Cell migration orchestrates migrasome formation by shaping retraction fibers

Fan, Changyuan; Shi, Xuemeng; Zhao, Kaikai; Wang, Linbo; Shi, Kun; Liu, Yan-Jun; Li, Hui; Ji, Baohua; Jiu, Yaming

doi:10.1083/jcb.202109168

Cited by 42 publications

(35 citation statements)

References 51 publications

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“…While it is proven that fibroblasts can produce migrasomes, it is not clear whether these structures may participate in orienting cancer cell migration. In addition, depending on the cell type, migrasomes are often less numerous than the total amount of membranous tubules left behind by fibroblasts (Fan et al, 2022). This opens the possibility that the tubular part of the network also plays a role in directing following cells.…”

Section: Main Textmentioning

confidence: 99%

Fibroblasts generate topographical cues that steer cancer cell migration

Baschieri

Illand

Barbazán

et al. 2022

Preprint

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Fibroblasts play a fundamental role in tumor development. Among other functions, they regulate cancer cells migration through rearranging the extracellular matrix, secreting soluble factors and establishing direct physical contacts with cancer cells. Here, we report that migrating fibroblasts deposit on the substrate a network of tubular structures that serves as guidance cue for cancer cell migration. Such membranous tubular network, hereafter called tracks, is stably anchored to the substrate in a β5 integrin-dependent manner. We found that cancer cells specifically adhere to tracks by using clathrin-coated structures that pinch and engulf tracks. Tracks represent thus a spatial memory of fibroblast migration paths that is read and erased by cancer cells directionally migrating along them. We propose that fibroblast tracks represent a topography-based intercellular communication system capable of steering cancer cells migration.

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Section: Main Textmentioning

confidence: 99%

Fibroblasts generate topographical cues that steer cancer cell migration

Baschieri

Illand

Barbazán

et al. 2022

Preprint

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“…Migrating cells leave behind a distinctive network of branching membranous structures called retraction fibers, first described in 1963 [ 78 ]. Found only at the trailing edge of migrating cells, retraction fibers are actin-rich [ 79 ] and possess cholesterol and tetraspanin-enriched microdomains [ 21 , 80 ]. Integrins also anchor retraction fibers to the ECM and aid in migrasome formation [ 80 ].…”

Section: Extracellular Protrusions: Highways For Ev Transportmentioning

confidence: 99%

“…Integrins also anchor retraction fibers to the ECM and aid in migrasome formation [ 80 ]. Since they are migration-dependent structures, speed and directionality impact retraction fiber and migrasome formation with slower, turning cells producing shorter fibers with fewer migrasomes [ 79 ].…”

Section: Extracellular Protrusions: Highways For Ev Transportmentioning

confidence: 99%

Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

Gustafson

Gammill

2022

JDB

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During embryonic development, cells communicate with each other to determine cell fate, guide migration, and shape morphogenesis. While the relevant secreted factors and their downstream target genes have been characterized extensively, how these signals travel between embryonic cells is still emerging. Evidence is accumulating that extracellular vesicles (EVs), which are well defined in cell culture and cancer, offer a crucial means of communication in embryos. Moreover, the release and/or reception of EVs is often facilitated by fine cellular protrusions, which have a history of study in development. However, due in part to the complexities of identifying fragile nanometer-scale extracellular structures within the three-dimensional embryonic environment, the nomenclature of developmental EVs and protrusions can be ambiguous, confounding progress. In this review, we provide a robust guide to categorizing these structures in order to enable comparisons between developmental systems and stages. Then, we discuss existing evidence supporting a role for EVs and fine cellular protrusions throughout development.

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“…TSPAN4 has been shown to regulate formation of migrasomes, the recently discovered cell organelles playing essential roles in cell-cell signalling, lateral transfer of mRNA and proteins, transport of damaged mitochondria, and organ morphogenesis in vivo 6,7,8,9 . Structurally, migrasomes are few micron large spherical swellings formed on the retraction fibers, tens of microns long and about hundred nanometer thick protrusions of cell plasma membrane pulled out of the cell rear during migration 10 . Recent evidence suggests that retraction fibers are enriched with TSPANs and over-expression of 14 different TSPANs enhances migrasome formation 6 .…”

Section: Introductionmentioning

confidence: 99%

Transmembrane proteins tetraspanin 4 and CD9 sense membrane curvature

Dharan

Goren

Cheppali

et al. 2022

Preprint

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Multiple membrane shaping and remodelling processes are associated with tetraspanin proteins by yet unknown mechanisms. Tetraspanins constitute a family of proteins with four transmembrane domains present in high copy numbers in every cell type. Prominent examples are tetraspanin4 and CD9 that are required for the fundamental cellular processes of migrasome formation and fertilization, respectively. These proteins are enriched in curved membrane structures, such as cellular retraction fibers and oocyte microvilli. The factors driving this enrichment are, however, unknown. Here we revealed that tetrasapnin4 and CD9 are curvature sensors with a preference for positive membrane curvature. To this end we used a biomimetic system emulating membranes of cell retraction fibers and oocyte microvilli by membrane tubes pulled out of giant plasma membrane vesicles with controllable membrane tension and curvature. We developed a simple thermodynamic model for the partitioning of curvature sensors between flat and tubular membranes, which allowed us to estimate the individual intrinsic curvatures of the two proteins. Overall, our findings illuminate the process of migrasome formation and oocyte microvilli shaping and provide insight into the role of tetraspanin proteins in membrane remodelling processes.

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Cell migration orchestrates migrasome formation by shaping retraction fibers

Cited by 42 publications

References 51 publications

Fibroblasts generate topographical cues that steer cancer cell migration

Fibroblasts generate topographical cues that steer cancer cell migration

Extracellular Vesicles and Membrane Protrusions in Developmental Signaling

Transmembrane proteins tetraspanin 4 and CD9 sense membrane curvature

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