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J. Biol. Chem., Vol. 283, Issue 18, 12129-12135, May 2, 2008

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Active Negative Control of Collagen Fibrillogenesis in Vivo

INTRACELLULAR CLEAVAGE OF THE TYPE I PROCOLLAGEN PROPEPTIDES IN TENDON FIBROBLASTS WITHOUT INTRACELLULAR FIBRILS^*

From the Wellcome Trust Centre for Cell-Matrix Research, University of Manchester, Faculty of Life Sciences, Michael Smith Building, Oxford Road, Manchester M13 9PT, United Kingdom

It is established fact that type I collagen spontaneously self-assembles in vitro in the absence of cells or other macromolecules. Whether or not this is the situation in vivo was unknown. Recent evidence shows that intracellular cleavage of procollagen (the soluble precursor of collagen) to collagen can occur in embryonic tendon cells in vivo, and when this occurs, intracellular collagen fibrils are observed. A cause-and-effect relationship between intracellular collagen and intracellular fibrils was not established. Here we show that intracellular cleavage of procollagen to collagen occurs in postnatal murine tendon cells in situ. Pulse-chase analyses showed cleavage of procollagen to collagen via its two propeptide-retained intermediates. Furthermore, immunoelectron microscopy, using an antibody that recognizes the triple helical domain of collagen, shows collagen molecules in large-diameter transport compartments close to the plasma membrane. However, neither intracellular fibrils nor fibripositors (collagen fibril-containing plasma membrane protrusions) were observed. The results show that intracellular collagen occurs in murine tendon in the absence of intracellular fibrillogenesis and fibripositor formation. Furthermore, the results show that murine postnatal tendon cells have a high capacity to prevent intracellular collagen fibrillogenesis.

Received for publication, October 2, 2007 , and in revised form, January 14, 2008.

^* This work was supported by the Wellcome Trust (to K. E. K.) and the Biotechnology and Biological Sciences Research Council (as an equipment grant to K. E. K. and a postgraduate studentship to S. M. H.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Tel.: 44-0-161-275-5086; Fax: 44-0-161-275-1505; E-mail: karl.kadler{at}manchester.ac.uk.

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