基因調控網路與 Sox32 和Sox17 之內胚層斑馬魚發育次基因調控網路

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研究生：	詹子民 Chan, Tzu-Min
論文名稱：	基因調控網路與 Sox32 和Sox17 之內胚層斑馬魚發育次基因調控網路 Gene Regulatory Networks and Subcircuits of Sox32 and Sox17 in Zebrafish Endoderm Development
指導教授：	喻秋華 Yuh, Chiou-Hwa 汪宏達 Wang, Horng-Dar
口試委員:
學位類別：	博士 Doctor
系所名稱：	生命科學暨醫學院 - 生物科技研究所 Biotechnology
論文出版年：	2009
畢業學年度：	97
語文別：	英文
論文頁數：	161
中文關鍵詞：	斑馬魚、背腹側生成、內中胚分化、基因調控網路、轉錄因子、斑馬魚內胚層發育
外文關鍵詞：	Zebrafish, Dorsal–ventral polarity, Mesendoderm specification, Gene regulatory network, Transcription regulation, Zebrafish endoderm development
相關次數：	點閱：2 下載：0
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The process of development is a result of cascades made by gene regulated interaction,
which operates mainly through the regulated expression of genes encoding transcription factors
and signaling pathways. In this thesis, I first integrated preexist bioinformatics data, combining
gene expression pattern from ZFIN website and the interrelationship between genes from
previous literatures. We established a database, and then constructed the genomic regulatory
networks in zebrafish embryogenesis by using BioTapestry. We focused on the endoderm
formation and dorsoanterior–ventroposterior patterning. This is the first part of this thesis.
In vertebrate development, the process of gastrulation leads to three germ layers: ectoderm,
endoderm, and mesoderm. The endoderm originates from the most marginal blastomeres of
blastula stage embryos in zebrafish (Danio rerio). The most important signaling molecule in the
endoderm formation is Nodal. Upon binding to its receptors, Nodal leads to the activation of
gata5, bon and og9x, which then activate sox32 to promote the expression of sox17 and activate
the endoderm differentiation. In the second part of this thesis, we established the subcircuits of
sox32 and sox17 using morpholinos against sox32 and sox17, measured certain gene expression
profiles by real time RT-PCR and validation by in situ hybridization. We identified several
interesting functional motifs that are important building blocks in zebrafish developmental gene
regulatory networks (GRNs). At the early stage, Sox32 and sox17 provide an autoregulatory lock
on the endodermal fate of cells. Early activation turns to late repression for Sox32 to sox32 itself,
and for Otx2 to sox17. Late transcription factors repress early activators: e.g., Gata5 activates
sox17 and then Sox17 represses gata5; Gbx1 activates sox32 and then Sox32 represses gbx1. We
found Sox32 and Sox17 repress many early transcription factors such as foxh1, and sox17
represses itself at a later stage. This interaction network extends from the two important
endoderm transcription factors and provides in-depth understanding of the complex regulatory
architecture in early embryonic development.
In the third part of this thesis, we further analyzed cis-regulatory element and directly tested
for the existence of functional modules. The sox17 gene is a key marker of endodermal cell in
the zebrafish. According to the predictions of the GRNs, based on perturbation experiment and
literature search, the sox17 gene is engaged with two other regulatory genes, sox32 and pou5f1,however the regulatory inputs of sox17 at the genomic sequence level are not known. I analyzed
the regulatory modules and transcription factor binding sites on the sox17 gene, and discovered
three evolutionary conserved region, A, B, and C, are positive regulatory modules with a
synergistic effect among them. I revealed the functionality for Pou5f1-transcription factor
binding site on the B module, and Sox32-transcription factor binding site on the C module, and
those two transcription factors work synergistically to positively regulate sox17. Furthermore, an
evolutionarily non-conserved R module exhibits a repressive effect on both the ventral and dorsal
side of the ectoderm. My research provides new insight into the complexity of endoderm
formation. This is the first elucidated node in the zebrafish endoderm GRN`s which has been
proved directly by their structural and functional relationships. It may serve as a landmark for
decipher the complete endoderm gene regulatory network.

