Skip to main content

Role of Aberrant Protein Modification, Assembly, and Localization in Cloned Embryo Phenotypes

  • Chapter
  • First Online:
Posttranslational Protein Modifications in the Reproductive System

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 759))

Abstract

Aberrant post-translational modifications of proteins contribute markedly to the abnormal characteristics of cloned embryos. This review summarizes aberrant aspects of protein modifications and protein interactions, taking an inside–outside view to the cell. These aberrant aspects affect a range of processes including the control of chromatin structure, expression of pluripotency genes, propagation of epigenetic inheritance, protein trafficking, localization and signaling, cytoskeletal structure, mitosis, and correct localization of membrane proteins. By observing these aberrant features of cloned embryos, how they arise, and their impacts on development, it is possible to gain insight into normal development and identify novel strategies for enhancing cloning outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Kim YJ, Ahn KS, Kim M, Shim H. 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. 2011;47:283–9.

    Article  CAS  PubMed  Google Scholar 

  2. Kishigami S, Bui HT, Wakayama S, Tokunaga K, Van Thuan N, Hikichi T, Mizutani E, Ohta H, Suetsugu R, Sata T, Wakayama T. Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer. J Reprod Dev. 2007;53:165–70.

    Article  PubMed  Google Scholar 

  3. Van Thuan N, Bui HT, Kim JH, Hikichi T, Wakayama S, Kishigami S, Mizutani E, Wakayama T. The histone deacetylase inhibitor scriptaid enhances nascent mRNA production and rescues full-term development in cloned inbred mice. Reproduction. 2009;138:309–17.

    Article  PubMed  Google Scholar 

  4. Zhao J, Ross JW, Hao Y, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS. Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer. Biol Reprod. 2009;81: 525–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui HT, Wakayama T. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun. 2006;340:183–9.

    Article  CAS  PubMed  Google Scholar 

  6. Terashita Y, Wakayama S, Yamagata K, Li C, Sato E, Wakayama T. Latrunculin a can improve the birth rate of cloned mice and simplify the nuclear transfer protocol by gently inhibiting actin polymerization. Biol Reprod. 2012;86:180.

    Article  PubMed  Google Scholar 

  7. Zhao J, Hao Y, Ross JW, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS. Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram. 2010;12:75–83.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Martinez-Diaz MA, Che L, Albornoz M, Seneda MM, Collis D, Coutinho AR, El-Beirouthi N, Laurin D, Zhao X, Bordignon V. Pre- and postimplantation development of swine-cloned embryos derived from fibroblasts and bone marrow cells after inhibition of histone deacetylases. Cell Reprogram. 2010;12:85–94.

    Article  CAS  PubMed  Google Scholar 

  9. Costa-Borges N, Santalo J, Ibanez E. 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. 2010;12:437–46.

    Article  CAS  PubMed  Google Scholar 

  10. Shi LH, Miao YL, Ouyang YC, Huang JC, Lei ZL, Yang JW, Han ZM, Song XF, Sun QY, Chen DY. Trichostatin A (TSA) improves the development of rabbit–rabbit intraspecies cloned embryos, but not rabbit–human interspecies cloned embryos. Dev Dyn. 2008;237:640–8.

    Article  PubMed  Google Scholar 

  11. Huang Y, Tang X, Xie W, Zhou Y, Li D, Yao C, Zhou Y, Zhu J, Lai L, Ouyang H, Pang D. Histone deacetylase inhibitor significantly improved the cloning efficiency of porcine somatic cell nuclear transfer embryos. Cell Reprogram. 2011;13:513–20.

    Article  CAS  PubMed  Google Scholar 

  12. Su J, Wang Y, Li Y, Li R, Li Q, Wu Y, Quan F, Liu J, Guo Z, Zhang Y. Oxamflatin significantly improves nuclear reprogramming, blastocyst quality, and in vitro development of bovine SCNT embryos. PLoS One. 2011;6:e23805.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Dai X, Hao J, Hou XJ, Hai T, Fan Y, Yu Y, Jouneau A, Wang L, Zhou Q. Somatic nucleus reprogramming is significantly improved by m-carboxycinnamic acid bishydroxamide, a histone deacetylase inhibitor. J Biol Chem. 2010;285:31002–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Akagi S, Matsukawa K, Mizutani E, Fukunari K, Kaneda M, Watanabe S, Takahashi S. Treatment with a histone deacetylase inhibitor after nuclear transfer improves the preimplantation development of cloned bovine embryos. J Reprod Dev. 2011;57:120–6.

