Biehl Matthew J, Raetzman Lori T
Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
Dev Biol. 2015 Oct 15;406(2):235-46. doi: 10.1016/j.ydbio.2015.08.016. Epub 2015 Aug 28.
The mammalian arcuate nucleus (ARC) houses neurons critical for energy homeostasis and sexual maturation. Proopiomelanocortin (POMC) and Neuropeptide Y (NPY) neurons function to balance energy intake and Kisspeptin neurons are critical for the onset of puberty and reproductive function. While the physiological roles of these neurons have been well established, their development remains unclear. We have previously shown that Notch signaling plays an important role in cell fate within the ARC of mice. Active Notch signaling prevented neural progenitors from differentiating into feeding circuit neurons, whereas conditional loss of Notch signaling lead to a premature differentiation of these neurons. Presently, we hypothesized that Kisspeptin neurons would similarly be affected by Notch manipulation. To address this, we utilized mice with a conditional deletion of the Notch signaling co-factor Rbpj-κ (Rbpj cKO), or mice persistently expressing the Notch1 intracellular domain (NICD tg) within Nkx2.1 expressing cells of the developing hypothalamus. Interestingly, we found that in both models, a lack of Kisspeptin neurons are observed. This suggests that Notch signaling must be properly titrated for formation of Kisspeptin neurons. These results led us to hypothesize that Kisspeptin neurons of the ARC may arise from a different lineage of intermediate progenitors than NPY neurons and that Notch was responsible for the fate choice between these neurons. To determine if Kisspeptin neurons of the ARC differentiate similarly through a Pomc intermediate, we utilized a genetic model expressing the tdTomato fluorescent protein in all cells that have ever expressed Pomc. We observed some Kisspeptin expressing neurons labeled with the Pomc reporter similar to NPY neurons, suggesting that these distinct neurons can arise from a common progenitor. Finally, we hypothesized that temporal differences leading to premature depletion of progenitors in cKO mice lead to our observed phenotype. Using a BrdU birthdating paradigm, we determined the percentage of NPY and Kisspeptin neurons born on embryonic days 11.5, 12.5, and 13.5. We found no difference in the timing of differentiation of either neuronal subtype, with a majority occurring at e11.5. Taken together, our findings suggest that active Notch signaling is an important molecular switch involved in instructing subpopulations of progenitor cells to differentiate into Kisspeptin neurons.
哺乳动物的弓状核(ARC)包含对能量稳态和性成熟至关重要的神经元。阿黑皮素原(POMC)和神经肽Y(NPY)神经元的功能是平衡能量摄入,而 kisspeptin 神经元对青春期的开始和生殖功能至关重要。虽然这些神经元的生理作用已经得到充分证实,但其发育过程仍不清楚。我们之前已经表明,Notch 信号通路在小鼠ARC的细胞命运中起重要作用。活跃的 Notch 信号通路可阻止神经祖细胞分化为进食回路神经元,而 Notch 信号通路的条件性缺失则导致这些神经元过早分化。目前,我们假设 kisspeptin 神经元同样会受到 Notch 操纵的影响。为了解决这个问题,我们利用了条件性缺失 Notch 信号辅助因子Rbpj-κ(Rbpj cKO)的小鼠,或在发育中的下丘脑表达Nkx2.1的细胞中持续表达Notch1细胞内结构域(NICD tg)的小鼠。有趣的是,我们发现在这两种模型中,都观察到 kisspeptin 神经元缺失。这表明 Notch 信号通路必须进行适当调节才能形成 kisspeptin 神经元。这些结果使我们推测,ARC的 kisspeptin 神经元可能起源于与NPY神经元不同的中间祖细胞谱系,并且 Notch 负责这些神经元之间的命运选择。为了确定ARC的 kisspeptin 神经元是否通过POMC中间神经元以类似方式分化,我们利用了一种遗传模型,该模型在所有曾经表达过POMC的细胞中表达tdTomato荧光蛋白。我们观察到一些表达 kisspeptin 的神经元被POMC报告基因标记,类似于NPY神经元,这表明这些不同的神经元可能起源于共同的祖细胞。最后,我们推测导致cKO小鼠祖细胞过早耗尽的时间差异导致了我们观察到的表型。使用BrdU出生时间标记范式,我们确定了在胚胎第11.5、12.5和13.5天出生的NPY和 kisspeptin 神经元的百分比。我们发现这两种神经元亚型的分化时间没有差异,大多数在e11.5时发生。综上所述,我们的研究结果表明,活跃的 Notch 信号通路是一个重要的分子开关,参与指导祖细胞亚群分化为 kisspeptin 神经元。