Irregular transcriptome reprogramming probably causes thec developmental failure of embryos produced by interspecies somatic cell nuclear transfer between the Przewalski’s gazelle and the bovine

BMC Genomics

Guangpeng Li¹  Shorgan Bou¹  Qianzhong Li²  Kun Liu¹  Zhuying Wei¹  Chunling Bai¹  Guanghua Su¹  Yu Gao¹  Yongchun Zuo¹ 

[1] The Key Laboratory of National Education Ministry for Mammalian Reproductive Biology and Biotechnology, Inner Mongolia University, Hohhot 010070, China;Laboratory of Theoretical Biophysics, School of Physical Science and Technology, Inner Mongolia University, Hohhot 010021, China

关键词: Mitochondrial DNA;    Transcriptional regulation;    Embryonic genome activation;    Transcriptome reprogramming;    Interspecies somatic cell nuclear transfer (iSCNT);   

Others  :  1127229
DOI  :  10.1186/1471-2164-15-1113

 received in 2014-05-20, accepted in 2014-12-09,  发布年份 2014

【 摘 要 】

Background

Interspecies somatic cell nuclear transfer (iSCNT) has been regarded as a potential alternative for rescuing highly endangered species and can be used as a model for studying nuclear–cytoplasmic interactions. However, iSCNT embryos often fail to produce viable offspring. The alterations in normal molecular mechanisms contributing to extremely poor development are for the most part unknown.

Results

Przewalski’s gazelle–bovine iSCNT embryos (PBNT) were produced by transferring Przewalski’s gazelle fibroblast nuclei into enucleated bovine oocytes. The percentages of PBNT embryos that developed to morula/blastocyst stages were extremely low even with the use of various treatments that included different SCNT protocols and treatment of embryos with small molecules. Transcriptional microarray analyses of the cloned embryos showed that the upregulation of reprogramming-associated genes in bovine–bovine SCNT (BBNT) embryos was significantly higher than those observed in PBNT embryos (1527:643). In all, 139 transcripts related to various transcription regulation factors (TFs) were unsuccessfully activated in the iSCNT embryos. Maternal degradation profiles showed that 1515 genes were uniquely downregulated in the BBNT embryos, while 343 genes were downregulated in the PBNT embryos. Incompatibilities between mitochondrial DNA (mtDNA) and nuclear DNA revealed that the TOMM (translocase of outer mitochondrial membrane)/TIMM (translocase of inner mitochondrial membrane) complex-associated genes in BBNT embryos had the highest expression levels, while the PBNT embryos exhibited much lower expression rates.

Conclusions

Improper degradation of maternal transcripts, incomplete activation of TFs and abnormal expression of genes associated with mitochondrial function in PBNT embryos likely contributed to incomplete reprogramming of the donor cell nuclei and therefore led to the developmental failure of these cloned embryos.