    Article  CAS  PubMed  Google Scholar 

  15. Lee MJ, Kim SW, Lee HG, Im GS, Yang BC, Kim NH, Kim DH. Trichostatin A promotes the development of bovine somatic cell nuclear transfer embryos. J Reprod Dev. 2011;57:34–42.

    Article  CAS  PubMed  Google Scholar 

  16. Sangalli JR, De Bem TH, Perecin F, Chiaratti MR, Oliveira Lde J, de Araujo RR, Valim Pimentel JR, Smith LC, Meirelles FV. 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. 2012;14:235–47.

    CAS  PubMed  Google Scholar 

  17. Sawai K, Fujii T, Hirayama H, Hashizume T, Minamihashi A. Epigenetic status and full-term development of bovine cloned embryos treated with trichostatin A. J Reprod Dev. 2012;58:302–9.

    Article  CAS  PubMed  Google Scholar 

  18. Jafarpour F, Hosseini SM, Hajian M, Forouzanfar M, Ostadhosseini S, Abedi P, Gholami S, Ghaedi K, Gourabi H, Shahverdi AH, Vosough AD, Nasr-Esfahani MH. Somatic cell-induced hyperacetylation, but not hypomethylation, positively and reversibly affects the efficiency of in vitro cloned blastocyst production in cattle. Cell Reprogram. 2011;13:483–93.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Wu X, Li Y, Li GP, Yang D, Yue Y, Wang L, Li K, Xin P, Bou S, Yu H. Trichostatin A improved epigenetic modifications of transfected cells but did not improve subsequent cloned embryo development. Anim Biotechnol. 2008;19:211–24.

    Article  CAS  PubMed  Google Scholar 

  20. Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE. Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev Biol. 2004;266:62–75.

    Article  CAS  PubMed  Google Scholar 

  21. Chang CC, Gao S, Sung LY, Corry GN, Ma Y, Nagy ZP, Tian XC, Rasmussen TP. Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. Cell Reprogram. 2010;12:43–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Karpiuk O, Najafova Z, Kramer F, Hennion M, Galonska C, Konig A, Snaidero N, Vogel T, Shchebet A, Begus-Nahrmann Y, Kassem M, Simons M, Shcherbata H, Beissbarth T, Johnsen SA. The histone H2B monoubiquitination regulatory pathway is required for differentiation of multipotent stem cells. Mol Cell. 2012;46:705–13.

    Article  CAS  PubMed  Google Scholar 

  23. Endoh M, Endo TA, Endoh T, Isono K, Sharif J, Ohara O, Toyoda T, Ito T, Eskeland R, Bickmore WA, Vidal M, Bernstein BE, Koseki H. Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity. PLoS Genet. 2012;8:e1002774.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Tavares L, Dimitrova E, Oxley D, Webster J, Poot R, Demmers J, Bezstarosti K, Taylor S, Ura H, Koide H, Wutz A, Vidal M, Elderkin S, Brockdorff N. RYBP–PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell. 2012;148:664–78.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Gutierrez L, Oktaba K, Scheuermann JC, Gambetta MC, Ly-Hartig N, Muller J. The role of the histone H2A ubiquitinase Sce in polycomb repression. Development. 2012;139:117–27.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Scheuermann JC, de Ayala Alonso AG, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Muller J. Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature. 2010;465:243–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Mao J, Tessanne K, Whitworth KM, Spate LD, Walters EM, Samuel MS, Murphy CN, Tracy L, Zhao J, Prather RS. Effects of combined treatment of MG132 and scriptaid on early and term development of porcine somatic cell nuclear transfer embryos. Cell Reprogram. 2012;14:385–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Gao S, Han Z, Kihara M, Adashi E, Latham KE. Protease inhibitor MG132 in cloning: no end to the nightmare. Trends Biotechnol. 2005;23:66–8.

