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研究生:張傳慈
研究生(外文):Chuan-Chie Josephine Chang
論文名稱:Zswim基因家族Zswim5與Zswim6於小鼠前腦發育之分布與定性分析
論文名稱(外文):Characterization of the Zswim family genes, Zswim5 and Zswim6, in the developing mouse forebrain
指導教授:劉福清劉福清引用關係
指導教授(外文):Fu-Chin Liu
學位類別:碩士
校院名稱:國立陽明大學
系所名稱:神經科學研究所
學門:醫藥衛生學門
學類:醫學學類
論文種類:學術論文
論文出版年:2009
畢業學年度:97
語文別:英文
論文頁數:142
中文關鍵詞:Zswim5Zswim6前腦發育切線式遷移大腦皮層中間神經元紋狀體
外文關鍵詞:Zswim5Zswim6Forebrain developmentTangential migrationCortical interneuronStriatum
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中文摘要

在脊椎動物的前腦發育過程中,各種生長分子及轉錄因子會在特定的時間與位置,精確地調控神經之生成、分布及連結,構成調節高階腦功能的前腦。前腦又可分為終腦與間腦,前者是由背側的大腦皮層以及腹側的基底核及杏人核構成,負責智力、動作或特定情緒上之調控;後者則包含丘腦以及丘腦下部。研究調控因子之表現與功能是探索腦部正常發育之重要步驟。本論文藉由原位雜交的方式,將兩個Zswim family成員,Zswim5與Zswim6,在前腦發育過程中之表現區域做定性上的研究。在前腦發育初期E11.5至E13.5,Zswim5 mRNA主要高量表現在前腦腹側的medial ganglionic eminence (MGE) 之 subventricular zone (SVZ)中;而Zswim6 mRNA 則主要高量表現在MGE背外側之lateral ganglionic eminence (LGE)的SVZ中。在E15.5與E17.5之發育時期, Zswim5仍然明顯地表現在pallidum前驅構造 (MGE) 之SVZ中, 而Zswim6除了仍高量表現在紋狀體前驅構造 (LGE) 的SVZ外,亦同時在發育中的紋狀體,大腦皮質(neocortex)之cortical plate (CP) 和海馬回(hippocampus)中有著高量的表現。從出生至成鼠的階段,Zswim5在前腦的表現,較胚胎時期有顯著的降低。相反地,Zswim6則持續地表現在一些成熟的前腦構造中,例如: 紋狀體、大腦皮層、海馬回以及嗅球。相對於其他會表現Zswim6的前腦構造中,大腦皮層的Zswim6則在出生後14天,隨著發育成熟而降低其表現量。

除此以外,Zswim5與Zswim6亦表現在不同的神經前驅細胞族群中。首先,藉由與細胞分化標定分子Tuj1,或細胞增生標定分子Ki67之雙重原位雜交與免疫染色之結果發現,Zswim5與Zswim6均各自表現在進行分化中,而非仍在分裂增生狀態之前驅細胞中。另外,Zswim5亦與一些標定MGE中不同前驅細胞族群的神經標定分子做雙重染色定性上之分析,例如: Nkx2.1,Lhx6以及Lhx8。結果顯示,Zswim5確實表現在調控MGE發育之重要因子Nkx2.1的細胞族群中。另外,根據Zswim5與Lhx6表現於同一細胞,但並不與Lhx8共同表現之結果而論,推測Zswim5是屬於MGE前驅細胞中,會經過tangential migration而生成同樣具有Lhx6之大腦皮層GABAergic中間神經元的族群,而非表現於生成紋狀體cholinergic中間神經元的Lhx8-positive MGE前驅細胞族群中。與前述假設一致,Zswim5除了高量表現在MGE之SVZ,亦延伸其表現於LGE的SVZ以及neocortex之Intermediate zone(IZ)/SVZ的細胞中。而此表現之分布情況,則極相似於MGE前驅細胞,在生成大腦皮層GABAergic中間神經元的tangential migration所經之路徑。另一方面,Zswim6則與紋狀體投射神經元之標定分子Nolz-1的表現區域,亦即LGE之SVZ,有顯著的重疊。然而,在LGE/SVZ最背側區域的Zswim6-positive細胞則無Nolz-1表現。因此,Zswim6進一步與標示LGE最背側以及生成嗅球中間神經元的之前驅細胞的標定分子Er81,做雙重染色定性分析。結果顯示,縱然Zswim6確實表現在Er81表現之區域,然而單一細胞分析顯示,Zswim6並不表現在Er81-positive之細胞族群中。以上結果推測,Zswim6雖會表現在嗅球細胞中,但可能並不參與在嗅球中間神經元之生成。最後,藉由雙重原位雜交之方式,發現在中段(*p < 0.05)以及後段(**p < 0.001)的成熟紋狀體中,Zswim6較多表現在具有D2多巴胺接受器之投射神經元細胞族群中,而較少表現在具D1多巴胺接受器的投射神經元細胞族群中。