發育過程是轉錄因子(transcription factors) 及訊號傳遞路徑(signaling pathways) 相
互作用的結果。在這份論文研究，首先我利用整合生物資訊的方法，結合ZFIN 基因表現
的資訊以及過去研究所產生出來的基因與基因之間關係的資料，統整成資料庫並建構出胚
胎發育調控網路，尤其是著重內胚層的發育及背腹的區別之基因調控網路，構成本論文的
第一部分。
在脊椎動物發育過程當中，經過原腸期(gastrulation) 分化出外胚層、內胚層和中胚
層，而在斑馬魚胚胎囊胚(blastula) 階段內胚層源自於胚葉細胞(blastomeres) 最邊緣。內
胚層形成中最重要的訊息分子是Nodal 訊號傳遞路徑，經由Nodal 與它的接受體(receptor)
結合之後活化gata5、bon 和og9x，然後活化sox32 進而促成sox17 的表現和內胚層的分
化(differentiation)。內胚層形成中最重要的轉錄因子為sox32 及sox17。因此為了清楚了解
這两個基因如何影響內胚層基因表現，第二部分的論文以實驗方法建立sox32 和sox17 次
調控網路(subcircuits)。我們使用嗎琳代低聚核甘酸(morpholinos oligonucleotides) 專一性
的抑制sox32 和sox17 基因的轉譯，然後利用即時定量聚合酶鏈反應(real time RT-PCR)
測量下游基因表現量的改變，並利用原位雜交(in situ hybridization)的方法驗證，以建立
sox32 和sox17 次調控網路(subcircuits)。其中我們發現許多在斑馬魚發育之基因調控網路
中重要的功能性群組。在早期的階段，sox32 和sox17 提供一個自我調控的循環位於將來
會分化成內胚層區域。Sox32 早期活化但是晚期卻抑制sox32 它自己，並且Otx2 早期活
化sox17 而晚期被Sox17 所抑制。另外還有一些相同調控的轉錄因子，如Gata5 早期活化
sox17 而晚期被Sox17 所抑制和Gbx1 早期活化sox32 而晚期被Sox32 所抑制。我們也發
現在晚期Sox32 和Sox17 會抑制早期的轉錄因子諸如foxh1，而Sox17 會抑制它自己。
Sox32 及Sox17 這兩個重要的轉錄因子所組成的次調控網路關係，讓我們對於胚胎發育過
程中複雜調控機制有了更深入的瞭解。
第三部分的論文進一步在斑馬魚的內胚層發育基因調控網路，直接證明關鍵的基因調
控之結構和功能性上的關係。在斑馬魚sox17 基因是一個內胚層細胞之關鍵性的標誌，根據來自於擾動實驗(perturbation experiment) 和文獻搜尋的基因調控網路，顯示Sox32 和
Pou5f1 這兩個重要的轉錄因子對於sox17 基因的調控扮演非常重要的角色，但在DNA 序
列層次上，sox17 基因同側調控元素(cis-regulatory elements)並不是很清楚。我分析sox17 的
調控模組（regulatory module）及基因調控子序列（transcription factor binding site），發現
sox17 基因上含有三個演化保守區域A、B、C，在功能上是具有協同作用的正調控模組。
並證明B 模組上含有Pou5f1 調控子序列，且C 模組上含有Sox32 調控子序列，而Pou5f1
和Sox32 互相作用對於正調控sox17 基因具有增效作用。此外，sox17 基因上非演化保守
區域R 模組具有抑制sox17 基因表現在腹側及背側外胚層的作用。我的研究對於內胚層形
成的複雜度提供一個新的見解，這是第一個斑馬魚的內胚層發育基因調控網路中，被研究
透徹的網點(node)，對於完整的內胚層基因調控網路的譯解具有指標性意義。