    Article  CAS  PubMed  Google Scholar 

  29. Nolen LD, Gao S, Han Z, Mann MR, Gie Chung Y, Otte AP, Bartolomei MS, Latham KE. X chromosome reactivation and regulation in cloned embryos. Dev Biol. 2005;279:525–40.

    Article  CAS  PubMed  Google Scholar 

  30. Matoba S, Inoue K, Kohda T, Sugimoto M, Mizutani E, Ogonuki N, Nakamura T, Abe K, Nakano T, Ishino F, Ogura A. RNAi-mediated knockdown of Xist can rescue the impaired postimplantation development of cloned mouse embryos. Proc Natl Acad Sci U S A. 2011;108:20621–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Inoue K, Kohda T, Sugimoto M, Sado T, Ogonuki N, Matoba S, Shiura H, Ikeda R, Mochida K, Fujii T, Sawai K, Otte AP, Tian XC, Yang X, Ishino F, Abe K, Ogura A. Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science. 2010;330:496–9.

    Article  CAS  PubMed  Google Scholar 

  32. Eggan K, Akutsu H, Hochedlinger K, Rideout 3rd W, Yanagimachi R, Jaenisch R. X-chromosome inactivation in cloned mouse embryos. Science. 2000;290:1578–81.

    Article  CAS  PubMed  Google Scholar 

  33. Jeon BG, Coppola G, Perrault SD, Rho GJ, Betts DH, King WA. S-adenosylhomocysteine treatment of adult female fibroblasts alters X-chromosome inactivation and improves in vitro embryo development after somatic cell nuclear transfer. Reproduction. 2008;135:815–28.

    Article  CAS  PubMed  Google Scholar 

  34. Chung YG, Ratnam S, Chaillet JR, Latham KE. Abnormal regulation of DNA methyltransferase expression in cloned mouse embryos. Biol Reprod. 2003;69:146–53.

    Article  CAS  PubMed  Google Scholar 

  35. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, Chaillet JR. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell. 2001;104:829–38.

    Article  CAS  PubMed  Google Scholar 

  36. Ratnam S, Mertineit C, Ding F, Howell CY, Clarke HJ, Bestor TH, Chaillet JR, Trasler JM. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev Biol. 2002;245:304–14.

    Article  CAS  PubMed  Google Scholar 

  37. Doherty AS, Bartolomei MS, Schultz RM. Regulation of stage-specific nuclear translocation of Dnmt1o during preimplantation mouse development. Dev Biol. 2002;242:255–66.

    Article  CAS  PubMed  Google Scholar 

  38. Cardoso MC, Leonhardt H. DNA methyltransferase is actively retained in the cytoplasm during early development. J Cell Biol. 1999;147:25–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Grohmann M, Spada F, Schermelleh L, Alenina N, Bader M, Cardoso MC, Leonhardt H. Restricted mobility of Dnmt1 in preimplantation embryos: implications for epigenetic reprogramming. BMC Dev Biol. 2005;5:18.

    Article  PubMed Central  PubMed  Google Scholar 

  40. Ding F, Chaillet JR. In vivo stabilization of the Dnmt1 (cytosine-5)-methyltransferase protein. Proc Natl Acad Sci U S A. 2002;99:14861–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Kurihara Y, Kawamura Y, Uchijima Y, Amamo T, Kobayashi H, Asano T, Kurihara H. Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltransferase 1. Dev Biol. 2008;313:335–46.

    Article  CAS  PubMed  Google Scholar 

  42. Haines TR, Rodenhiser DI, Ainsworth PJ. Allele-specific non-CpG methylation of the Nf1 gene during early mouse development. Dev Biol. 2001;240:585–98.

