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系統識別號 U0026-0507201311075400
論文名稱(中文) NRF-1所調控的新基因在神經突生長的不同功能
論文名稱(英文) Novel Genes that Are Regulated by NRF-1 and Have Differential Functions in Neurite Outgrowth
校院名稱 成功大學
系所名稱(中) 基礎醫學研究所
系所名稱(英) Institute of Basic Medical Sciences
學年度 101
學期 2
出版年 102
研究生(中文) 王仁伶
研究生(英文) Jen-Ling Wang
電子信箱 nohxo@yahoo.com.tw
學號 S58961549
學位類別 博士
語文別 英文
論文頁數 129頁
口試委員 指導教授-黃阿敏
口試委員-張玲
口試委員-黃朝慶
口試委員-許桂森
口試委員-簡正鼎
口試委員-陳志成
中文關鍵字 核內呼吸因子  神經纖維母細胞瘤細胞株  初代海馬迴神經細胞  神經突生長  軸突和樹突生長  生物資訊 
英文關鍵字 nuclear respiratory factor-1  neuroblastoma cells  primary hippocampal neurons  neurite outgrowth  axonal and dendritic outgrowth  bioinformatics 
學科別分類
中文摘要 核內呼吸因子NRF-1是人類基因體中重要的轉錄因子,可促進人類神經纖維母細胞瘤的神經突生長。神經突的生長是神經發育與神經再生的重要步驟,研究發現許多分子參與神經突生長的調控。然而轉錄因子NRF-1如何調控神經突生長仍屬未知。此研究利用生物資訊工具來搜尋NRF-1的下游基因,並探討NRF-1是否透過不同的下游基因群來調控神經突生長。本研究第一部分針對已知的synapsin I,探討其是否受到NRF-1調控,並參與NRF-1調控神經分化的過程。以EMSA、ChIP、site-directed mutagenesis和啟動子的實驗證實NRF-1是調控synapsin I重要的轉錄因子,且NRF-1的大量表現會增加synapsin I mRNA和蛋白質的表現量。藉由synapsin I的反向序列抑制NRF-1所促進神經突生長的現象,證實synapsin I確實為NRF-1調控神經分化的關鍵基因之一。為了進一步了解NRF-1調控神經突生長的分子網路,於本篇研究的第二部分利用生物資訊工具來搜尋NRF-1的下游基因,發現啟動子含NRF-1辨識序列的人類基因多達916個,其中包含691個已註解和225個假設性基因(hypothetical gene)。此部分針對分別來自五個不同生物過程的基因群: (1)細胞週期: MAPRE3、NPDC1、SUV39H2、SKA3; (2)運輸作用: RAB3IP、TRAPPC3 ; (3)訊息傳遞: SMAD5、PIP5K1A、USP10、SPRY4 ; (4)轉錄作用: NR1D1、GTF2F2; (5)調控GTPase活性: RHOA、RAPGEF6、SMAP1的15個已註解基因進行研究。我們證實12個已註解基因會受到NRF-1調控,其中10個基因參與NRF-1所調控人類神經纖維母細胞瘤的神經突生長。第三部分探討NRF-1是否可藉由假設性基因FAM134C、C3orf10和ENOX1調控神經突生長。藉由EMSA、ChIP、site-directed mutagenesis和啟動子的研究等實驗方式進行確認測試,結果顯示在人類神經瘤母細胞株與大鼠初代大腦皮層的神經細胞培養中,FAM134C和ENOX1的基因表達受到NRF-1正向調控,而 C3orf10基因則受到NRF-1反向調控。此外,透過核酸干擾和大量表現全長基因的正反雙向基因表現作為差異性比對分析實驗,結果顯示FAM134C正向調控神經突生長,C3orf10反向調控神經突生長,至於ENOX1則不會影響神經突的生長。實驗進一步分析大鼠初代海馬迴神經細胞發育時期中,Fam134c大量表達在軸突軸丘,而C3orf10廣泛地表達在細胞本體、軸突和樹突,意味著這些基因可能參與調控神經細胞軸突與樹突發育。透過核酸干擾和大量表現全長基因表現實驗,結果發現Fam134c正向調控軸突長度,而C3orf10則會負向調控樹突與軸突分支的數目。本研究發現NRF-1可以藉由調控細胞週期、運輸作用、訊息傳遞、轉
錄作用、GTPase活性等基因群,也可藉由調控假設性基因來正向或負向調控神經突生長,意味著NRF-1可透過不同生物過程來影響神經分化。
英文摘要 Nuclear respiratory factor-1 (NRF-1) is a major transcription factor in the human genome and plays a key role in neurite outgrowth in human neuroblastoma IMR-32 cells. Neurite outgrowth is a critical process in neuronal development, and many genes are involved in this well-regulated process. However, how NRF-1 regulates neurite outgrowth is still unclear. In this study, we used bioinformatic tools to search for genes downstream from NRF-1 and hypothesized that these genes mediate NRF-1 function in neurite outgrowth in neurons.