【 授权许可】

   
2014 Zuo et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Group ISAS: Specialist Group: Procapra przewalskii. IUCN 2008. IUCN Red List of Threatened Species. Retrieved 10 December 2008. Database entry includes justification for why this species is Endangered 2008.
• [2]Leslie DM, Groves CP, Abramov AV: Procapra przewalskii (Artiodactyla: Bovidae). Mamm Species 2010, 42:124-137.
• [3]Li Z, Jiang Z, Beauchamp G: Nonrandom mixing between groups of Przewalski’s gazelle and Tibetan gazelle. J Mammalogy 2010, 91:674-680.
• [4]Jiang Z, Lei R, Liu B, Li C: A review on the researches of Przewalski’s gazelle. Chinese J Zool 2002, 38:129-132.
• [5]Liu B, Jiang Z: Impacts of grassland fencing on plant communities and conservation of a rare gazelle, the Przewalski’s gazelle. Chin Biodiversity 2001, 10:326-331.
• [6]Chen D, Sun Q, Liu J, Li G, Lian L, Wang M, Han Z, Song X, Li J, Sun Q: The giant panda (Ailuropoda melanoleuca) somatic nucleus can dedifferentiate in rabbit ooplasm and support early development of the reconstructed egg. Sci Chin Ser C: Life Sci 1999, 42:346-353.
• [7]Chen D, Han Z, Ziyu Z, Ruicheng W, Zhonghua L, Minkang W, Li L, Jinsong L, Jun D, Pengyan W, Hemin Z: The effect of series nuclear transfer protocol on the embryonic development of the giant panda interpecies cloning. Chin Sci Bulletin 2001, 46:1899-1901.
• [8]Zhao ZJ, Li RC, Cao HH, Zhang QJ, Jiang MX, Ouyang YC, Nan CL, Lei ZL, Song XF, Sun QY, Chen DY: Interspecies nuclear transfer of Tibetan antelope using caprine oocyte as recipient. Mol Reprod Dev 2007, 74:412-419.
• [9]Sansinena MJ, Hylan D, Hebert K, Denniston RS, Godke RA: Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology 2005, 63:1081-1091.
• [10]Li Y, Dai Y, Du W, Zhao C, Wang L, Wang H, Liu Y, Li R, Li N: In vitro development of yak (Bos grunniens) embryos generated by interspecies nuclear transfer. Anim Reprod Sci 2007, 101:45-59.
• [11]Song J, Hua S, Song K, Zhang Y: Culture, characteristics and chromosome complement of Siberian tiger fibroblasts for nuclear transfer. In Vitro Cell Dev Biol Anim 2007, 43:203-209.
• [12]Bhuiyan MMU, Suzuki Y, Watanabe H, Lee E, Hirayama H, Matsuoka K, Fujise Y, Ishikawa H, Ohsumi S, Fukui Y: Production of sei whale (Balaenoptera borealis) cloned embryos by inter-and intra-species somatic cell nuclear transfer. J Reprod Dev 2010, 56:131-139.
• [13]Loi P, Ptak G, Barboni B, Fulka J, Cappai P, Clinton M: Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat Biotech 2001, 19:962-964.
• [14]Yang CY, Li RC, Pang CY, Yang BZ, Qin GS, Chen MT, Zhang XF, Huang FX, Zheng HY, Huang YJ, Liang XW: Study on the inter-subspecies nuclear transfer of river buffalo somatic cell nuclei into swamp buffalo oocyte cytoplasm. Anim Reprod Sci 2010, 121:78-83.
• [15]Amarnath D, Choi I, Moawad AR, Wakayama T, Campbell KH: Nuclear-cytoplasmic incompatibility and inefficient development of pig-mouse cytoplasmic hybrid embryos. Reproduction 2011, 142:295-307.
• [16]Bowles EJ, Lee JH, Alberio R, Lloyd RE, Stekel D, Campbell KH, St John JC: Contrasting effects of in vitro fertilization and nuclear transfer on the expression of mtDNA replication factors. Genetics 2007, 176:1511-1526.
• [17]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. Clon Stem Cell 2009, 11:187-202.
• [18]Chung Y, Bishop CE, Treff NR, Walker SJ, Sandler VM, Becker S, Klimanskaya I, Wun WS, Dunn R, Hall RM, Su J, Lu SJ, Maserati M, Choi YH, Scott R, Atala A, Dittman R, Lanza R: Reprogramming of human somatic cells using human and animal oocytes. Clon Stem Cell 2009, 11:213-223.
• [19]Narbonne P, Simpson DE, Gurdon JB: Deficient induction response in a Xenopus nucleocytoplasmic hybrid. PLoS Biol 2011, 9:e1001197.