    Article  CAS  PubMed  Google Scholar 

  43. Wei Y, Huan Y, Shi Y, Liu Z, Bou G, Luo Y, Zhang L, Yang C, Kong Q, Tian J, Xia P, Sun QY, Liu Z. Unfaithful maintenance of methylation imprints due to loss of maternal nuclear Dnmt1 during somatic cell nuclear transfer. PLoS One. 2011;6:e20154.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Mann MR, Chung YG, Nolen LD, Verona RI, Latham KE, Bartolomei MS. Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol Reprod. 2003;69:902–14.

    Article  CAS  PubMed  Google Scholar 

  45. Su JM, Yang B, Wang YS, Li YY, Xiong XR, Wang LJ, Guo ZK, Zhang Y. Expression and methylation status of imprinted genes in placentas of deceased and live cloned transgenic calves. Theriogenology. 2011;75:1346–59.

    Article  CAS  PubMed  Google Scholar 

  46. Shen CJ, Cheng WT, Wu SC, Chen HL, Tsai TC, Yang SH, Chen CM. Differential differences in methylation status of putative imprinted genes among cloned swine genomes. PLoS One. 2012;7:e32812.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Grandjean V, Yaman R, Cuzin F, Rassoulzadegan M. Inheritance of an epigenetic mark: the CpG DNA methyltransferase 1 is required for de novo establishment of a complex pattern of non-CpG methylation. PLoS One. 2007;2:e1136.

    Article  PubMed Central  PubMed  Google Scholar 

  48. Nasonkin IO, Lazo K, Hambright D, Brooks M, Fariss R, Swaroop A. Distinct nuclear localization patterns of DNA methyltransferases in developing and mature mammalian retina. J Comp Neurol. 2011;519:1914–30.

    Article  CAS  PubMed  Google Scholar 

  49. Desplats P, Spencer B, Coffee E, Patel P, Michael S, Patrick C, Adame A, Rockenstein E, Masliah E. Alpha-synuclein sequesters Dnmt1 from the nucleus: a novel mechanism for epigenetic alterations in Lewy body diseases. J Biol Chem. 2011;286:9031–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Mastroeni D, Chouliaras L, Grover A, Liang WS, Hauns K, Rogers J, Coleman PD. Reduced RAN expression and disrupted transport between cytoplasm and nucleus; a key event in Alzheimer’s disease pathophysiology. PLoS One. 2013;8:e53349.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Qin W, Leonhardt H, Spada F. Usp7 and Uhrf1 control ubiquitination and stability of the maintenance DNA methyltransferase Dnmt1. J Cell Biochem. 2011;112:439–44.

    Article  CAS  PubMed  Google Scholar 

  52. Boiani M, Eckardt S, Scholer HR, McLaughlin KJ. Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev. 2002;16:1209–19.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Cheng Y, Gaughan JP, Midic U, Han Z, Liang CG, Patel BG, Latham K. Systems genetics implicates cytoskeletal genes in oocyte control of cloned embryo quality. Genetics. 2013;193(3):877–96.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Schnetz MP, Handoko L, Akhtar-Zaidi B, Bartels CF, Pereira CF, Fisher AG, Adams DJ, Flicek P, Crawford GE, Laframboise T, Tesar P, Wei CL, Scacheri PC. CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet. 2010;6:e1001023.

    Article  PubMed Central  PubMed  Google Scholar 

  55. Gelmetti V, Zhang J, Fanelli M, Minucci S, Pelicci PG, Lazar MA. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol Cell Biol. 1998;18:7185–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Kahali S, Sarcar B, Prabhu A, Seto E, Chinnaiyan P. Class I histone deacetylases localize to the endoplasmic reticulum and modulate the unfolded protein response. FASEB J. 2012;26:2437–45.

    Article  CAS  PubMed  Google Scholar 

  57. Samant SA, Courson DS, Sundaresan NR, Pillai VB, Tan M, Zhao Y, Shroff SG, Rock RS, Gupta MP. HDAC3-dependent reversible lysine acetylation of cardiac myosin heavy chain isoforms modulates their enzymatic and motor activity. J Biol Chem. 2011;286:5567–77.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Ryhanen T, Viiri J, Hyttinen JM, Uusitalo H, Salminen A, Kaarniranta K. Influence of Hsp90 and HDAC inhibition and tubulin acetylation on perinuclear protein aggregation in human retinal pigment epithelial cells. J Biomed Biotechnol. 2011;2011:798052.

