Optogenetic control of cAMP oscillations reveals frequency-selective transcription factor dynamics in Dictyostelium.

IF 3.7 2区生物学 Q1 DEVELOPMENTAL BIOLOGY

Development Pub Date : 2025-01-01 Epub Date: 2025-01-14 DOI:10.1242/dev.204403

Kensuke Yamashita, Kazuya Shimane, Tetsuya Muramoto

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Abstract

Oscillatory dynamics and their modulation are crucial for cellular decision-making; however, analysing these dynamics remains challenging. Here, we present a tool that combines the light-activated adenylate cyclase mPAC with the cAMP biosensor Pink Flamindo, enabling precise manipulation and real-time monitoring of cAMP oscillation frequencies in Dictyostelium. High-frequency modulation of cAMP oscillations induced cell aggregation and multicellular formation, even at low cell densities, such as a few dozen cells. At the population level, chemotactic aggregation is driven by modulated frequency signals. Additionally, modulation of cAMP frequency significantly reduced the amplitude of the shuttling behaviour of the transcription factor GtaC, demonstrating low-pass filter characteristics capable of converting subtle oscillation changes, such as from 6 min to 4 min, into gene expression. These findings enhance our understanding of frequency-selective cellular decoding and its role in cellular signalling and development.

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cAMP振荡的光遗传学控制揭示了盘齿骨菌频率选择性转录因子动力学。

振荡动力学及其调制对细胞决策至关重要；然而，分析这些动态仍然具有挑战性。在这里，我们提出了一种结合光激活腺苷酸环化酶mPAC和cAMP生物传感器Pink Flamindo的工具，能够精确地操纵和实时监测Dictyostelium中的cAMP振荡频率。cAMP振荡的高频调制诱导细胞聚集和多细胞形成，即使在低细胞密度，如几十个细胞。在种群水平上，趋化聚集是由调制频率信号驱动的。此外，cAMP频率的调制显著降低了GtaC转录因子穿梭行为的幅度，显示出低通滤波器特性，能够将微妙的振荡变化（如6到4分钟）转化为基因表达。这些发现增强了我们对频率选择性细胞解码及其在细胞信号传导和发育中的作用的理解。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Development 生物-发育生物学

CiteScore

6.70

自引率

4.30%

发文量

433

审稿时长

3 months

期刊介绍： Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.