Nuclear reprogramming: Kinetics of cell cycle and metabolic progression as determinants of success

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Balbach, Sebastian Thomas ^a   Esteves, Telma Cristina ^a   Houghton, Franchesca Dawn ^b   Siatkowski, Marcin ^c,d   Pfeiffer, Martin Johannes ^a   Tsurumi, Chizuko ^e   Kanzler, Benoit ^f   Fuellen, Georg ^d   Boiani, Michele ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d UNIVERSITY OF ROSTOCK   (Germany)

^e UNIVERSITY OF FREIBURG   (Germany)

^f MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GREEN FLUORESCENT PROTEIN; HISTONE H2B; MOLECULAR MARKER;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL ACTIVATION; CELL COUNT; CELL CYCLE ARREST; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL KINETICS; CELL METABOLISM; CELL NUCLEUS TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYO TRANSFER; EMBRYONIC STEM CELL; FEMALE; FLUORESCENCE IMAGING; GENE EXPRESSION REGULATION; INTRACYTOPLASMIC SPERM INJECTION; MITOSIS; MOLECULAR CLONING; MORULA; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PREIMPLANTATION EMBRYO; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SOMATIC CELL;

AMINO ACIDS; ANIMALS; ARGININE; BLASTOCYST; CELL CYCLE; CLUSTER ANALYSIS; DNA DAMAGE; EMBRYO TRANSFER; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KINETICS; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; NUCLEAR REPROGRAMMING; NUCLEAR TRANSFER TECHNIQUES; TIME-LAPSE IMAGING; TRANSGENES;

EID: 84859941748     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035322     Document Type: Article

References (76)

1. Cavaleri FM, Balbach ST, Gentile L, Jauch A, Böhm-Steuer B, et al. (2008) Subsets of cloned mouse embryos and their non-random relationship to development and nuclear reprogramming. Mech Dev 125: 153-166.
2. Wakayama S, Jakt ML, Suzuki M, Araki R, Hikichi T, et al. (2006) Equivalency of nuclear transfer-derived embryonic stem cells to those derived from fertilized mouse blastocysts. Stem Cells 24: 2023-2033.
3. Brambrink T, Hochedlinger K, Bell G, Jaenisch R, (2006) ES cells derived from cloned and fertilized blastocysts are transcriptionally and functionally indistinguishable. Proc Natl Acad Sci U S A 103: 933-938.
4. Ding J, Guo Y, Liu S, Yan Y, Chang G, et al. (2009) Embryonic stem cells derived from somatic cloned and fertilized blastocysts are post-transcriptionally indistinguishable: a MicroRNA and protein profile comparison. Proteomics 9: 2711-2721.
5. Boiani M, Eckardt S, Leu NA, Schöler HR, McLaughlin KJ, (2003) Pluripotency deficit in clones overcome by clone-clone aggregation: epigenetic complementation? EMBO J 22: 5304-5312.
6. Loi P, Beaujean N, Khochbin S, Fulka J Jr, Ptak G, (2008) Asymmetric nuclear reprogramming in somatic cell nuclear transfer? BioEssays: news and reviews in molecular, cellular and developmental biology 30: 66-74.
7. Vassena R, Han Z, Gao S, Latham KE, (2007) Deficiency in recapitulation of stage-specific embryonic gene transcription in two-cell stage cloned mouse embryos. Molecular Reproduction and Development 74: 1548-1556.
8. Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, et al. (2009) Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462: 595-601.
9. Day ML, Winston N, McConnell JL, Cook D, Johnson MH, (2001) tiK+ toK+: an embryonic clock? Reprod Fertil Dev 13: 69-79.
10. Goval JJ, Alexandre H, (2000) Effect of genistein on the temporal coordination of cleavage and compaction in mouse preimplantation embryos. Eur J Morphol 38: 88-96.
11. Zuccotti M, Boiani M, Ponce R, Guizzardi S, Scandroglio R, et al. (2002) Mouse Xist expression begins at zygotic genome activation and is timed by a zygotic clock. Mol Reprod Dev 61: 14-20.
12. Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL, et al. (2006) Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J Cell Physiol 209: 883-893.
13. Li CB, Wang ZD, Zheng Z, Hu LL, Zhong SQ, et al. (2011) Number of blastomeres and distribution of microvilli in cloned mouse embryos during compaction. Zygote 19: 271-276.
14. Yamagata K, Suetsugu R, Wakayama T, (2009) Long-term, six-dimensional live-cell imaging for the mouse preimplantation embryo that does not affect full-term development. J Reprod Dev 55: 343-350.
15. Wong CC, Loewke KE, Bossert NL, Behr B, De Jonge CJ, et al. (2010) Non-invasive imaging of human embryos before embryonic genome activation predicts development to the blastocyst stage. Nat Biotechnol 28: 1115-1121.
16. Kubiak JZ, Ciemerych MA, (2001) Cell cycle regulation in early mouse embryos. Novartis Found Symp 237: 79-89; discussion 89-99.
17. Boiani M, Gambles V, Schöler HR, (2004) ATP levels in clone mouse embryos. Cytogenetic and Genome Research 105: 270-278.
18. Boiani M, Gentile L, Gambles VV, Cavaleri F, Redi CA, et al. (2005) Variable reprogramming of the pluripotent stem cell marker Oct4 in mouse clones: distinct developmental potentials in different culture environments. Stem Cells 23: 1089-1104.
19. Gao S, Chung YG, Williams JW, Riley J, Moley K, et al. (2003) Somatic cell-like features of cloned mouse embryos prepared with cultured myoblast nuclei. Biol Reprod 69: 48-56.
20. Lane M, Gardner DK, (1998) Amino acids and vitamins prevent culture-induced metabolic perturbations and associated loss of viability of mouse blastocysts. Hum Reprod 13: 991-997.
21. Sturmey RG, Brison DR, Leese HJ, (2008) Symposium: innovative techniques in human embryo viability assessment. Assessing embryo viability by measurement of amino acid turnover. Reprod Biomed Online 17: 486-496.
22. Brison DR, Houghton FD, Falconer D, Roberts SA, Hawkhead J, et al. (2004) Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum Reprod 19: 2319-2324.
23. Stokes PJ, Hawkhead JA, Fawthrop RK, Picton HM, Sharma V, et al. (2007) Metabolism of human embryos following cryopreservation: implications for the safety and selection of embryos for transfer in clinical IVF. Hum Reprod 22: 829-835.
24. Bowman P, McLaren A, (1970) Cleavage rate of mouse embryos in vivo and in vitro. J Embryol Exp Morphol 24: 203-207.
25. Harlow GM, Quinn P, (1982) Development of preimplantation mouse embryos in vivo and in vitro. Aust J Biol Sci 35: 187-193.
26. Streffer C, van Beuningen D, Molls M, Zamboglou N, Schulz S, (1980) Kinetics of cell proliferation in the pre-implanted mouse embryo in vivo and in vitro. Cell Tissue Kinet 13: 135-143.
27. Schultz RM, (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8: 323-331.
28. Falco G, Lee SL, Stanghellini I, Bassey UC, Hamatani T, et al. (2007) Zscan4: a novel gene expressed exclusively in late 2-cell embryos and embryonic stem cells. Dev Biol 307: 539-550.
29. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, et al. (2006) Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 20: 1744-1754.
30. Wang Q, Latham KE, (1997) Requirement for protein synthesis during embryonic genome activation in mice. Mol Reprod Dev 47: 265-270.
31. Gates AH, (2008) Rate of ovular development as a factor in embryonic survival. In: Wolstenholme GEW, O'Connor M, editors. Ciba Foundation Symposium - Preimplantation stages of pregnancy John Wiley & Sons, Ltd pp. 270-293.
32. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ, (2002) The human and mouse replication-dependent histone genes. Genomics 80: 487-498.
33. Wang J, Han X, Saha S, Xu T, Rai R, et al. (2011) Arginyltransferase is an ATP-independent self-regulating enzyme that forms distinct functional complexes in vivo. Chem Biol 18: 121-130.
34. Varshavsky A, (2011) The N-end rule pathway and regulation by proteolysis. Protein Sci.
35. Zeng F, Baldwin DA, Schultz RM, (2004) Transcript profiling during preimplantation mouse development. Dev Biol 272: 483-496.
36. Hamatani T, Carter MG, Sharov AA, Ko MS, (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6: 117-131.
37. Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, et al. (2004) A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 6: 133-144.
38. Blake JA, Bult CJ, Kadin JA, Richardson JE, Eppig JT, (2011) The Mouse Genome Database (MGD): premier model organism resource for mammalian genomics and genetics. Nucleic Acids Res 39: D842-848.
39. Rowley R, Hudson J, Young PG, (1992) The wee1 protein kinase is required for radiation-induced mitotic delay. Nature 356: 353-355.
40. Balbach ST, Jauch A, Böhm-Steuer B, Cavaleri FM, Han YM, et al. (2007) Chromosome stability differs in cloned mouse embryos and derivative ES cells. Dev Biol 308: 309-321.
41. Yu Y, Ding C, Wang E, Chen X, Li X, et al. (2007) Piezo-assisted nuclear transfer affects cloning efficiency and may cause apoptosis. Reproduction 133: 947-954.
42. Wossidlo M, Arand J, Sebastiano V, Lepikhov K, Boiani M, et al. (2010) Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J 29: 1877-1888.
43. Kawasumi M, Anzai M, Takehara T, Mitani T, Kato H, et al. (2007) Abnormal distribution of chromosomes in the first division of nuclear transferred mouse embryos. J Reprod Dev 53: 615-622.
44. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, et al. (2004) Cell death by mitotic catastrophe: a molecular definition. Oncogene 23: 2825-2837.
45. Kalousek DK, Dill FJ, (1983) Chromosomal mosaicism confined to the placenta in human conceptions. Science 221: 665-667.
46. Lightfoot DA, Kouznetsova A, Mahdy E, Wilbertz J, Hoog C, (2006) The fate of mosaic aneuploid embryos during mouse development. Dev Biol 289: 384-394.
47. Munne S, Velilla E, Colls P, Garcia Bermudez M, Vemuri MC, et al. (2005) Self-correction of chromosomally abnormal embryos in culture and implications for stem cell production. Fertil Steril 84: 1328-1334.
48. Boiani M, Eckardt S, Schöler HR, McLaughlin KJ, (2002) Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev 16: 1209-1219.
49. Houghton FD, Hawkhead JA, Humpherson PG, Hogg JE, Balen AH, et al. (2002) Non-invasive amino acid turnover predicts human embryo developmental capacity. Hum Reprod 17: 999-1005.
50. Booth PJ, Humpherson PG, Watson TJ, Leese HJ, (2005) Amino acid depletion and appearance during porcine preimplantation embryo development in vitro. Reproduction 130: 655-668.
51. Houghton FD, (2006) Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74: 11-18.
52. Manser RC, Leese HJ, Houghton FD, (2004) Effect of inhibiting nitric oxide production on mouse preimplantation embryo development and metabolism. Biol Reprod 71: 528-533.
53. Chu L, Jiang Y, Hao H, Xia Y, Xu J, et al. (2008) Nitric oxide enhances Oct-4 expression in bone marrow stem cells and promotes endothelial differentiation. Eur J Pharmacol 591: 59-65.
54. Colussi C, Gurtner A, Rosati J, Illi B, Ragone G, et al. (2009) Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy. FASEB J 23: 2131-2141.
55. Maccarrone M, Bari M, Battista N, Di Rienzo M, Falciglia K, et al. (2001) Oxidation products of polyamines induce mitochondrial uncoupling and cytochrome c release. FEBS Lett 507: 30-34.
56. Lux GD, Marton LJ, Baylin SB, (1980) Ornithine decarboxylase is important in intestinal mucosal maturation and recovery from injury in rats. Science 210: 195-198.
57. Balbach ST, Esteves TC, Brink T, Gentile L, McLaughlin KJ, et al. (2010) Governing cell lineage formation in cloned mouse embryos. Dev Biol 343: 71-83.
58. Chirino-Galindo G, Baiza-Gutman LA, Barrera-Escorcia E, Palomar-Morales M, (2009) Polyamines protect rat embryo in vitro from high glucose-induced developmental delay and dysmorphogenesis. Birth Defects Res B Dev Reprod Toxicol 86: 58-64.
59. Kim JY, Burghardt RC, Wu G, Johnson GA, Spencer TE, et al. (2011) Select nutrients in the ovine uterine lumen. VIII. Arginine stimulates proliferation of ovine trophectoderm cells through MTOR-RPS6K-RPS6 signaling cascade and synthesis of nitric oxide and polyamines. Biol Reprod 84: 70-78.
60. Foster DA, Yellen P, Xu L, Saqcena M, (2010) Regulation of G1 Cell Cycle Progression: Distinguishing the Restriction Point from a Nutrient-Sensing Cell Growth Checkpoint(s). Genes Cancer 1: 1124-1131.
61. Pfeiffer MJ, Siatkowski M, Paudel Y, Balbach ST, Baeumer N, et al. (2011) Proteomic analysis of mouse oocytes reveals 28 candidate factors of the "reprogrammome". J Proteome Res 10: 2140-2153.
62. Singhal N, Graumann J, Wu G, Arauzo-Bravo MJ, Han DW, et al. (2010) Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141: 943-955.
63. Pfeiffer MJ, Balbach ST, Esteves TC, Crosetto N, Boiani M, (2010) Enhancing somatic nuclear reprogramming by Oct4 gain-of-function in cloned mouse embryos. Int J Dev Biol 54: 1649-1657.
64. Szabo PE, Hubner K, Scholer H, Mann JR, (2002) Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech Dev 115: 157-160.
65. Wang JP, Her WY, Meir YJ, Liu TS, Chang HL, et al. (1992) Seasonal variation in cell cycle during early development of the mouse embryo. J Reprod Fertil 94: 431-436.
66. Lemaire P, Garrett N, Gurdon JB, (1995) Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81: 85-94.
67. Esteves TC, Balbach ST, Pfeiffer MJ, Arauzo-Bravo MJ, Klein DC, et al. (2011) Somatic cell nuclear reprogramming of mouse oocytes endures beyond reproductive decline. Aging Cell 10: 80-95.
68. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
69. R Development Core Team (2011) R: A language and environment for statistical computing Vienna, Austria R Foundation for Statistical Computing.
70. Du P, Kibbe WA, Lin SM, (2008) lumi: a pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548.
71. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article 3.
72. Du P, Kibbe WA, Lin SM, (2007) nuID: a universal naming scheme of oligonucleotides for illumina, affymetrix, and other microarrays. Biol Direct 2: 16.
73. Davis S, Meltzer PS, (2007) GEOquery: a bridge between the Gene Expression Omnibus (GEO) and BioConductor. Bioinformatics 23: 1846-1847.
74. Gautier L, Cope L, Bolstad BM, Irizarry RA, (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
75. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M, (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18 (Suppl 1): S96-104.
76. Tay JI, Rutherford AJ, Killick SR, Maguiness SD, Partridge RJ, et al. (1997) Human tubal fluid: production, nutrient composition and response to adrenergic agents. Hum Reprod 12: 2451-2456.