    Article  PubMed Central  PubMed  Google Scholar 

  59. Wilson AJ, Byun DS, Nasser S, Murray LB, Ayyanar K, Arango D, Figueroa M, Melnick A, Kao GD, Augenlicht LH, Mariadason JM. HDAC4 promotes growth of colon cancer cells via repression of p21. Mol Biol Cell. 2008;19:4062–75.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Carta S, Tassi S, Semino C, Fossati G, Mascagni P, Dinarello CA, Rubartelli A. Histone deacetylase inhibitors prevent exocytosis of interleukin-1beta-containing secretory lysosomes: role of microtubules. Blood. 2006;108:1618–26.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Haworth RS, Stathopoulou K, Candasamy AJ, Avkiran M. Neurohormonal regulation of cardiac histone deacetylase 5 nuclear localization by phosphorylation-dependent and phosphorylation-independent mechanisms. Circ Res. 2012;110:1585–95.

    Article  CAS  PubMed  Google Scholar 

  62. Han Z, Vassena R, Chi MM, Potireddy S, Sutovsky M, Moley KH, Sutovsky P, Latham KE. Role of glucose in cloned mouse embryo development. Am J Physiol Endocrinol Metab. 2008;295:E798–809.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Vassena R, Han Z, Gao S, Baldwin DA, Schultz RM, Latham KE. Tough beginnings: alterations in the transcriptome of cloned embryos during the first two cell cycles. Dev Biol. 2007;304:75–89.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Sutovsky P, Prather RS. Nuclear remodeling after SCNT: a contractor’s nightmare. Trends Biotechnol. 2004;22:205–8.

    Article  CAS  PubMed  Google Scholar 

  65. Zhou Q, Renard JP, Le Friec G, Brochard V, Beaujean N, Cherifi Y, Fraichard A, Cozzi J. Generation of fertile cloned rats by regulating oocyte activation. Science. 2003;302:1179.

    Article  CAS  PubMed  Google Scholar 

  66. Simerly C, Dominko T, Navara C, Payne C, Capuano S, Gosman G, Chong KY, Takahashi D, Chace C, Compton D, Hewitson L, Schatten G. Molecular correlates of primate nuclear transfer failures. Science. 2003;300:297.

    Article  PubMed  Google Scholar 

  67. Miyara F, Han Z, Gao S, Vassena R, Latham KE. Non-equivalence of embryonic and somatic cell nuclei affecting spindle composition in clones. Dev Biol. 2006;289:206–17.

    Article  CAS  PubMed  Google Scholar 

  68. Han Z, Liang CG, Cheng Y, Duan X, Zhong Z, Potireddy S, Moncada C, Merali S, Latham KE. Oocyte spindle proteomics analysis leading to rescue of chromosome congression defects in cloned embryos. J Proteome Res. 2010;9:6025–32.

    Article  CAS  PubMed  Google Scholar 

  69. Mizutani E, Yamagata K, Ono T, Akagi S, Geshi M, Wakayama T. Abnormal chromosome segregation at early cleavage is a major cause of the full-term developmental failure of mouse clones. Dev Biol. 2012;364:56–65.

    Article  CAS  PubMed  Google Scholar 

  70. Lin CH, Hu CK, Shih HM. Clathrin heavy chain mediates TACC3 targeting to mitotic spindles to ensure spindle stability. J Cell Biol. 2010;189:1097–105.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Royle SJ, Lagnado L. Trimerisation is important for the function of clathrin at the mitotic spindle. J Cell Sci. 2006;119:4071–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Gao S, Czirr E, Chung YG, Han Z, Latham KE. Genetic variation in oocyte phenotype revealed through parthenogenesis and cloning: correlation with differences in pronuclear epigenetic modification. Biol Reprod. 2004;70:1162–70.

    Article  CAS  PubMed  Google Scholar 

  73. Li L, Baibakov B, Dean J. A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev Cell. 2008;15:416–25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Ohsugi M, Zheng P, Baibakov B, Li L, Dean J. Maternally derived FILIA-MATER complex localizes asymmetrically in cleavage-stage mouse embryos. Development. 2008;135: 259–69.

