Cell totipotency: molecular features, induction, and maintenance

Lu, Falong; Zhang, Yi

doi:10.1093/nsr/nwv009

Cited by 69 publications

(54 citation statements)

References 95 publications

(114 reference statements)

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“…In animals, after fertilization and the formation of the zygote (totipotent) chromatin is decondensed and acquires specific epigenetic marks ( Burton and Torres-Padilla, 2010 ). High mobility of core histones, remodeling of constitutive heterochromatin marks, and acquisition of specific permissive histone modifications have been suggested as required features for the chromatin state compatible with cellular reprogramming ( Burton and Torres-Padilla, 2010 ; Boskovic et al, 2014 ; Lu and Zhang, 2015 ). In plants, cellular reprogramming has been associated with nuclear changes including chromatin decondensation, reduction in heterochromatin and changes in DNA methylation and histone modifications landscapes ( Solís et al, 2012 ; She et al, 2013 ; El-Tantawy et al, 2014 ; Rodriguez-Sanz et al, 2014b ).…”

Section: Discussionmentioning

confidence: 99%

5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley

et al. 2015

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Microspores are reprogrammed by stress in vitro toward embryogenesis. This process is an important tool in breeding to obtain double-haploid plants. DNA methylation is a major epigenetic modification that changes in differentiation and proliferation. We have shown changes in global DNA methylation during microspore reprogramming. 5-Azacytidine (AzaC) cannot be methylated and leads to DNA hypomethylation. AzaC is a useful demethylating agent to study DNA dynamics, with a potential application in microspore embryogenesis. This work analyzes the effects of short and long AzaC treatments on microspore embryogenesis initiation and progression in two species, the dicot Brassica napus and the monocot Hordeum vulgare. This involved the quantitative analyses of proembryo and embryo production, the quantification of DNA methylation, 5-methyl-deoxy-cytidine (5mdC) immunofluorescence and confocal microscopy, and the analysis of chromatin organization (condensation/decondensation) by light and electron microscopy. Four days of AzaC treatments (2.5 μM) increased embryo induction, response associated with a decrease of DNA methylation, modified 5mdC, and heterochromatin patterns compared to untreated embryos. By contrast, longer AzaC treatments diminished embryo production. Similar effects were found in both species, indicating that DNA demethylation promotes microspore reprogramming, totipotency acquisition, and embryogenesis initiation, while embryo differentiation requires de novo DNA methylation and is prevented by AzaC. This suggests a role for DNA methylation in the repression of microspore reprogramming and possibly totipotency acquisition. Results provide new insights into the role of epigenetic modifications in microspore embryogenesis and suggest a potential benefit of inhibitors, such as AzaC, to improve the process efficiency in biotechnology and breeding programs.

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Section: Discussionmentioning

confidence: 99%

5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley

et al. 2015

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“…Following fertilization, the newly formed zygotic genome is activated through a process known as the zygotic genome activation (ZGA), which enables zygote can subsequently development to the adult animal (Lu & Zhang, 2015). A similar mechanism is likely used in ZGA of SCNT embryos (T. Gao et al, 2007; Matoba & Zhang, 2018).…”

Section: Introductionmentioning

confidence: 99%

Significant improvement of reprogramming efficiency by transient overexpression of ZGA inducer Dux but not Dppa2/4

