DOI: 10.1083/jcb.148.5.1075. Integrin Dynamics and Matrix Assembly

10.1083/jcb.148.5.1075

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Fibronectin matrix assembly is a multistep, integrin-dependent process. To investigate the role of integrin dynamics in fibronectin fibrillogenesis, we developed an antibody-chasing technique for simultaneous tracking of two integrin populations by different antibodies. We established that whereas the vitronectin receptor αvβ3 remains within focal contacts, the fibronectin receptor α5β1 translocates from focal contacts into and along extracellular matrix (ECM) contacts. This escalator-like translocation occurs relative to the focal contacts at 6.5 ± 0.7 μm/h and is independent of cell migration. It is induced by ligation of α5β1 integrins and depends on interactions with a functional actin cytoskeleton and vitronectin receptor ligation. During cell spreading, translocation of ligand-occupied α5β1 integrins away from focal contacts and along bundles of actin filaments generates ECM contacts. Tensin is a primary cytoskeletal component of these ECM contacts, and a novel dominant-negative inhibitor of tensin blocked ECM contact formation, integrin translocation, and fibronectin fibrillogenesis without affecting focal contacts. We propose that translocating α5β1 integrins induce initial fibronectin fibrillogenesis by transmitting cytoskeleton-generated tension to extracellular fibronectin molecules. Blocking this integrin translocation by a variety of treatments prevents the formation of ECM contacts and fibronectin fibrillogenesis. These studies identify a localized, directional, integrin translocation mechanism for matrix assembly.

Bibliography

Pankov, R., Cukierman, E., Katz, B.-Z., Matsumoto, K., Lin, D. C., Lin, S., Hahn, C., & Yamada, K. M. (2000). Integrin Dynamics and Matrix Assembly. The Journal of Cell Biology, 148(5), 1075â1090.

Authors 8

Roumen Pankov (first)
Edna Cukierman (additional)
Ben-Zion Katz (additional)
Kazue Matsumoto (additional)
Diane C. Lin (additional)
Shin Lin (additional)
Cornelia Hahn (additional)
Kenneth M. Yamada (additional)

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Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 10:10 p.m.)
Indexed	37 minutes ago (Aug. 28, 2025, 3:12 a.m.)
Issued	25 years, 5 months ago (March 6, 2000)
Published	25 years, 5 months ago (March 6, 2000)
Published Online	25 years, 5 months ago (March 6, 2000)
Published Print	25 years, 5 months ago (March 6, 2000)

Funders 0

None

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  "abstract": "<jats:p>Fibronectin matrix assembly is a multistep, integrin-dependent process. To investigate the role of integrin dynamics in fibronectin fibrillogenesis, we developed an antibody-chasing technique for simultaneous tracking of two integrin populations by different antibodies. We established that whereas the vitronectin receptor \u03b1v\u03b23 remains within focal contacts, the fibronectin receptor \u03b15\u03b21 translocates from focal contacts into and along extracellular matrix (ECM) contacts. This escalator-like translocation occurs relative to the focal contacts at 6.5 \u00b1 0.7 \u03bcm/h and is independent of cell migration. It is induced by ligation of \u03b15\u03b21 integrins and depends on interactions with a functional actin cytoskeleton and vitronectin receptor ligation. During cell spreading, translocation of ligand-occupied \u03b15\u03b21 integrins away from focal contacts and along bundles of actin filaments generates ECM contacts. Tensin is a primary cytoskeletal component of these ECM contacts, and a novel dominant-negative inhibitor of tensin blocked ECM contact formation, integrin translocation, and fibronectin fibrillogenesis without affecting focal contacts. We propose that translocating \u03b15\u03b21 integrins induce initial fibronectin fibrillogenesis by transmitting cytoskeleton-generated tension to extracellular fibronectin molecules. Blocking this integrin translocation by a variety of treatments prevents the formation of ECM contacts and fibronectin fibrillogenesis. These studies identify a localized, directional, integrin translocation mechanism for matrix assembly.</jats:p>",
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