Specification and spatial arrangement of cells in the germline stem cell niche of the Drosophila ovary depend on the Maf transcription factor Traffic jam.

Specification and spatial arrangement of cells in the germline stem cell niche of the Drosophila ovary depend on the Maf transcription factor Traffic jam.
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DOI:
10.1371/journal.pgen.1006790
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发表时间:
2017-05
期刊:
影响因子:
4.5
通讯作者:
Godt D
Godt D
中科院分区:
生物学2区
文献类型:
--
作者:
Panchal T;Chen X;Alchits E;Oh Y;Poon J;Kouptsova J;Laski FA;Godt D

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果蝇卵巢中的生殖系干细胞由体细胞小生境维持。生态位是结构和功能复杂,包含四种细胞类型,护送,帽,和终端丝细胞和新发现的过渡细胞。我们发现大Maf转录因子Traffic Jam(Tj)对于确定小生境细胞命运和结构是必不可少的,使得卵巢中的每个小生境能够支持2-3个生殖系干细胞的正常补体。特别是,我们专注于帽细胞如何形成的问题。帽细胞表达Tj,被认为是成熟生殖系干细胞小生境的关键组成部分。我们的结论是,Tj控制帽细胞的规格,Tj功能的完全丧失导致额外的终端丝细胞的发展,在帽细胞的费用,和终端丝细胞开发帽细胞的特性时,诱导表达Tj。此外,我们提出,Tj控制帽细胞的形态发生行为,因为它们采用了终丝细胞的形状和空间组织,但在Tj表达仅部分减少时,似乎保留了它们的命运。我们的数据表明,Tj通过促进帽细胞的命运,有助于生殖系干细胞的建立,并通过调节生态位结构控制干细胞的承载能力的生态位。对Tj和Notch(N)通路之间相互作用的分析表明,Tj和N在帽细胞特化程序中具有不同的功能。我们建议,帽细胞的形成取决于Tj和N通路的联合活动,Tj通过阻断终丝细胞的命运来促进帽细胞的命运,N通过阻止护送细胞的命运和/或控制帽细胞前体的数量来支持帽细胞。干细胞的建立和维持往往依赖于相关的小生境细胞。果蝇卵巢生殖干细胞生态位是研究干细胞与生态位细胞相互作用的一个长期模型。然而,令人惊讶的是,人们对形成这种生态位的机制知之甚少,导致了不同生态位细胞类型的特化以及它们在干细胞周围的独特排列。Tj在生态位的不同细胞类型中以不同水平表达的观察促使我们询问这种转录因子对生态位的形成有何贡献。我们的数据表明,Tj的活动是需要的护送细胞的存在和帽细胞的正确规范,但似乎是在生殖系干细胞龛中的终末丝细胞的形成被忽视。此外,我们的分析表明,帽细胞命运的建立依赖于Tj和N信号通路之间的合作。我们的结论是,Tj调节生殖系干细胞的承载能力的小生境通过控制的命运和空间排列的小生境细胞。
Germline stem cells in the Drosophila ovary are maintained by a somatic niche. The niche is structurally and functionally complex and contains four cell types, the escort, cap, and terminal filament cells and the newly identified transition cell. We find that the large Maf transcription factor Traffic jam (Tj) is essential for determining niche cell fates and architecture, enabling each niche in the ovary to support a normal complement of 2–3 germline stem cells. In particular, we focused on the question of how cap cells form. Cap cells express Tj and are considered the key component of a mature germline stem cell niche. We conclude that Tj controls the specification of cap cells, as the complete loss of Tj function caused the development of additional terminal filament cells at the expense of cap cells, and terminal filament cells developed cap cell characteristics when induced to express Tj. Further, we propose that Tj controls the morphogenetic behavior of cap cells as they adopted the shape and spatial organization of terminal filament cells but otherwise appeared to retain their fate when Tj expression was only partially reduced. Our data indicate that Tj contributes to the establishment of germline stem cells by promoting the cap cell fate, and controls the stem cell-carrying capacity of the niche by regulating niche architecture. Analysis of the interactions between Tj and the Notch (N) pathway indicates that Tj and N have distinct functions in the cap cell specification program. We propose that formation of cap cells depends on the combined activities of Tj and the N pathway, with Tj promoting the cap cell fate by blocking the terminal filament cell fate, and N supporting cap cells by preventing the escort cell fate and/or controlling the number of cap cell precursors. Establishment and maintenance of stem cells often depends on associated niche cells. The germline stem cell niche of the Drosophila ovary has been a long-standing model for the analysis of the interactions between stem cells and niche cells. Surprisingly little is known, however, about the mechanisms that pattern this niche, leading to the specification of different niche cell types and to their distinct arrangement around the stem cells. The observation that Tj is expressed at different levels in the different cell types of the niche motivated us to ask what contribution this transcription factor makes to the formation of the niche. Our data suggest that Tj activity is needed for the presence of escort cells and for the correct specification of cap cells but appears to be dispensable for the formation of terminal filament cells in the germline stem cell niche. Moreover, our analysis indicates that the establishment of the cap cell fate depends on the cooperation between Tj and the N signaling pathway. We conclude that Tj regulates the germline stem cell carrying capacity of the niche by controlling the fate and the spatial arrangement of niche cells.