Dataset Information

The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis.

ABSTRACT: Dynamic coupling of microtubule ends to kinetochores, built on the centromeres of chromosomes, directs chromosome segregation during cell division. Here, we report that the evolutionarily ancient kinetochore-microtubule coupling machine, the KMN (Knl1/Mis12/Ndc80-complex) network, plays a critical role in neuronal morphogenesis. We show that the KMN network concentrates in microtubule-rich dendrites of developing sensory neurons that collectively extend in a multicellular morphogenetic event that occurs during C. elegans embryogenesis. Post-mitotic degradation of KMN components in sensory neurons disrupts dendritic extension, leading to patterning and functional defects in the sensory nervous system. Structure-guided mutations revealed that the molecular interface that couples kinetochores to spindle microtubules also functions in neuronal development. These results identify a cell-division-independent function for the chromosome-segregation machinery and define a microtubule-coupling-dependent event in sensory nervous system morphogenesis.

SUBMITTER: Cheerambathur DK

PROVIDER: S-EPMC6436928 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis.

Cheerambathur Dhanya K DK Prevo Bram B Chow Tiffany-Lynn TL Hattersley Neil N Wang Shaohe S Zhao Zhiling Z Kim Taekyung T Gerson-Gurwitz Adina A Oegema Karen K Green Rebecca R Desai Arshad A

Developmental cell 20190228 6

Dynamic coupling of microtubule ends to kinetochores, built on the centromeres of chromosomes, directs chromosome segregation during cell division. Here, we report that the evolutionarily ancient kinetochore-microtubule coupling machine, the KMN (Knl1/Mis12/Ndc80-complex) network, plays a critical role in neuronal morphogenesis. We show that the KMN network concentrates in microtubule-rich dendrites of developing sensory neurons that collectively extend in a multicellular morphogenetic event tha ...[more]

PMID: 30827898

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Project description:Sensory filtering - prioritizing relevant stimuli while ignoring irrelevant ones - is crucial for animals to adapt and survive in complex environments. While this phenomenon has been primarily studied in organisms with complex nervous systems, it remains unclear whether simpler organisms also possess such capabilities. Here, we studied temporal information processing in Schmidtea mediterranea, a freshwater planarian flatworm with a primitive nervous system. Using long-term behavioral imaging and oscillatory ultraviolet (UV) light stimulations with rhythms matching the timescale of the animal's short-term memory (~minutes), we observed that planarians initially ignored rhythmic oscillations in UV intensity but eventually began tracking them after several cycles, demonstrating sensory filtering. We identified two neuropeptides, knockdown of which eliminated the initial ignoring phase and led to immediate stimulus-tracking, suggesting that these neuropeptides mediate an active sensory gating mechanism preventing response to transient fluctuations in stimuli. Notably, when UV stimulation was coupled with synchronous visible light oscillations, the planarians tracked the combined signals immediately, indicating that coherence across sensory modalities can override the initial gating. Our findings demonstrate that even simple nervous systems can filter temporal information and that this mechanism is mediated by neuropeptides. Unlike classical fast-acting small-molecule neurotransmitters, neuropeptides provide a slower, sustained, and global form of modulation that allows for more sophisticated control of sensory processing.Significance statementWe show that simple nervous systems can use specific neuropeptides to achieve sensory filtering, a behavior previously thought to require complex brain architecture. This neuropeptide-mediated sensory gating mechanism reveals a fundamental role for neuropeptides in temporal information processing, offering insights into the mechanistic and evolutionary origins of attention-like behaviors.

Dataset Information

The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis.

Publications

The Kinetochore-Microtubule Coupling Machinery Is Repurposed in Sensory Nervous System Morphogenesis.

Similar Datasets

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