Yang¹,

Liu²,

Song

et al. 2019

Preprint

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12Cloned animal have been reported by somatic cell nuclear transfer (SCNT) for many years. 13However, the SCNT biotechnology is extremely inefficient, and zygotic genome activation 14 (ZGA) is required for SCNT and chemical mediated somatic cell reprogramming. To identify 15 candidate factors that facilitate ZGA in SCNT reprogramming, we carried out a siRNA-16 repressor and mRNA-inducer screening in SCNT to identify epigenetic and chromatin 17 regulators of the ZGA transcriptional program. Through a series of experiments, we 18 demonstrate that transient overexpression of Dux not only improved SCNT efficiency, but also 19 increased the efficiency of chemical reprogramming. Furthermore, transient overexpression 20 of Dux combined with inactivation of DNA methyltransferases (Dnmts) further promote the 21 overall development of SCNT-derived animals. These findings enhance our understanding of 22 ZGA-regulators in SCNT and chemical mediated somatic cell reprogramming, and suggest 23 that transient overexpression of Dux may serve as a useful tool to enhances the somatic 24 reprogramming efficiency. 25 26 29 term for china) 1. After the first mammal Dolly sheep to be cloned 2, the created non-human 30 primate has once again attracted worldwide attention. Indeed, successful cloning of the sheep 31 and monkey not only made reproductive cloning possible, but also raised the possibility of 32 therapeutic cloning. Somatic cell nuclear transfer (SCNT) is the technical term for cloning in 33 which terminal differentiated somatic cell is transferred into enucleated oocyte, in which the 34 cytoplasmic factors reprogram the nucleus to become a zygote-like state 3. Both SCNT derived 35 and Yamanaka factors induced pluripotent stem (iPS) cells have the potential to generate36 patient-specific pluripotent stem cells for replacement therapy. Compared with iPS, the SCNT 37 reprogramming is transgene-free and oncogene-free methodologies. Thus, SCNT derived 38 pluripotent stem cells would be more suitable for human therapeutic applications.39 3 40Following fertilization, the newly formed zygotic genome is activated through a process 41 known as the zygotic genome activation (ZGA), which enables zygotes can subsequently drive 42 the differentiation of all the diverse cell types of the adult animal 4. A similar mechanism is 43 likely used in ZGA of SCNT embryos 3,5. The 'erase-and-rebuild' strategy is used to establish 44 the zygotic transcription program during SCNT reprogramming 5. Consistently, our and others 45 recent results have revealed that incomplete ZGA is a major SCNT reprogramming barrier 6-8. 46Although many advances have been made in SCNT technology via different epigenetic 47 regulators, the SCNT for producing cloned animals still inefficient. 48 49 Materials and Methods 50 Animals and Chemicals 51 Specific pathogen-free (SPF)-grade BDF1 (C57BL/6N × DBA/2), CD1, and Kun-Ming (KM) 52 mice mice were purchased from Laboratory Animal Research Center (Inner Mongolia 53 University) or Vital River Laboratories (Beijing, China). A...

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“…However, the factors that confer totipotency, the ability to give rise to cells in both embryonic and extra-embryonic lineages, are still elusive. Moreover, although it is currently unknown whether totipotency in metazoans can be induced and maintained in vitro [ 4 ], differentiated plant somatic cells can be induced in vitro to give rise to fully totipotent cells which develop into somatic embryos [ 5 ]. Many plant species, including Arabidopsis thaliana ( Arabidopsis ), respond well to somatic embryogenesis (SE) induction [ 6 , 7 ].…”

Section: Introductionmentioning

confidence: 99%

Profiling the onset of somatic embryogenesis in Arabidopsis

et al. 2017

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BackgroundTotipotency is the ability of a cell to regenerate a whole organism. Plant somatic embryogenesis (SE) is a remarkable example of totipotency because somatic cells reverse differentiation, respond to an appropriate stimulus and initiate embryo development. Although SE is an ideal system to investigate de-differentiation and differentiation, we still lack a deep molecular understanding of the phenomenon due to experimental restraints.ResultsWe applied the INTACT method to specifically isolate the nuclei of those cells undergoing SE among the majority of non-embryogenic cells that make up a callus. We compared the transcriptome of embryogenic cells to the one of proliferating callus cells. Our analyses revealed that embryogenic cells are transcriptionally rather than metabolically active. Embryogenic cells shut off biochemical pathways involved in carbohydrate and lipid metabolism and activate the transcriptional machinery. Furthermore, we show how early in SE, ground tissue and leaf primordia specification are switched on before the specification of a shoot apical meristem.ConclusionsThis is the first attempt to specifically profile embryogenic cells among the different cell types that constitute plant in vitro tissue cultures. Our comparative analyses provide insights in the gene networks regulating SE and open new research avenues in the field of plant regeneration.Electronic supplementary materialThe online version of this article (doi: 10.1186/s12864-017-4391-1) contains supplementary material, which is available to authorized users.

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Cell totipotency: molecular features, induction, and maintenance

Cited by 69 publications

References 95 publications

5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley

5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley

Significant improvement of reprogramming efficiency by transient overexpression of ZGA inducer Dux but not Dppa2/4

Profiling the onset of somatic embryogenesis in Arabidopsis

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