    Article  CAS  PubMed  Google Scholar 

  75. Kan R, Yurttas P, Kim B, Jin M, Wo L, Lee B, Gosden R, Coonrod SA. Regulation of mouse oocyte microtubule and organelle dynamics by PADI6 and the cytoplasmic lattices. Dev Biol. 2011;350:311–22.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Houliston E, Maro B. Posttranslational modification of distinct microtubule subpopulations during cell polarization and differentiation in the mouse preimplantation embryo. J Cell Biol. 1989;108:543–51.

    Article  CAS  PubMed  Google Scholar 

  77. Chung YG, Mann MR, Bartolomei MS, Latham KE. Nuclear–cytoplasmic “tug of war” during cloning: effects of somatic cell nuclei on culture medium preferences of preimplantation cloned mouse embryos. Biol Reprod. 2002;66:1178–84.

    Article  CAS  PubMed  Google Scholar 

  78. Gao S, Chung YG, Williams JW, Riley J, Moley K, Latham KE. Somatic cell-like features of cloned mouse embryos prepared with cultured myoblast nuclei. Biol Reprod. 2003;69: 48–56.

    Article  CAS  PubMed  Google Scholar 

  79. Sommermann TG, O’Neill K, Plas DR, Cahir-McFarland E. IKKbeta and NF-kappaB transcription govern lymphoma cell survival through AKT-induced plasma membrane trafficking of GLUT1. Cancer Res. 2011;71:7291–300.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Ribeiro-Mason K, Boulesteix C, Brochard V, Aguirre-Lavin T, Salvaing J, Fleurot R, Adenot P, Maalouf WE, Beaujean N. Nuclear dynamics of histone H3 trimethylated on lysine 9 and/or phosphorylated on serine 10 in mouse cloned embryos as new markers of reprogramming? Cell Reprogram. 2012;14:283–94.

    CAS  PubMed  Google Scholar 

  81. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol. 2003;13:1116–21.

    Article  CAS  PubMed  Google Scholar 

  82. Wu X, Li Y, Xue L, Wang L, Yue Y, Li K, Bou S, Li GP, Yu H. Multiple histone site epigenetic modifications in nuclear transfer and in vitro fertilized bovine embryos. Zygote. 2011;19:31–45.

    Article  CAS  PubMed  Google Scholar 

  83. Shao GB, Ding HM, Gong AH, Xiao DS. Inheritance of histone H3 methylation in reprogramming of somatic nuclei following nuclear transfer. J Reprod Dev. 2008;54:233–8.

    Article  CAS  PubMed  Google Scholar 

  84. Bui HT, Wakayama S, Kishigami S, Park KK, Kim JH, Thuan NV, Wakayama T. Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos. Biol Reprod. 2010;83:454–63.

    Article  CAS  PubMed  Google Scholar 

  85. Wang F, Kou Z, Zhang Y, Gao S. Dynamic reprogramming of histone acetylation and methylation in the first cell cycle of cloned mouse embryos. Biol Reprod. 2007;77:1007–16.

    Article  CAS  PubMed  Google Scholar 

  86. Suzuki T, Kondo S, Wakayama T, Cizdziel PE, Hayashizaki Y. Genome-wide analysis of abnormal H3K9 acetylation in cloned mice. PLoS One. 2008;3:e1905.

    Article  PubMed Central  PubMed  Google Scholar 

  87. Nishida H, Kondo S, Suzuki T, Tsujimura Y, Komatsu S, Wakayama T, Hayashizaki Y. An epigenetic aberration increased in intergenic regions of cloned mice. Mamm Genome. 2008;19:667–74.

    Article  CAS  PubMed  Google Scholar 

  88. Yang J, Yang S, Beaujean N, Niu Y, He X, Xie Y, Tang X, Wang L, Zhou Q, Ji W. Epigenetic marks in cloned rhesus monkey embryos: comparison with counterparts produced in vitro. Biol Reprod. 2007;76:36–42.