• [20]Esteves TC, Balbach ST, Pfeiffer MJ: Araúzo‒Bravo MJ, Klein DC, Sinn M, Boiani M: Somatic cell nuclear reprogramming of mouse oocytes endures beyond reproductive decline. Aging Cell 2011, 10:80-95.
• [21]Xu W, Wang Y, Li Y, Wang L, Xiong X, Su J, Zhang Y: Valproic acid improves the in vitro development competence of bovine somatic cell nuclear transfer embryos. Cell Reprogram 2012, 14:138-145.
• [22]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 Develop 2011, 57:120-126.
• [23]Sun L, Wu KL, Zhang D, Wang HY, Wang Y, Xu ZY, Huang XY, Chen ZJ, Liu HQ: Increased cleavage rate of human nuclear transfer embryos after 5-aza-2’-deoxycytidine treatment. Reprod Biomed Online 2012, 25:425-433.
• [24]Xue Z, Huang K, Cai C, Cai L, Jiang CY, Feng Y, Liu Z, Zeng Q, Cheng L, Sun YE, Liu JY, Horvath S, Fan G: Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 2013, 500:593-597.
• [25]Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J, Huang J, Li M, Wu X, Wen L, Lao K, Li R, Qiao J, Tang F: Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 2013, 20:1131-1139.
• [26]Vassena R, Boue S, Gonzalez-Roca E, Aran B, Auer H, Veiga A, Izpisua Belmonte JC: Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development 2011, 138:3699-3709.
• [27]Bauer MF, Hofmann S, Neupert W, Brunner M: Protein translocation into mitochondria: the role of TIM complexes. Trends Cell Biol 2000, 10:25-31.
• [28]Wang K, Otu HH, Chen Y, Lee Y, Latham K, Cibelli JB: Reprogrammed transcriptome in rhesus-bovine interspecies somatic cell nuclear transfer embryos. PLoS One 2011, 6:e22197.
• [29]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.
• [30]Narbonne P, Miyamoto K, Gurdon JB: Reprogramming and development in nuclear transfer embryos and in interspecific systems. Curr Opin Genet Dev 2012, 22:450-458.
• [31]Wen DC, Bi CM, Xu Y, Yang CX, Zhu ZY, Sun QY, Chen DY: Hybrid embryos produced by transferring panda or cat somatic nuclei into rabbit MII oocytes can develop to blastocyst in vitro. J Exp Zool A Comp Exp Biol 2005, 303:689-697.
• [32]Wee G, Shim JJ, Koo DB, Chae JI, Lee KK, Han YM: Epigenetic alteration of the donor cells does not recapitulate the reprogramming of DNA methylation in cloned embryos. Reproduction 2007, 134:781-787.
• [33]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.
• [34]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, 58:302-309.
• [35]Srirattana K, Matsukawa K, Akagi S, Tasai M, Tagami T, Nirasawa K, Nagai T, Kanai Y, Parnpai R, Takeda K: Constant transmission of mitochondrial DNA in intergeneric cloned embryos reconstructed from swamp buffalo fibroblasts and bovine ooplasm. Anim Sci J 2011, 82:236-243.
• [36]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, 237:640-648.
• [37]Sugimura S, Narita K, Yamashiro H, Sugawara A, Shoji T, Terashita Y, Nishimori K, Konno T, Yoshida M, Sato E: Interspecies somatic cell nucleus transfer with porcine oocytes as recipients: A novel bioassay system for assessing the competence of canine somatic cells to develop into embryos. Theriogenology 2009, 72:549-559.
• [38]Wakayama S, Cibelli JB, Wakayama T: Effect of timing of the removal of oocyte chromosomes before or after injection of somatic nucleus on development of NT embryos. Clon Stem Cell 2003, 5:181-189.
• [39]Meng Q, Bai C, Liu Y, Wu X, Bunch TD, Li GP: In vitro development and chromosomal configuration of bovine somatic cloned embryos with nonenucleated metaphase II oocytes. Cell Reprogram 2010, 12:481-490.
• [40]Lagutina I, Fulka H, Brevini TA, Antonini S, Brunetti D, Colleoni S, Gandolfi F, Lazzari G, Fulka J Jr, Galli C: Development, embryonic genome activity and mitochondrial characteristics of bovine-pig inter-family nuclear transfer embryos. Reproduction 2010, 140:273-285.