In the first part of this study, we hypothesized that synapsin I is downstream of NRF-1 and mediates its function in neurite outgrowth. Synapsin I protein is a well-known phosphoprotein in neuronal terminals and has been implicated in neuronal differentiation. Human synapsin I gene promoter has a putative NRF-1 response element (NRE), but it is not known whether this NRE is functional. Gel electrophoretic mobility shift assays (EMSA), chromatin immunoprecipitation (ChIP), site-directed mutagenesis, and promoter studies indicated that NRF-1 is a positive regulator of synapsin I promoter. Exogenous NRF-1 overexpression increased synapsin I protein levels in IMR-32 and HEK293T cells. Down-regulating synapsin I expression markedly decreased the percentage of neurite-bearing cells and the average length of the longest neurites in IMR-32 cells that stably or transiently overexpressed NRF-1. We confirmed that the human synapsin I gene is positively regulated by NRF-1 and mediates the function of NRF-1 in neurite outgrowth.
In the second part, genome-wide analyses have identified that 916 genes in the human genome are potential NRF-1-regulated genes, including 691 annotated and 225 hypothetical genes. Fifteen annotated genes from different biological processes, cell cycle-related genes- MAPRE3, NPDC1, SUV39H2, SKA3, transport-related genes- RAB3IP, TRAPPC3, signal transduction-related genes- SMAD5, PIP5K1A, USP10, SPRY4, transcription-related genes- GTF2F2, NR1D1, and regulation of GTPase activity-related genes- RHOA, RAPGEF6, SMAP1, were selected for biological confirmation. EMSA and ChIP confirmed that all NREs of these fifteen genes are critical for NRF-1 binding. Quantitative RT-PCR demonstrated that mRNA levels of 12 of these genes are regulated by NRF-1. Overexpression or knockdown of candidate genes demonstrated that MAPRE3, NPDC1, SMAD5, USP10, SPRY4, GTF2F2, SKA3, RAPGEF6 positively regulated, and RHOA and SMAP1 negatively regulated neurite outgrowth. In this part, we have confirmed that 12 annotated genes are regulated by NRF-1 and 10 of them mediate NRF-1 function in neurite outgrowth in IMR-32 cells.
In the third part, we focused on three hypothetical genes, FAM134C, C3orf10, and ENOX1, and determine whether these hypothetical genes mediate NRF-1 function in neurite outgrowth in IMR-32 cells and primary hippocampal neurons. We found that NRF-1 positively regulated FAM134C and ENOX1, but negatively regulated C3orf10 in IMR-32 cells and primary rat cortical neurons. FAM134C positively regulates and C3orf10 negatively regulates neurite outgrowth, but ENOX1 plays no role in neurite outgrowth regulation. FAM134C and C3orf10 mediates NRF-1-enhanced neurite outgrowth. In primary rat hippocampal neurons, Fam134c is predominantly expressed in the axon hillock and C3orf10 is ubiquitously expressed in all neurites and cell bodies at different developmental stages, suggesting their roles in axonal and dendritic outgrowth. Fam134c positively regulates axonal length, but C3orf10 negatively regulates the number of axonal collaterals and dendrites. In the third part, we annotated FAM134C, C3orf10, and ENOX1 as NRF-1-regulated genes, which have differential effects on neurite outgrowth in neuroblastoma cells as well as neurons. Overall, we found that NRF-1 regulates neurite outgrowth through cell cycle-, transport-, signal transduction-, transcription-, regulation of GTPase activity-related genes and hypothetical genes, which suggest that NRF-1 regulates neuronal differentiation through a variety of biological processes.
