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First published online 14 March 2006
doi: 10.1242/jcs.02830

Journal of Cell Science 119, 1350-1360 (2006)
Published by The Company of Biologists 2006
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Research Article

New insights into extracellular matrix assembly and reorganization from dynamic imaging of extracellular matrix proteins in living osteoblasts

Pitchumani Sivakumar1, Andras Czirok2, Brenda J. Rongish2, Vivek P. Divakara1,3, Yu-Ping Wang3 and Sarah L. Dallas1,*

1 Department of Oral Biology, UMKC School of Dentistry, 650 E 25th Street, Kansas City, MO 64108, USA
2 Department of Anatomy and Cell Biology, The University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS 66160, USA
3 School of Computing and Engineering, UMKC, 5100 Rockhill Road, Kansas City, MO 64 USA

* Author for correspondence (e-mail: dallass{at}umkc.edu)

Accepted 7 December 2005

The extracellular matrix (ECM) has been traditionally viewed as a static scaffold that supports cells and tissues. However, recent dynamic imaging studies suggest that ECM components are highly elastic and undergo continual movement and deformation. Latent transforming growth factor beta (TGFß) binding protein-1 (LTBP1) is an ECM glycoprotein that binds latent TGFß and regulates its availability and activity. LTBP1 initially co-distributes with fibronectin in the extracellular matrix of osteoblasts, and depends on fibronectin for its assembly. To gain further insights into the mechanisms of assembly of LTBP1 and its spatial and temporal interactions with fibronectin, we have performed dual fluorescence time-lapse imaging of these two proteins in living osteoblasts using fluorescent probes. Time-lapse movies showed surprisingly large fibril displacements associated with cellular movement as well as occasional breaking of LTBP1 or fibronectin-containing fibrils. Individual fibrils stretched to as much as 3.5 times or contracted to as much as one fourth of their original length. Motile cells appeared to actively mediate extracellular matrix assembly by adding `globules' or `packets' of matrix material onto existing fibrils. They also actively reorganized the extracellular matrix by shunting matrix material from one location to another and exchanging fibrillar material between fibrils. This cell-mediated matrix reorganization was primarily associated with the assembly and remodeling of the initial (early) matrix, whereas mature, established ECM was more stable. Displacement vector mapping showed that different matrix fibrillar networks within the same cultures can show different dynamic motion in response to cell movement and showed that the motion of fibrils was correlated with cell motion. These data suggest novel cell-mediated mechanisms for assembly and reorganization of the extracellular matrix and highlight a role for cell motility in the assembly process.

Key words: Dynamic imaging, Extracellular matrix, Fibronectin, LTBP1, Osteoblasts






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