綜合而論,本論文發現Zswim5與Zswim6雖隸屬於同一基因家族,然而兩者在前腦的胚胎發育時期或出生後之表現量及分布位置極為不同。其中,Zswim5在胚胎時期之表現區域主要分佈在前腦的MGE/SVZ,又其可能參與在形成大腦皮層之GABAergic中間神經元的生成過程中。然而,此推測仍需將Zswim5與一些中間神經元之標定分子做定性分析後才能確認。而在胚胎時期,最主要表現在前腦之LGE/SVZ的Zswim6,則有可能參與在紋狀體投射神經元之發育過程,或在成熟時期參與紋狀體一般機制的調控。
Abstract

During development, various morphogenetic molecules and transcription factors regulate the formation, distribution, and connections of neurons under specific time and place, constituting the forebrain that regulates high-level brain functions. The forebrain is divided into the telencephalon and the diencephalon. Telencephalon is composed of the dorsally located cerebral cortex and the ventrally located basal ganglia and amygdale. These are brain regions responsible for organizing the highest intellectual functions, the motions, and certain types of emotion behaviors. Diencephalon contains thalamus and hypothalamus. Investigating the expression pattern and functions of the regulatory molecules in the brain is a crucial step for understanding the normal brain development. In my thesis study, in situ hybridization was used to explore the expression patterns of two previously uncharacterized Zswim gene family members, Zswim5 and Zswim6, during forebrain development. In the early forebrain development from E11.5 to E13.5, strong expression of Zswim5 mRNA was mainly detected in the subventricular zone (SVZ) of the medial ganglionic eminence (MGE) of the ventral forebrain, whereas strong expression of Zswim6 mRNA was mainly found in the SVZ of lateral ganglionic eminence (LGE) dorsally to the MGE. At E15.5 and E17.5, prominent expression of Zswim5 remained detectable in the SVZ of the pallidal primordium (MGE), however, Zswim6 remained its high expression level not only in the SVZ of the striatal primordium (LGE), but was also detected in some developing structures of the forebrain, such as striatum, the cortical plate (CP) of neocortex, hippocampus and olfactory bulb. From neonatal to adult stages, Zswim5 expression in the forebrain was found drastically decreased comparing to embryonic stages. On the contrary, Zswim6 was found persistently expressed in the mature forebrain, including striatum, cortex, hippocampus, and olfactory bulb. Among these brain regions, Zswim6 was relatively down-regulated in the cortex after P14.