Keywords: nuclear respiratory factor-1; neuroblastoma cells; primary hippocampal neurons; neurite outgrowth; axonal and dendritic outgrowth; bioinformatics.
論文目次 Contents
I. Introduction 1
1.1. Nuclear respiratory factor 1 (NRF-1) 1
1.1.1 The neuronal function of NRF-1 1
1.2. Physiological importance of neurite outgrowth 2
1.3. The molecules of different biological processes are involved in neurite outgrowth 3
1.3.1 Molecules involved in cytoskeleton organization 3
1.3.2 Molecules involved in membrane trafficking and transport 4
1.3.3 Molecules involved in cell cycle 4
1.3.4 Molecules involved in signal transduction 5
1.3.5 Molecules involved in transcriptional regulation 6
1.4 Genome-wide screening of NRE-containing genes in neurite outgrowth 7
1.5. The annotated genes which contain NRE in their promoter regions 8
1.5.1. SYN1 (synapsin I) 8
1.5.2. RAB3IP (RAB3A interacting protein) 8
1.5.3. TRAPPC3 (trafficking protein particle complex 3) 9
1.5.4. MAPRE3 (microtubule-associated protein, RP/EB family, member 3) 9
1.5.5. NPDC1 (neural proliferation, differentiation and control, 1) 10
1.5.6. SUV39H2 (suppressor of variegation 3-9 homolog 2) 10
1.5.7. SKA3 (spindle and kinetochore associated complex subunit 3) 11
1.5.8. SMAD5 (SMAD family member 5) 11
1.5.9. PIP5K1A (phosphatidylinositol-4-phosphate 5-kinase, type I, alpha) 11
1.5.10. USP10 (ubiquitin specific peptidase 10) 12
1.5.11. SPRY4 (sprouty homolog 4 (Drosophila)) 12
1.5.12. NR1D1 (nuclear receptor subfamily 1, group D, member 1) 13
1.5.13. GTF2F2 (general transcription factor IIF, polypeptide 2, 30kDa) 13
1.5.14. RHOA (ras homolog family member A) 14
1.5.15. RAPGEF6 (Rap guanine nucleotide exchange factor (GEF) 6) 14
1.5.16. SMAP1 (small ArfGAP 1) 15
1.6. The hypothetical genes which contain NRE in their promoter regions 15
1.6.1. FAM134C (Family with sequence similarity 134, member C) 15
1.6.2. C3orf10 (chromosome 3 open reading frame 10) 15
1.6.3. ENOX1 (ecto-NOX disulfide-thiol exchanger 1) 16
1.7. Hypothesis 17
1.8. Specific aims 17
II. Materials and methods 18
2.1. Cell cultures 18
2.2. Gel Electrophoretic Mobility Shift Assays (EMSA) 18
2.3. Chromatin immunoprecipitation (ChIP) Assay 20
2.4. Plasmid constructs 21
2.5. Lentiviral gene transfer 22
2.6. Transient transfection and dual-luciferase assay 24
2.7. Semi-quantitative RT-PCR 25
2.8. Western blot analysis 25
2.9. Quantitative real-time PCR (qPCR) 26
2.10. Primary hippocampal and cortical neuronal cultures 26
2.11. Immunocytochemistry 27
2.12. Measuring neurite outgrowth in IMR-32 cells 27
2.13. Measuring axonal and dendritic outgrowth in primary rat hippocampal neurons 27
2.14. Bioinformatic analysis 28
2.15. Statistical analysis 29
III. Results 30
Part I - Human Synapsin I Mediates the Function of Nuclear Respiratory Factor-1 in Neurite Outgrowth in Neuroblastoma IMR-32 cells 30
3.1. NRF-1 regulates human synapsin I promoter 30
3.2. NRF-1 regulates synapsin I mRNA and protein expression 31
3.3. Serum deprivation increases DNA binding of NRF-1 to the synapsin I NRE 32
3.4. Serum deprivation induces alternating synapsin I protein expression 32
3.5. Antisense synapsin I cDNA reduces neurite outgrowth in neuroblastoma cells 33
3.6. Antisense synapsin I cDNA inhibits the neurite outgrowth induced by NRF-1 33
