Expression of the fras1/frem gene family during zebrafish development and fin morphogenesis

Mouse studies have highlighted the requirement of the extracellular matrix Fras and Frem proteins for embryonic epidermal adhesion. Mutations of the genes encoding some of these proteins underlie the blebs mouse mutants, whereas mutations in human FRAS1 and FREM2 cause Fraser syndrome, a congenital disorder characterized by embryonic blistering and renal defects. We have cloned the zebrafish homologues of these genes and characterized their evolutionary diversification and expression during development. The fish gene complement includes fras1, frem1a, frem1b, frem2a, frem2b, and frem3, which display complex overlapping and complementary expression patterns in developing tissues including the pharyngeal arches, hypochord, musculature, and otic vesicle. Expression during fin development delineates distinct populations of epidermal cells which have previously only been described at a morphological level. We detect relatively little gene expression in epidermis or pronephros, suggesting that the essential role of these proteins in mediating their development in humans and mice is recently evolved. Developmental Dynamics 237:3295–3304, 2008. © 2008 Wiley‐Liss, Inc.

[1]  M. Zenker,et al.  Fraser syndrome due to homozygosity for a splice site mutation of FREM2 , 2008, American journal of medical genetics. Part A.

[2]  G. Chalepakis,et al.  Basement membrane localization of Frem3 is independent of the Fras1/Frem1/Frem2 protein complex within the sublamina densa. , 2007, Matrix biology : journal of the International Society for Matrix Biology.

[3]  K. Sekiguchi,et al.  Frem3, a member of the 12 CSPG repeats-containing extracellular matrix protein family, is a basement membrane protein with tissue distribution patterns distinct from those of Fras1, Frem2, and QBRICK/Frem1. , 2007, Matrix biology : journal of the International Society for Matrix Biology.

[4]  G. Chalepakis,et al.  Overlapping and divergent localization of Frem1 and Fras1 and its functional implications during mouse embryonic development. , 2007, Experimental cell research.

[5]  G. Chalepakis,et al.  Spatiotemporal distribution of Fras1/Frem proteins during mouse embryonic development. , 2007, Gene expression patterns : GEP.

[6]  I. Smyth,et al.  Let's stick together: The role of the Fras1 and Frem proteins in epidermal adhesion , 2007, IUBMB life.

[7]  A. Slavotinek,et al.  Mutation analysis of the FRAS1 gene demonstrates new mutations in a propositus with Fraser syndrome , 2006, American journal of medical genetics. Part A.

[8]  K. Sekiguchi,et al.  Breakdown of the reciprocal stabilization of QBRICK/Frem1, Fras1, and Frem2 at the basement membrane provokes Fraser syndrome-like defects , 2006, Proceedings of the National Academy of Sciences.

[9]  P. Scambler,et al.  The genetics of Fraser syndrome and the blebs mouse mutants. , 2005, Human Molecular Genetics.

[10]  Martin S. Taylor,et al.  Identification of a new gene mutated in Fraser syndrome and mouse myelencephalic blebs , 2005, Nature Genetics.

[11]  Martin S. Taylor,et al.  The extracellular matrix gene Frem1 is essential for the normal adhesion of the embryonic epidermis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Huganir,et al.  A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1 , 2004, Nature Genetics.

[13]  N. Prescott,et al.  Fraser syndrome and mouse blebbed phenotype caused by mutations in FRAS1/Fras1 encoding a putative extracellular matrix protein , 2003, Nature Genetics.

[14]  P. Scambler,et al.  Fras1 deficiency results in cryptophthalmos, renal agenesis and blebbed phenotype in mice , 2003, Nature Genetics.

[15]  A. Rosenthal,et al.  A novel repeat in the melanoma‐associated chondroitin sulfate proteoglycan defines a new protein family , 2002, FEBS letters.

[16]  B. Appel,et al.  Delta-Notch signaling induces hypochord development in zebrafish. , 2002, Development.

[17]  C. Clarke,et al.  A gene expression screen in zebrafish embryogenesis. , 2001, Genome research.

[18]  J. Löfberg,et al.  Development of the hypochord and dorsal aorta in the zebrafish embryo (Danio rerio) , 2000, Journal of morphology.

[19]  T. Jowett,et al.  Analysis of protein and gene expression. , 1999, Methods in cell biology.

[20]  P. Krieg,et al.  VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. , 1998, Development.

[21]  S. Higashijima,et al.  Mindin/F-spondin family: novel ECM proteins expressed in the zebrafish embryonic axis. , 1997, Developmental biology.

[22]  C. Nüsslein-Volhard,et al.  Mutations affecting development of the midline and general body shape during zebrafish embryogenesis. , 1996, Development.

[23]  J. Postlethwait,et al.  Expression of a type II collagen gene in the zebrafish embryonic axis , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[24]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[25]  R. Winter Fraser syndrome and mouse ‘bleb’ mutants , 1990, Clinical genetics.

[26]  J. Tucker,et al.  Modulation of epidermal cell shaping and extracellular matrix during caudal fin morphogenesis in the zebra fish Brachydanio rerio. , 1985, Journal of embryology and experimental morphology.