In addition, distinct neuronal progenitor populations express Zswim5 or Zswim6. Based on the results of double in situ hybridization/immunohistochemistry of Zswim5 and Zswim6 with the differentiation marker Tuj1 or the proliferation marker KI67, both Zswim5 and Zswim6 were likely to express in the differentiating but not the proliferating progenitors. Zswim5 was characterized with some MGE markers that specify different progenitor populations, such as Nkx2.1, Lhx6, and Lhx8. The results suggested that Zswim5 was expressed in the Nkx2.1-positive population, which plays essential roles in MGE development. In addition, as Zswim5 was found co-localized with Lhx6 but not Lhx8, we speculate that Zswim5 might be expressed in the MGE progenitors that undergo tangential migration to form cortical Lhx6-positive GABAergic interneurons instead of those Lhx8-positive progenitors that are involved in forming striatal cholinergic interneurons. Consistent with this hypothesis, In addition to the strong expression in the SVZ of MGE, Zswim5 expression was further extended up into the SVZ of LGE and the intermediate zone/subventricular zone (IZ/SVZ) of the developing neocortex. This pattern is similar to the tangential migratory pathway of GABAergic interneurons from the MGE to the cerebral cortex. On the other hand, the expression region of Zswim6 and the stiratal projection neuron marker Nolz-1 was found to highly overlapp in the SVZ of the LGE. However, Zswim6-positive progenitors in the dorsal-most part of the SVZ of LGE were not found to co-express Nolz-1. Therefore, Zswimi6-positive cells in the dorsal-most part of the LGE/SVZ were further characterized with the marker Er81, which not only is the marker of dorsal LGE, but also marks the progenitor cells that form olfactory bulb interneurons. The results showed that although Zswim6 was found to express in the Er81-positive region, however, at the single cell level, Zswim6 was not found to express in Er81-positive cells. These findings suggest that Zswim6 is not expressed in the progenitors of the olfactory bulb interneurons during development, despite that Zswim6 was found to express in the olfactory bulb. Finally, by double labeling of Zswim6 and dopamine D1 receptor (D1R) or D2 receptor (D2R), I found that Zswim6 was co-localized in D2R-positive striatal projection neurons at a higher incident rate than that in the D1R-positive striatal neurons, especially at the middle (D2R/Zswim6 v.s D1R/Zswim6, 60.29% ± 1.56% v.s 53.99% ± 2.07%, *p < 0.05) and caudal (D2R/Zswim6 v.s D1R/Zswim6, 62.73% ± 1.46% v.s 50.98% ± 2.42%, **p < 0.001) levels of the striatum in adulthood.

In summary, although Zswim5 and Zswim6 belong to the same gene family, they show distinctive expression patterns in the forebrain during embryonic and postnatal stages. Zswim5 mRNA was mainly found in the SVZ of the MGE during embryonic stages, and it might be involved in the formation of cortical GABAergic interneurons. This possibility requires further validation by double labeling of Zswim5 and markers of cortical BABAergic interneurons. In contrast, Zswim6 mRNA was mainly detected in the SVZ of the LGE, it is possible that Zswim6 may play a role in generation of striatal projection neuron during development, or participate in regulating normal striatal functions in the mature stage.
TABLE OF CONTENTS

ABSTRACT 1-2

ABSTRACT (IN CHINESE) 3

CHAPTERI INTRODUCTION 4-18

1.1 FOREBRAIN.....................................4
1.2 TRANSIENT STRUCTURES IN THE SUBPALLIUM DURING
DEVELOPMENT...................................5
1.3 NEUROGENESIS IN THE TELENCEPHALON.............8
1.4 FROM THE SUBPALLIUM TO THE BASAL GANGLIA.....10
1.5 FROM THE PALLIUM TO THE CEREBRAL CORTEX......12
1.6 THE ZSWIM FAMILY.............................13

CHAPTER 2 MATERIALS AND METHODS 19-28

2.1 ANIMALS......................................19
2.2 THE TEMPLATE PLASMIDS USED FOR PROBE SYNTHESIS 20
2.3 IN SITU HYBRIDIZATION........................21
2.4 IMMUNOHISTOCHEMISTRY (IHC)...................26

CHAPTER 3 RESULTS 29-50

3.1 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN E11.5
FOREBRAIN....................................29
3.2 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN E12.5
FOREBRAIN....................................32
3.3 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN E13.5
FOREBRAIN....................................38
3.4 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN E15.5
FOREBRAIN....................................41
3.5 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN E17.5
FOREBRAIN....................................43
3.6 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN P0
FOREBRAIN....................................45
3.7 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN P7
FOREBRAIN....................................46
3.8 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN P14
FOREBRAIN....................................47
3.9 CHARACTERIZTION OF ZSWIM5 AND ZSWIM6 IN ADULT BRIAN 48

CHAPTER 4 DISCUSSION 51-64

4.1 METHODOLOGY................................51
4.2 CHARACTERIZATION OF ZSWIM5.................52
4.3 CHARACTERIZATION OF ZSWIM6.................57
4.4 EVOLUTIONARILY CONSERVED ZSWIM5 AND ZSWIM6.61
4.5 FUTURE DIRECTIONS..........................63

REFERENCES 65-72

FIGURES 73-133

TABLES 134-138

APPENDIX 139-142
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