    Article  CAS  PubMed  Google Scholar 

  89. Enright BP, Kubota C, Yang X, Tian XC. Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2′-deoxycytidine. Biol Reprod. 2003;69:896–901.

    Article  CAS  PubMed  Google Scholar 

  90. Fan Y, Jiang Y, Chen X, Ou Z, Yin Y, Huang S, Kou Z, Li Q, Long X, Liu J, Luo Y, Liao B, Gao S, Sun X. Derivation of cloned human blastocysts by histone deacetylase inhibitor treatment after somatic cell nuclear transfer with beta-thalassemia fibroblasts. Stem Cells Dev. 2011;20:1951–9.

    Article  CAS  PubMed  Google Scholar 

  91. Lee HS, Yu XF, Bang JI, Cho SJ, Deb GK, Kim BW, Kong IK. Enhanced histone acetylation in somatic cells induced by a histone deacetylase inhibitor improved inter-generic cloned leopard cat blastocysts. Theriogenology. 2010;74:1439–49.

    Article  CAS  PubMed  Google Scholar 

  92. Enright BP, Sung LY, Chang CC, Yang X, Tian XC. Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2′-deoxycytidine. Biol Reprod. 2005;72:944–8.

    Article  CAS  PubMed  Google Scholar 

  93. Cervera RP, Marti-Gutierrez N, Escorihuela E, Moreno R, Stojkovic M. Trichostatin A affects histone acetylation and gene expression in porcine somatic cell nucleus transfer embryos. Theriogenology. 2009;72:1097–110.

    Article  CAS  PubMed  Google Scholar 

  94. Wang K, Beyhan Z, Rodriguez RM, Ross PJ, Iager AE, Kaiser GG, Chen Y, Cibelli JB. Bovine ooplasm partially remodels primate somatic nuclei following somatic cell nuclear transfer. Cloning Stem Cells. 2009;11:187–202.

    Article  CAS  PubMed  Google Scholar 

  95. Iager AE, Ragina NP, Ross PJ, Beyhan Z, Cunniff K, Rodriguez RM, Cibelli JB. Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells. 2008;10:371–9.

    Article  CAS  PubMed  Google Scholar 

  96. Maalouf WE, Alberio R, Campbell KH. Differential acetylation of histone H4 lysine during development of in vitro fertilized, cloned and parthenogenetically activated bovine embryos. Epigenetics. 2008;3:199–209.

    Article  PubMed  Google Scholar 

  97. Lim JH, Boozer L, Mariani CL, Piedrahita JA, Olby NJ. Generation and characterization of neurospheres from canine adipose tissue-derived stromal cells. Cell Reprogram. 2010;12:417–25.

    Article  CAS  PubMed  Google Scholar 

  98. Suteevun T, Smith SL, Muenthaisong S, Yang X, Parnpai R, Tian XC. Anomalous mRNA levels of chromatin remodeling genes in swamp buffalo (Bubalus bubalis) cloned embryos. Theriogenology. 2006;65:1704–15.

    Article  CAS  PubMed  Google Scholar 

  99. Yang F, Hao R, Kessler B, Brem G, Wolf E, Zakhartchenko V. Rabbit somatic cell cloning: effects of donor cell type, histone acetylation status and chimeric embryo complementation. Reproduction. 2007;133:219–30.

    Article  CAS  PubMed  Google Scholar 

  100. Bui HT, Van Thuan N, Wakayama T, Miyano T. Chromatin remodeling in somatic cells injected into mature pig oocytes. Reproduction. 2006;131:1037–49.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

The work in the author’s laboratory is supported in part by a grant from the National Institute of Child Health and Human Development/National Institutes of Health (HD43092).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keith E. Latham .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Latham, K.E. (2014). Role of Aberrant Protein Modification, Assembly, and Localization in Cloned Embryo Phenotypes. In: Sutovsky, P. (eds) Posttranslational Protein Modifications in the Reproductive System. Advances in Experimental Medicine and Biology, vol 759. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0817-2_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-0817-2_7

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4939-0816-5

  • Online ISBN: 978-1-4939-0817-2

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics