Actin nucleator formins regulate the tension-buffering function of caveolin-1

Author:

Shi Xuemeng12ORCID,Tang Daijiao34,Xing Yifan45,Zhao Shuangshuang12,Fan Changyuan34,Zhong Jin45,Cui Yanqin12,Shi Kun12ORCID,Jiu Yaming1234ORCID

Affiliation:

1. The Joint Program in Infection and Immunity, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangzhou 510623, China

2. The Joint Program in Infection and Immunity, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China

3. Unit of Cell Biology and Imaging Study of Pathogen Host Interaction, The Center for Microbes, Development and Health, CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China

4. College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China

5. Unit of Viral Hepatitis, CAS Key Laboratory of Molecular Virology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China

Abstract

Abstract Both the mechanosensitive actin cytoskeleton and caveolae contribute to active processes such as cell migration, morphogenesis, and vesicular trafficking. Although distinct actin components are well studied, how they contribute to cytoplasmic caveolae, especially in the context of mechano-stress, has remained elusive. Here, we identify two actin-associated mobility stereotypes of caveolin-1 (CAV-1)-marked intracellular vesicles, which are characterized as ‘dwelling’ and ‘go and dwelling’. In order to exploit the reason for their distinct dynamics, elongated actin-associated formin functions are perturbed. We find drastically decreased density, increased clustering, and compromised motility of cytoplasmic CAV-1 vesicles resulting from lacking actin nucleator formins by both chemical treatment and RNA silencing of formin genes. Furthermore, hypo-osmosis-stimulated diminishing of CAV-1 is dramatically intensified upon blocking formins. The clustering of CAV-1 vesicles when cells are cultured on soft substrate is also aggravated under formin inhibition condition. Together, we reveal that actin-associated formins are essential for maintaining the dynamic organization of cytoplasmic CAV-1 and importantly its sensitivity upon mechanical challenge. We conclude that tension-controlled actin formins act as a safety valve dampening excessive tension on CAV-1 and safeguarding CAV-1 against mechanical damage.

Funder

National Natural Science Foundation of China

CAS–VPST Silk Road Science Fund 2021

Shanghai Municipal Science and Technology Major Project

Natural Science Foundation of Shanghai

100 Talents Program’ from the Chinese Academy of Sciences

Publisher

Oxford University Press (OUP)

Subject

Cell Biology,Genetics,Molecular Biology,General Medicine

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