Part II - Novel Genes that mediate NRF-1-regulated Neurite Outgrowth in Neuroblastoma IMR-32 Cells 35
3.7. Genome-wide analysis of human genes containing putative NRE in the promoter regions 35
3.8. NRF-1 binds to the NREs of 15 annotated genes in vitro and in vivo 36
3.9. NRF-1 positively regulates MAPRE3, NPDC1, SKA3, RAB3IP, SMAD5, USP10, SPRY4, and RAPGEF6, and negatively regulates NR1D1, GTF2F2, RHOA, and SMAP1 genes 36
3.10. Overexpression of MAPRE3, NPDC1, and SMAD5, but not RAB3IP, mediate NRF-1-regulated neurite outgrowth in human neuroblastoma IMR-32 cells 37
3.11. Knockdown of USP10, SPRY4, GTF2F2, SKA3 or RAPGEF6 decreased and knockdown of RHOA and SMAP1 increased NRF-1-regulated neurite outgrowth in neuroblastoma IMR-32 cells 38
Part III - Novel Genes FAM134C, C3orf10, and ENOX1 Are Regulated by NRF-1 and Differentially Regulate Neurite Outgrowth in Neuroblastoma Cells and Hippocampal Neurons 40
3.12. NRF-1 positively regulates FAM134C and ENOX1, and negatively regulates C3orf10 in human neuroblastoma IMR-32 cells and primary rat cortical neurons 40
3.13. Serum deprivation increases DNA binding of NRF-1 to the NREs of FAM134C, C3orf10, and ENOX1 genes 42
3.14. FAM134C positively regulates, C3orf10 negatively regulates, but ENOX1 does not regulate neurite outgrowth in IMR-32 cells 42
3.15. FAM134C and C3orf10 mediates NRF-1-regulated neurite outgrowth in IMR-32 cells 44
3.16. FAM134C is a predicted transmembrane protein and colocalized with the markers of Golgi apparatus in IMR-32 cells 45
3.17. Other members of the SCAR/WAVE complex are also bound and regulated by NRF-1 45
3.18. Expression profiles of rat Nrf-1, Fam134c, and C3orf10 in hippocampus tissues and primary hippocampal neurons at different developmental stages 46
3.19. Fam134c and C3orf10 have differential roles in axonal and dendritic outgrowth in primary rat hippocampal neurons 48
IV. Discussion 50
4.1. Major findings - Identifying of novel genes that are regulated by NRF-1 and involved in neurite outgrowth 50
4.2. NRF-1 is a critical positive regulator of synapsin I 50
4.3. Synapsin I mediates NRF-1 function in neurite outgrowth 52
4.4. Genome-wide searching for NRF-1 downstream genes which involved in different biological processes 53
4.5. Genes involved in cell cycle mediate NRF-1-regulated neurite outgrowth 54
4.6. Genes involved in transcriptional regulation mediate NRF-1-regulated neurite outgrowth 54
4.7. Genes involved in signal transduction mediate NRF-1-regulated neurite outgrowth 55
4.8. Genes involved in the regulation of GTPase activity mediate NRF-1-regulated neurite outgrowth 55
4.9. NRF-1-regulated neurite outgrowth is a workable platform to annotate novel genes 56
4.10. FAM134C is positively regulated by NRF-1 56
4.11. FAM134C positively regulates neurite outgrowth in human neuroblastoma cells and primary rat hippocampal neurons 57
4.12. C3orf10 is negatively regulated by NRF-1 58
4.13. C3orf10 negatively regulates neurite outgrowth in human neuroblastoma cells and primary rat hippocampal neurons 59
4.14. ENOX1 is positively regulated by NRF-1 and has no effect on neurite outgrowth 60
V. Conclusion 61
VI. References 62
VII. Tables 78
VIII. Figures 92
IX. Appendix 127
X. Publications 129
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