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Mechanisms of motor-independent membrane remodeling driven by dynamic microtubules

By Ruddi Rodríguez-García, Vladimir A. Volkov, Chiung-Yi Chen, Eugene A. Katrukha, Natacha Olieric, Amol Aher, Ilya Grigoriev, Magdalena Preciado López, Michel O. Steinmetz, Lukas C Kapitein, Gijsje Koenderink, Marileen Dogterom, Anna Akhmanova

Posted 27 Mar 2019
bioRxiv DOI: 10.1101/590869 (published DOI: 10.1016/j.cub.2020.01.036)

Microtubule-dependent organization of membranous organelles, such as the endoplasmic reticulum, occurs through motor-based pulling and by coupling microtubule dynamics to membrane remodeling. How highly transient protein-protein interactions occurring at growing microtubule tips can induce load-bearing processive motion is currently unclear. Here, we reconstituted membrane tubulation in a minimal system with giant unilamellar vesicles, dynamic microtubules, End-Binding (EB) proteins and a membrane-targeted protein that interacts with EBs and microtubules. We showed that these components are sufficient to drive membrane remodeling by three mechanisms: membrane tubulation by growing microtubule ends, motor-independent membrane sliding along microtubule shafts and pulling by shrinking microtubules. Experiments and modeling demonstrated that the first two mechanisms can be explained by adhesion-driven biased membrane spreading on microtubules. Force spectroscopy revealed that attachments to growing and shrinking microtubule ends can sustain forces of ∼0.5 and ∼5 pN, respectively. Rapidly exchanging molecules that connect membranes to dynamic microtubules can thus bear sufficient load to induce membrane deformation and motility.

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