Contents
Contents 1
List of tables and figures 3
Abstract (Chinese) 6
Abstract (English) 8
Chapter 1 Introduction 10
1.1 Background 10
1.2 Gene regulatory networks in zebrafish development 10
1.3 Specific transcription factors and genomic regulatory code on endoderm
specification 12
1.4 Figures 16
Chapter 2 Developmental Gene Regulatory Networks of the Zebrafish Embryo 19
2.1 Summary 19
2.2 Introduction 20
2.3 Overview of the strategy to establish the GRN 20
2.4 Overview of the embryogenesis in zebrafish 24
2.5 Four signaling pathways and their components 26
2.6 The major developmental stages and territories 29
2.7 Network motifs of the zebrafish GRNs controlling anterior-posterior axis and
mesendodermal formation 29
2.8 Dorsal-ventral patterning 35
2.9 Endoderm formation 37
2.10 Tables 41
2.11 Figures 45
Chapter 3 The Endoderm Gene Regulatory Networks: Subcircuits of sox32 and sox17 in
Zebrafish Development 59
3.1 Abstract 59
3.2 Introduction 60

3.3 Material and methods 62
3.4 Result 64
3.5 Discussion 71
3.6 Tables 75
3.7 Figures 79
Chapter 4 Functional Analysis of the Evolutionarily Conserved Cis-Regulatory Elements on
the sox17 Gene in Zebrafish 95
4.1 Abstract 95
4.2 Introduction 96
4.3 Material and methods 98
4.4 Result 103
4.5 Discussion 113
4.6 Tables 118
4.7 Figures 121
Chapter 5 Conclusions and future perspective 136
5.1 Conclusions 136
5.2 Making more complete developmental networks in zebrafish 137
5.3 Comparing the sox32 mutant and MASO knockdown 138
5.4 The structure of Sox32 and Pou5f1 on DNA localization 138
5.5 Migration defect of the endodermal prcuror cell 139
5.6 Figures 140
References 143
Appendix: supplementary data 156

