 333-338
43. Branco AF, Pereira SL, Moreira AC, Holy J, Sardão VA et al. (2011) Isoproterenol cytotoxicity is dependent on the differentiation state of the cardiomyoblast H9c2 cell line. Cardiovasc Toxicol 11: 191-203. doi:10.1007/s12012-011-9111-5. PubMed: 21455642.
44. Amaral S, Moreno AJ, Santos MS, Seiça R, Ramalho-Santos J (2006) Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes. Theriogenology 66: 2056-2067. doi:10.1016/j.theriogenology.2006.06.006. PubMed: 16860381.
45. Burgess A, Vigneron S, Brioudes E, Labbé JC, Lorca T et al. (2010) Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc Natl Acad Sci U S A 107: 12564-12569. doi:10.1073/pnas.0914191107. PubMed: 20538976.
46. Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91: 807-819. doi:10.1113/expphysiol.2006.033506. PubMed: 16857720.
47. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA et al. (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275: 25130-25138. doi:10.1074/jbc.M001914200. PubMed: 10833514.
48. Correia SC, Santos RX, Cardoso SM, Santos MS, Oliveira CR et al. (2012) Cyanide preconditioning protects brain endothelial and NT2 neuron-like cells against glucotoxicity: role of mitochondrial reactive oxygen species and HIF-1α. Neurobiol Dis 45: 206-218. doi:10.1016/j.nbd.2011.08.005. PubMed: 21854848.
49. Chen CT, Hsu SH, Wei YH (2012) Mitochondrial bioenergetic function and metabolic plasticity in stem cell differentiation and cellular reprogramming. Biochim Biophys Acta 1820: 571-576. doi:10.1016/j.bbagen.2011.09.013. PubMed: 21983491.
50. Papa S, Petruzzella V, Scacco S, Vergari R, Panelli D et al. (2004) Respiratory complex I in brain development and genetic disease. Neurochem Res 29: 547-560. doi:10.1023/B:NERE.0000014825.42365.16. PubMed: 15038602.
51. Candelario KM, Shuttleworth CW, Cunningham LA (2013) Neural stem/progenitor cells display a low requirement for oxidative metabolism independent of hypoxia inducible factor-1alpha expression. J Neurochem 125: 420-429. doi:10.1111/jnc.12204. PubMed: 23410250.
52. Han YH, Kim SH, Kim SZ, Park WH (2008) Antimycin A as a mitochondria damage agent induces an S phase arrest of the cell cycle in HeLa cells. Life Sci 83: 346-355. doi:10.1016/j.lfs.2008.06.023. PubMed: 18655793.
53. Han YH, Kim SH, Kim SZ, Park WH (2008) Antimycin A as a mitochondrial electron transport inhibitor prevents the growth of human lung cancer A549 cells. Oncol Rep 20: 689-693. PubMed: 18695925.
54. Han YH, Park WH (2009) Growth inhibition in antimycin A treated-lung cancer Calu-6 cells via inducing a G1 phase arrest and apoptosis. Lung Cancer 65: 150-160. doi:10.1016/j.lungcan.2008.11.005. PubMed: 19111365.
55. Ataullakhanov FI, Vitvitsky VM (2002) What determines the intracellular ATP concentration. Biosci Rep 22: 501-511. doi:10.1023/A:1022069718709. PubMed: 12635847.
56. Steinberg GR, Kemp BE (2009) AMPK in Health and Disease. Physiol Rev 89: 1025-1078. doi:10.1152/physrev.00011.2008. PubMed: 19584320.
57. Byun HO, Kim HY, Lim JJ, Seo YH, Yoon G (2008) Mitochondrial dysfunction by complex II inhibition delays overall cell cycle progression via reactive oxygen species production. J Cell Biochem 104: 1747-1759. doi:10.1002/jcb.21741. PubMed: 18395845.
58. Evans DR, Guy HI (2004) Mammalian pyrimidine biosynthesis: fresh insights into an ancient pathway. J Biol Chem 279: 33035-33038. doi:10.1074/jbc. R400007200. PubMed: 15096496.
59. Carrière A, Carmona MC, Fernandez Y, Rigoulet M, Wenger RH et al. (2004) Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. J Biol Chem 279: 40462-40469. doi:10.1074/jbc.M407258200. PubMed: 15265861.
60. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH (2008) Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26: 960-968. doi:10.1634/stemcells.2007-0509. PubMed: 18218821.
61. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC et al. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95: 11715-11720. doi:10.1073/pnas.95.20.11715. PubMed: 9751731.
62. Semenza GL (2010) HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20: 51-56. doi:10.1016/j.gde.2009.10.009. PubMed: 19942427.
63. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM et al. (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20: 557-570. doi:10.1101/gad.1399906. PubMed: 16510872.
64. Mathieu J, Zhang Z, Nelson A, Lamba DA, Reh TA et al. (2013) Hypoxia Induces Re-Entry of Committed Cells into Pluripotency. Stem Cells, 31: 1737-48. PubMed: 23765801.