• [41]Kues W, Sudheer S, Herrmann D, Carnwath J, Havlicek V, Besenfelder U, Lehrach H, Adjaye J, Niemann H: Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. PNAS 2008, 105:19768-19773.
• [42]Lagutina I, Zakhartchenko V, Fulka H, Colleoni S, Wolf E, Fulka J Jr, Lazzari G, Galli C: Formation of nucleoli in interspecies nuclear transfer embryos derived from bovine, porcine, and rabbit oocytes and nuclear donor cells of various species. Reproduction 2011, 141:453-465.
• [43]Alizadeh Z, Kageyama S, Aoki F: Degradation of maternal mRNA in mouse embryos: selective degradation of specific mRNAs after fertilization. Mol Reprod Dev 2005, 72:281-290.
• [44]Minami N, Suzuki T, Tsukamoto S: Zygotic gene activation and maternal factors in mammals. J Reprod Dev 2007, 53:707-715.
• [45]Shin SW, Shimizu N, Tokoro M, Nishikawa S, Hatanaka Y, Anzai M, Hamazaki J, Kishigami S, Saeki K, Hosoi Y, Iritani A, Murata S, Matsumoto K: Mouse zygote-specific proteasome assembly chaperone important for maternal-to-zygotic transition. Biol Open 2013, 2:170-182.
• [46]Maddox-Hyttel P, Svarcova O, Laurincik J: Ribosomal RNA and nucleolar proteins from the oocyte are to some degree used for embryonic nucleolar formation in cattle and pig. Theriogenology 2007, 68(Suppl 1):S63-S70.
• [47]Laurincik J, Maddox-Hyttel P: Nucleolar remodeling in nuclear transfer embryos. Adv Exp Med Biol 2007, 591:84-92.
• [48]Jiang Y, Kelly R, Peters A, Fulka H, Dickinson A, Mitchell DA, St John JC: Interspecies somatic cell nuclear transfer is dependent on compatible mitochondrial DNA and reprogramming factors. PLoS One 2011, 6:e14805.
• [49]Hua S, Zhang Y, Song K, Song J, Zhang Z, Zhang L, Zhang C, Cao J, Ma L: Development of bovine-ovine interspecies cloned embryos and mitochondria segregation in blastomeres during preimplantation. Anim Reprod Sci 2008, 105:245-257.
• [50]Gomez MC, Pope CE, Ricks DM, Lyons J, Dumas C, Dresser BL: Cloning endangered felids using heterospecific donor oocytes and interspecies embryo transfer. Reprod Fertil Dev 2009, 21:76-82.
• [51]Sansinena MJ, Lynn J, Bondioli KR, Denniston RS, Godke RA: Ooplasm transfer and interspecies somatic cell nuclear transfer: heteroplasmy, pattern of mitochondrial migration and effect on embryo development. Zygote 2011, 19:147-156.
• [52]Hiendleder S, Zakhartchenko V, Wolf E: Mitochondria and the success of somatic cell nuclear transfer cloning: from nuclear-mitochondrial interactions to mitochondrial complementation and mitochondrial DNA recombination. Reprod Fertil Dev 2005, 17:69-83.
• [53]Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, Murphy AN, Gaucher SP, Capaldi RA, Gibson BW, Ghosh SS: Characterization of the human heart mitochondrial proteome. Nat Biotechnol 2003, 21:281-286.
• [54]Cotter D, Guda P, Fahy E, Subramaniam S: MitoProteome: mitochondrial protein sequence database and annotation system. Nucleic Acids Res 2004, 32:D463-D467.
• [55]Li GP, White KL, Aston KI, Meerdo LN, Bunch TD: Conditioned medium increases the polyploid cell composition of bovine somatic cell nuclear-transferred blastocysts. Reproduction 2004, 127:221-228.
• [56]Bai C, Liu H, Liu Y, Wu X, Cheng L, Bou S, Li GP: Diploid oocyte formation and tetraploid embryo development induced by cytochalasin B in bovine. Cell Reprogram 2011, 13:37-45.
• [57]Li GP, Bunch TD, White KL, Aston KI, Meerdo LN, Pate BJ, Sessions BR: Development, chromosomal composition, and cell allocation of bovine cloned blastocyst derived from chemically assisted enucleation and cultured in conditioned media. Mol Reprod Dev 2004, 68:189-197.
• [58]Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. PNAS 1998, 95:14863-14868.
• [59]Saldanha AJ: Java Treeview–extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248.
• [60]da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.