Development to term of cloned cattle derived from donor cells treated with valproic acid

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Sangalli, Juliano Rodrigues ^a,b   Chiaratti, Marcos Roberto ^a,c   De Bem, Tiago Henrique Camara ^a   De Araújo, Reno Roldi ^a   Bressan, Fabiana Fernandes ^a   Sampaio, Rafael Vilar ^a,b   Perecin, Felipe ^a   Smith, Lawrence Charles ^d   King, Willian Allan ^b   Meirelles, Flávio Vieira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF GUELPH   (Canada)

^c FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; OCTAMER TRANSCRIPTION FACTOR 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SOMATOMEDIN B RECEPTOR; VALPROIC ACID; HISTONE; HISTONE DEACETYLASE INHIBITOR;

ACTB GENE; ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BOS INDICUS; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; DONOR; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GENE SEQUENCE; GESTATION PERIOD; HISTONE ACETYLATION; IGF2R GENE; MOLECULAR CLONING; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; POSTIMPLANTATION EMBRYO; POU5F1 GENE; PPARGC1A GENE; PREIMPLANTATION EMBRYO; PROCEDURES CONCERNING CELLS; SOMATIC CELL NUCLEAR TRANSFER; UPREGULATION; ACETYLATION; ANIMAL; BOVINE; CELL DIFFERENTIATION; CELL NUCLEUS TRANSPLANTATION; CELL PROLIFERATION; CLONING; DRUG EFFECTS; GENETICS; METABOLISM; PROCEDURES;

ACETYLATION; ANIMALS; CATTLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONING, ORGANISM; DNA METHYLATION; EMBRYONIC DEVELOPMENT; HISTONE DEACETYLASE INHIBITORS; HISTONES; NUCLEAR TRANSFER TECHNIQUES; OCTAMER TRANSCRIPTION FACTOR-3; RECEPTOR, IGF TYPE 2; VALPROIC ACID;

EID: 84903648305     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101022     Document Type: Article

References (76)

1. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385: 810-813. (Pubitemid 27106068)
2. Wilmut I, Beaujean N, de Sousa PA, Dinnyes A, King TJ, et al. (2002) Somatic cell nuclear transfer. Nature 419: 583-586.
3. Meirelles F V, Birgel EH, Perecin F, Bertolini M, Traldi AS, et al. (2010) Delivery of cloned offspring: experience in Zebu cattle (Bos indicus). Reprod Fertil Dev 22: 88-97.
4. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, et al. (2003) Epigenetic marking correlates with developmental potential in cloned preimplantation embryos. Curr Biol 13: 1116-1121. (Pubitemid 36815259)
5. Wee G, Koo DB, Song BS, Kim JS, Kang MJ, et al. (2006) Inheritable histone H4 acetylation of somatic chromatins in cloned embryos. J Biol Chem 281: 6048-6057. (Pubitemid 43847706)
6. Suzuki J, Therrien J, Filion F, Lefebvre R, Goff AK, et al. (2011) Loss of methylation at H19 DMD is associated with biallelic expression and reduced development in cattle derived by somatic cell nuclear transfer. Biol Reprod 84: 947-956.
7. Arnold DR, Fortier AL, Lefebvre R, Miglino MA, Pfarrer C, et al. (2008) Placental insufficiencies in cloned animals - a workshop report. Placenta 29 Suppl A: S108-10.
8. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, et al. (2001) Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos. Proc Natl Acad Sci U S A 24: 13734-13738. (Pubitemid 33115967)
9. Pasque V, Jullien J, Miyamoto K, Halley-Stott RP, Gurdon JB (2011) Epigenetic factors influencing resistance to nuclear reprogramming. Trends Genet 27: 516-525.
10. Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M (2011) Open chromatin in pluripotency and reprogramming. Nat Rev Mol Cell Biol 12: 36-47.
11. Gurdon JB, Wilmut I (2011) Nuclear transfer to eggs and oocytes. Cold Spring Harb Perspect Biol 3 (6).
12. Zhao J, Hao Y, Ross JW, Spate LD, Walters EM, et al. (2010) Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram 12: 75-83.
13. Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan N Van, et al. (2006) Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun 340: 183-189. (Pubitemid 41827663)
14. Costa-borges N, Santaló J, Ibáñes E. (2010) Comparison between the effects of valproic acid and trichostatin A on the in vitro development, blastocyst quality, and full-term development of mouse somatic cell nuclear transfer embryos. Cell Reprogram 12: 437-446.
15. Shi W, Hoeflich A, Flaswinkel H, Stojkovic M, Wolf E, et al. (2003) Induction of a senescent-like phenotype does not confer the ability of bovine immortal cells to support the development of nuclear transfer embryos. Biol Reprod 69: 301-309. (Pubitemid 36806836)
16. Lee MJ, Kim SW, Lee HG, Im GS, Yang BC, et al. (2011) Trichostatin A promotes the development of bovine somatic cell nuclear transfer embryos. J Reprod Dev 57: 34-42.
17. Zhao J, Ross JW, Hao Y, Spate LD, Walters EM, et al. (2009) Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer. Biol Reprod 81: 525-530.
18. Yang F, Hao R, Kessler B, Brem G, Wolf E, et al. (2007) Rabbit somatic cell cloning: effects of donor cell type, histone acetylation status and chimeric embryo complementation. Reproduction 133: 219-230. (Pubitemid 46335540)
19. Enright BP, Kubota C, Yang X, Tian XC (2003) Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2′-deoxycytidine. Biol Reprod 69: 896-901. (Pubitemid 37064618)
20. Miyoshi K, Mori H, Mizobe Y, Akasaka E, Osawa A, et al. (2010) Valproic acid enhances in vitro development and OCT-3/4 expression of miniature pig somatic cell nuclear transfer embryos. Cell Reprogram 12: 67-74.
21. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, et al. (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26: 795-797. (Pubitemid 351961456)
22. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar M a, et al. (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741.
23. Göttlicher M, Minucci S, Zhu P, Krämer OH, Schimpf A, et al. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20: 6969-6978. (Pubitemid 34062289)
24. Marchion DC, Bicaku E, Daud AI, Sullivan DM, Munster PN (2005) Valproic acid alters chromatin structure by regulation of chromatin modulation proteins. Cancer Res 65: 3815-3822. (Pubitemid 40616361)
25. Hezroni H, Sailaja BS, Meshorer E (2011) Pluripotency-related, valproic acid (VPA)-induced genome-wide histone H3 lysine 9 (H3K9) acetylation patterns in embryonic stem cells. J Biol Chem 286: 35977-35988.
26. Turner BM (2007) Defining an epigenetic code. Nat Cell Biol 9: 2-6.
27. Xu W, Wang Y, Li Y, Wang L, Xiong X, et al. (2012) Valproic acid improves the in vitro development competence of bovine somatic cell nuclear transfer embryos. Cell Reprogram 14: 138-145.
28. Selokar NL, St John L, Revay T, King WA, Singla SK, et al. (2013) Effect of histone deacetylase inhibitor valproic acid treatment on donor cell growth characteristics, cell cycle arrest, apoptosis, and handmade cloned bovine embryo production efficiency. Cell Reprogram 15: 531-542.
29. Sangalli JR, De Bem THC, Perecin F, Chiaratti MR, Oliveira LDJ, et al. (2012) Treatment of nuclear-donor cells or cloned zygotes with chromatin-modifying agents increases histone acetylation but does not improve full-term development of cloned cattle. Cell Reprogram 14: 235-247.
30. Mosmann T (1983) Rapid Colorimetric Assay for Cellular Growth and Survival: Application to Proliferation and Cytotoxicity Assays. J Immunol Methods 65: 55-63.
31. Nasser LF, Reis EL, Oliveira MA, Bó GA, Baruselli PS (2004) Comparison of four synchronization protocols for fixed-time bovine embryo transfer in Bos indicus x Bos taurus recipients. Theriogenology 62: 1577-1584. (Pubitemid 39415747)
32. Ding X, Wang Y, Zhang D, Guo Z, Zhang Y (2008) Increased pre-implantation development of cloned bovine embryos treated with 5-aza-2′-deoxycytidine and trichostatin A. Theriogenology 70: 622-630.
33. Giraldo AM, Lynn JW, Purpera MN, Godke RA (2007) DNA methylation and histone acetylation patterns in cultured bovine fibroblasts for nuclear transfer. Mol Reprod Dev 74: 1514-1524. (Pubitemid 350058417)
34. Martinez-Diaz MA, Che L, Albornoz M, Seneda MM, Collis D, et al. (2010) Pre- and postimplantation development of swine-cloned embryos derived from fibroblasts and bone marrow cells after inhibition of histone deacetylases. Cell Reprogram 12: 85-94.
35. Ramakers C, Ruijter JM, Deprez RHL, Moorman AF. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66. (Pubitemid 36263221)
36. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
37. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
38. Detich N, Bovenzi V, Szyf M (2003) Valproate induces replication- independent active DNA demethylation. J Biol Chem 278: 27586-27592. (Pubitemid 36899944)
39. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, et al. (2001) Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 27: 153-154. (Pubitemid 32157439)
40. Boiani M, Eckardt S, Schöler HR, McLaughlin KJ (2002) Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev 16: 1209-1219.
41. Austin S, St-Pierre J (2012) PGC1α and mitochondrial metabolism-emerging concepts and relevance in ageing and neurodegenerative disorders. J Cell Sci 125: 4963-4971.
42. Gurdon JB, Melton DA (2008) Nuclear reprogramming in cells. Science 322: 1811-1815.
43. Yang X, Smith SL, Tian XC, Lewin HA, Renard JP, et al. (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39: 295-302. (Pubitemid 46328492)
44. Enright BP, Sung LY, Chang CC, Yang X, Tian XC (2005) Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2′-deoxycytidine. Biol Reprod 72: 944-948. (Pubitemid 40404270)
45. Das ZC, Gupta MK, Uhm SJ, Lee HT (2010) Increasing histone acetylation of cloned embryos, but not donor cells, by sodium butyrate improves their in vitro development in pigs. Cell Reprogram 12: 95-104.
46. Campbell KH (1999) Nuclear equivalence, nuclear transfer, and the cell cycle. Cloning 1: 3-15.
47. Miranda MDS, Bressan FF, Zecchin KG, Vercesi AE, Mesquita LG, et al. (2009) Serum-starved apoptotic fibroblasts reduce blastocyst production but enable development to term after SCNT in cattle. Cloning Stem Cells 11: 565-573.
48. Zhao S, Xu W, Jiang W, Yu W, Lin Y, et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327: 1000-1004.
49. Chiang MC, Cheng YC, Lin KH, Yen CH (2013) PPARγ regulates the mitochondrial dysfunction in human neural stem cells with tumor necrosis factor alpha. Neuroscience 229: 118-129.
50. Aouali N, Palissot V, El-Khoury V, Moussay E, Janji B, et al. (2009) Peroxisome proliferator-activated receptor gamma agonists potentiate the cytotoxic effect of valproic acid in multiple myeloma cells. Br J Haematol 147: 662-671.
51. VerMilyea MD, O'Neill LP, Turner BM (2009) Transcription-independent heritability of induced histone modifications in the mouse preimplantation embryo. PLoS One 4: e6086.
52. Jullien J, Pasque V, Halley-Stott RP, Miyamoto K, Gurdon JB (2011) Mechanisms of nuclear reprogramming by eggs and oocytes: a deterministic process? Nat Rev Mol Cell Biol 12: 453-459.
53. Gao T, Zheng J, Xing F, Fang H, Sun F, et al. (2007) Nuclear reprogramming: the strategy used in normal development is also used in somatic cell nuclear transfer and parthenogenesis. Cell Res 17: 135-150. (Pubitemid 46279236)
54. Felisbino MB, Tamashiro WMSC, Mello MLS (2011) Chromatin remodeling, cell proliferation and cell death in valproic acid-treated HeLa cells. PLoS One 6: e29144.
55. Bortvin A, Eggan K, Skaletsky H, Akutsu H, Berry DL, et al. (2003) Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130: 1673-1680. (Pubitemid 36527525)
56. Smith LC, Suzuki J, Goff AK, Filion F, Therrien J, et al. (2012) Developmental and epigenetic anomalies in cloned cattle. Reprod Domest Anim 47 Suppl 4: 107-114.
57. Teng HF, Kuo YL, Loo MR, Li CL, Chu TW, et al. (2010) Valproic acid enhances Oct4 promoter activity in myogenic cells. J Cell Biochem 110: 995-1004.
58. Simonsson S, Gurdon J (2004) DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol 6: 984-990. (Pubitemid 39359851)
59. Ludwig T, Eggenschwiler J, Fisher P, D'Ercole a J, Davenport ML, et al. (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 177: 517-535. (Pubitemid 26275902)
60. Lau MM, Stewart CE, Liu Z, Bhatt H, Rotwein P, et al. (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8: 2953-2963.
61. Perecin F, Méo SC, Yamazaki W, Ferreira CR, Merighe GKF, et al. (2009) Imprinted gene expression in in vivo- and in vitro-produced bovine embryos and chorio-allantoic membranes. Genet Mol Res 8: 76-85.
62. Feil R, Khosla S, Cappai P, Loi P (1998) Genomic imprinting in ruminants: allele-specific gene expression in parthenogenetic sheep. Mamm Genome 9: 831-834. (Pubitemid 28440099)
63. Hagemann LJ, Peterson AJ, Weilert LL, Lee RS, Tervit HR (1998) In vitro and early in vivo development of sheep gynogenones and putative androgenones. Mol Reprod Dev 50: 154-162. (Pubitemid 28234563)
64. Young LE, Schnieke AE, McCreath KJ, Wieckowski S, Konfortova G, et al. (2003) Conservation of IGF2-H19 and IGF2R imprinting in sheep: effects of somatic cell nuclear transfer. Mech Dev 120: 1433-1442. (Pubitemid 37488032)
65. Baqir S, Smith LC (2006) Inhibitors of histone deacetylases and DNA methyltransferases alter imprinted gene regulation in embryonic stem cells. Cloning Stem Cells 8: 200-213. (Pubitemid 44735174)
66. Hu JF, Pham J, Dey I, Li T, Vu TH, et al.(2000) Allele-Specific histone acetylation accompanies genomic imprinting of the insulin-like growth factor II receptor gene. 141: 4428-4435.
67. Ono T, Li C, Mizutani E, Terashita Y, Yamagata K, et al. (2010) Inhibition of class IIb histone deacetylase significantly improves cloning efficiency in mice. Biol Reprod 83: 929-937.
68. Xu W, Wang Y, Li Y, Wang L, Xiong X, et al. (2012) Valproic acid improves the in vitro development competence of bovine somatic cell nuclear transfer embryos. Cell Reprogram 14: 138-145.
69. Kim YJ, Ahn KS, Kim M, Shim H (2011) Comparison of potency between histone deacetylase inhibitors trichostatin A and valproic acid on enhancing in vitro development of porcine somatic cell nuclear transfer embryos. In Vitro Cell Dev Biol Anim 47: 283-289.
70. Akagi S, Geshi M, Nagai T (2013) Recent progress in bovine somatic cell nuclear transfer. Anim Sci J 84: 191-199.
71. Chavatte-Palmer P, Camous S, Jammes H, Le Cleac'h N,GuillomotM, et al. (2012) Review: Placental perturbations induce the developmental abnormalities often observed in bovine somatic cell nuclear transfer. Placenta 33 Suppl: S99-S104.
72. Hill JR, Burghardt RC, Jones K, Long CR, Looney CR, et al. (2000) Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol Reprod 63: 1787-1794.
73. Kang JD, Li S, Lu Y, Wang W, Liang S, et al. (2013) Valproic acid improved in vitro development of pig cloning embryos but did not improve survival of cloned pigs to adulthood. Theriogenology 79: 306-11.
74. Johnson AK, Clark-Price SC, Choi YH, Hartaman DL, Hinrichs K, (2010) Physical and clinicopathologic findings in foals derived by use of somatic cell nuclear transfer: 14 cases (2004-2008). J Am Med Vet Assoc 236: 983-990.
75. Ogura A, Inoue K, Wakayama T (2013) Recent advancements in cloning by somatic cell nuclear transfer. Philos Trans R Soc Lond B Biol Sci 368: 20110329.
76. Galli C, Duchi R, Colleoni S, Lagutina I, Lazzari G (2014) Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81: 138-151.