Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes

Invadosomes are a family of subcellular actin-based structures essential for cell–extracellular matrix (ECM) interaction and remodeling. In non-invasive cells, they are referred to as podosomes, which enable adhesion, migration, and ECM remodeling via secretion of metalloproteinases or mechano-tract...

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Main Author: Frédérique Gaits-Iacovoni
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-08-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2025.1644011/full
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author Frédérique Gaits-Iacovoni
author_facet Frédérique Gaits-Iacovoni
author_sort Frédérique Gaits-Iacovoni
collection DOAJ
description Invadosomes are a family of subcellular actin-based structures essential for cell–extracellular matrix (ECM) interaction and remodeling. In non-invasive cells, they are referred to as podosomes, which enable adhesion, migration, and ECM remodeling via secretion of metalloproteinases or mechano-traction. In invasive tumoral cells, these structures are called invadopodia due to their function. Despite structural similarity, podosomes appear as highly regular dots in 2D and do not always exhibit ECM-degradative abilities; hence, the term “degradative dot-podosomes” is used in this paper. Invadopodia are consistently degradative, fewer in number, slightly larger, deeper, less regular-shaped, and longer-lived. In tumor cells, collagen I induces the formation of linear invadosomes, which promote invasion by degrading collagen through the action of MT1–MMP (membrane type 1–matrix metalloproteinase) and the adaptor protein Tks5 (tyrosine kinase substrate 5). Interestingly, linear invadosomes also appear in non-tumor cells, such as megakaryocytes (MKs)—the platelet precursors—which display podosomes that closely resemble invadopodia. As MKs mature, Tks5 expression decreases, and dot-podosomes align along collagen I fibers, fusing into linear podosomes that remodel the ECM through mechanical traction but have lost their degradative ability. The GTPase Cdc42, crucial for invadosome formation, remains highly active in the MK internal demarcation membrane system (DMS) but is downregulated in linear podosomes. These observations suggest that Tks5, considered a marker of metastatic potential, also plays roles in normal physiology. Thus, linear podosomes with mechanotransductive properties may exist in a broader range of non-transformed cells. This mini-review focuses on the linear subfamily of invadosomes, highlighting their structure and function in MKs, a model in which invadosomes remain underexplored.
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spelling doaj-art-ca089df97a814ea78ca2b3ab84e104a32025-08-20T03:39:09ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-08-011310.3389/fcell.2025.16440111644011Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytesFrédérique Gaits-IacovoniInvadosomes are a family of subcellular actin-based structures essential for cell–extracellular matrix (ECM) interaction and remodeling. In non-invasive cells, they are referred to as podosomes, which enable adhesion, migration, and ECM remodeling via secretion of metalloproteinases or mechano-traction. In invasive tumoral cells, these structures are called invadopodia due to their function. Despite structural similarity, podosomes appear as highly regular dots in 2D and do not always exhibit ECM-degradative abilities; hence, the term “degradative dot-podosomes” is used in this paper. Invadopodia are consistently degradative, fewer in number, slightly larger, deeper, less regular-shaped, and longer-lived. In tumor cells, collagen I induces the formation of linear invadosomes, which promote invasion by degrading collagen through the action of MT1–MMP (membrane type 1–matrix metalloproteinase) and the adaptor protein Tks5 (tyrosine kinase substrate 5). Interestingly, linear invadosomes also appear in non-tumor cells, such as megakaryocytes (MKs)—the platelet precursors—which display podosomes that closely resemble invadopodia. As MKs mature, Tks5 expression decreases, and dot-podosomes align along collagen I fibers, fusing into linear podosomes that remodel the ECM through mechanical traction but have lost their degradative ability. The GTPase Cdc42, crucial for invadosome formation, remains highly active in the MK internal demarcation membrane system (DMS) but is downregulated in linear podosomes. These observations suggest that Tks5, considered a marker of metastatic potential, also plays roles in normal physiology. Thus, linear podosomes with mechanotransductive properties may exist in a broader range of non-transformed cells. This mini-review focuses on the linear subfamily of invadosomes, highlighting their structure and function in MKs, a model in which invadosomes remain underexplored.https://www.frontiersin.org/articles/10.3389/fcell.2025.1644011/fulllinear invadosomespodosomescytoskeletonextracellular matrixmetalloproteinaseCDC42 GTPase
spellingShingle Frédérique Gaits-Iacovoni
Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
Frontiers in Cell and Developmental Biology
linear invadosomes
podosomes
cytoskeleton
extracellular matrix
metalloproteinase
CDC42 GTPase
title Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
title_full Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
title_fullStr Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
title_full_unstemmed Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
title_short Invadosomes as “shape-shifters” of cellular maturation: insights from megakaryocytes
title_sort invadosomes as shape shifters of cellular maturation insights from megakaryocytes
topic linear invadosomes
podosomes
cytoskeleton
extracellular matrix
metalloproteinase
CDC42 GTPase
url https://www.frontiersin.org/articles/10.3389/fcell.2025.1644011/full
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