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J. Biol. Chem., Vol. 282, Issue 9, 6792-6802, March 2, 2007

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The Collagens of Hydra Provide Insight into the Evolution of Metazoan Extracellular Matrices^*

Xiaoming Zhang¹, Raymond P. Boot-Handford¹², Julie Huxley-Jones, Lorna N. Forse, A. Paul Mould, David L. Robertson, LiLi, Matthews Athiyal, and Michael P. Sarras, Jr.^¶

From the Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, Kansas 66160, Wellcome Trust Centre for Cell-Matrix Research, Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom, and ^¶Department of Cell Biology and Anatomy, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois 60064

A collagen-based extracellular matrix is one defining feature of all Metazoa. The thick sheet-like extracellular matrix (mesoglia) of the diploblast, hydra, has characteristics of both a basement membrane and an interstitial matrix. Several genes associated with mesoglea have been cloned including a basement membrane and fibrillar collagen and an A and B chain of laminin. Here we report the characterization of a further three fibrillar collagen genes (Hcol2, Hcol3, and Hcol5) and the partial sequence of a collagen gene with a unique structural organization consisting of multiple von Willebrand factor A domains interspersed with interrupted collagenous triple helices (Hcol6) from Hydra vulgaris. Hcol2 and -5 have major collagenous domains of classical length (1020 amino acid residues), whereas the equivalent domain in Hcol3 is shorter (969 residues). The N-propeptide of Hcol2 contains a whey acid protein four-cysteine repeat (WAP) domain, and the equivalent domain of Hcol3 contains two WAP and two von Willebrand factor A domains. Phylogenetic analyses reveal that the hydra fibrillar collagen genes form a distinct clade that appears related to the protostome/deuterostome A clade of fibrillar collagens. Data base searches reveal Hcol2, -5, and -6 are highly conserved in Hydra magnipapillata, which also provided preliminary evidence for the expression of a B-clade fibrillar collagen. All four of the H. vulgaris collagens are expressed specifically by the ectoderm. The expression pattern for Hcol2 is similar to that previously reported for Hcol1 (Deutzmann, R., Fowler, S., Zhang, X., Boone, K., Dexter, S., Boot-Handford, R. P., Rachel, R., and Sarras, M. P., Jr. (2000) Development 127, 4669-4680) but distinct from the pattern shared by Hcol3 and Hcol5. The characterization of multiple collagen genes in relatively simple diploblastic organisms provides new insights into the molecular evolution of collagens and the origins of the collagen-based extracellular matrix found throughout the multicellular animal kingdom.

Received for publication, August 7, 2006 , and in revised form, January 3, 2007.

The nucleotide sequence(s) reported in this paper has been submitted to the Gen-Bank^TM/EBI Data Bank with accession number(s) DQ679807 [GenBank] , DQ679808 [GenBank] , DQ679809 [GenBank] , and DQ679810 [GenBank] .

^* The work was supported by National Institutes of Health Grant DK065123 (to M. P. S. and X. Z.). The Royal Society, and Biotechnology and Biological Sciences Research Council, Swindon, United Kingdom. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. 1S.

¹ These are co-first authors.

² To whom correspondence should be addressed. Tel.: 44-161-275-5097; Fax: 44-161-275-5082; E-mail: ray.boot-handford{at}manchester.ac.uk.

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