List of tables and figures
Chapter 1 Introduction
Figure 1 GRN for endomesoderm specification in sea urchin embryos. 16
Figure 2 Early blastula (stages 7.5–9) in Xenopus mesendoderm formation. 17
Figure 3 Nodal signal in endoderm development in zebrafish. 18
Chapter 2 Developmental Gene Regulatory Networks of the Zebrafish Embryo
Table 1. Interaction data for sox17 41
Table 2. Spatial and temporal expression data for sox17 extracted from ZFIN 43
Figure 1A. Lateral view of the embryo at late blastula/early gastrula stage, with
dorsoanterior to the right, ventroposterior to the left, vegetal to the bottom and the
animal pole at the top 45
Figure 1B. Lateral view of the embryo at late blastula/early gastrula stage, with the
derivatives of the three germ layers labeled 46
Figure 2. The major developmental stages and territories in zebrafish embryos are
shown as a chart with developmental time (in hours post–fertilization (hpf)) labeled
on the left 47
Figure 3A. Six lock-on systems 48
Figure 3B. Dorsal-ventral bistable toggle switch systems 49
Figure 3C. Mesendoderm motifs 50
Figure 4A. Gene networks that determine the dorsal-ventral axis at the dorsoanterior
side of cleavage stage embryos 51
Figure 4B. Gene networks that determine the D-V axis at the dorsoanterior side of
early gastrula stage embryos 52
Figure 4C. Gene networks that determine the dorsal-ventral axis at the dorsoanterior
side of the late gastrula stage embryo 53
Figure 4D. Gene networks that determine the dorsal-ventral axis at the ventroposterior
side of the cleavage stage 54
Figure 4E. Gene networks that determine the dorsal-ventral axis at the ventroposterior
side of the late gastrula stage embryos 55
Figure 5A. Early mesendoderm specification 56
Figure 5B. Zygotic mesoderm and endoderm transcription factors activated by Nodal 57
- 4 -
Figure 5C. View of the gene regulatory interactions in the endoderm 58
Chapter 3 The Endoderm Gene Regulatory Networks: Subcircuits of sox32 and sox17 in
Zebrafish Development
Table 1. The sequences of the primers u used in real time RT-PCR 75
Table 2. The sequences of the primers used for in situ hybridization 76
Table 3. Sox32 downstream target genes 77
Table 4. Sox17 downstream target genes 78
Figure 1. Expression profiles of three members of HMG family transcription factor 79
Figure 2. Morphology of sox32 and sox17 MO injected embryos 80
Figure 3. Sox32 activates endoderm-specific transcription factors at 5 hpf, 8 hpf and 11
hpf, and activates pax2a and pou1 at 11 hpf 81
Figure 4. Sox32 represses bon, og9x, and sox32 at later stages; it seems feedback loop
is to have a temporal peak of expression 83
Figure 5. Sox32 represses drl, gbx1, tbx16, gata6, and pou5f1 at a later stage in
different territory 84
Figure 6. Sox17 activates two endoderm-specific transcription factors, og9x and sox32
at 8 hpf, represses sox17 itself and the endoderm-specific transcription factor foxa1
after the expression peak of sox17 86
Figure 7. Sox17 represses some ectoderm transcription factors, including six3a, six3b,
etv5, etv6, trh3, and sox4b, and in different areas at 24 hpf 88
Figure 8. The transcription factors drl, foxh1, gata4, gata5, and gata6, expressed in
mesoderm are repressed by Sox17 at 24 hpf 90
Figure 9. The genes verified as sox32 upstream input at different developmental stages 92
Figure 10. The upstream inputs of sox17 are verified by gene-specific MO perturbation
screening during embryo development 93
Figure 11. The sox32 and sox17 subcircuit network is divided into different areas
during processing of the developmental stages 94
Chapter 4 Functional Analysis of the Evolutionarily Conserved Cis-Regulatory Elements on
the sox17 Gene in Zebrafish
Table 1. Summary of the GFP expression percentage of the injected embryos 118
- 5 -
Table 2. Summary of the GFP constructs at 50% epiboly 119
Table 3. Summary of the GFP expression of the constructs at four different stages 120
Figure 1. Sox17 Conserved genomic modules and GFP constructs in this study 121
Figure 2. GFP expression patterns of different cis-element constructs during late
blastula stage 123
Figure 3. Embryos injected with sox17 constructs have different GFP expression
patterns during the gastrula stage 124
Figure 4. Double fluorescent in-situ hybridization for egfp and endogenous genes 125
Figure 5. Quantitative analysis of sox17 cis-element regulatory regions with GFP
constructs and identification of the input on C-Bp-GFP 126
Figure 6. The genomic sequences of the A, B, and C modules of zebrafish sox17
compared with Tetraodon (A module), human (B module), and fugu (C module),
respectively 127
Figure 7. Identification of the Pou5f1 target site on the B module, and the Sox32 target
site on the C module 128
Figure 8. Functional analysis of transcription factor-binding sites by using
gene-specific MO perturbation with real time RT-PCR 130
Figure 9. Over expression pou5f1 or sox32 mRNA increased the expression level of
module B and C 132
Figure 10. In-vivo binding analysis of Sox32 on the sox17 cis-element verified by
chromatinimmunoprecipitation 133
Figure 11. Summary of the regulation of the zebrafish sox17 cis-element compared
with Xenopus sox17 135
Chapter 5 Conclusion and future perspective
Figure 1. Workflow overview of the wet-lab portion of a ChIP-on-chip experiment. 140
Figure 2. Schematic View of ChIP-PETAnalysis. 141
Figure 3. External abnormalities at the 38-h stage after injection of 226D7 MO. 142

                                

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