Expression of a mutant human fibrillin allele upon a normal human or murine genetic background recapitulates a Marfan cellular phenotype.

The Marfan syndrome (MFS) is a connective tissue disorder inherited as an autosomal dominant trait and caused by mutations in the gene encoding fibrillin, a 350-kD glycoprotein that multimerizes to form extracellular microfibrils. It has been unclear whether disease results from a relative deficiency of wild-type fibrillin; from a dominant-negative effect, in which mutant fibrillin monomers disrupt the function of the wild-type protein encoded by the normal allele; or from a dynamic and variable interplay between these two pathogenetic mechanisms. We have now addressed this issue in a cell culture system. A mutant fibrillin allele from a patient with severe MFS was expressed in normal human and murine fibroblasts by stable transfection. Immunohistochemical analysis of the resultant cell lines revealed markedly diminished fibrillin deposition and disorganized microfibrillar architecture. Pulse-chase studies demonstrated normal levels of fibrillin synthesis but substantially reduced deposition into the extracellular matrix. These data illustrate that expression of a mutant fibrillin allele, on a background of two normal alleles, is sufficient to disrupt normal microfibrillar assembly and reproduce the MFS cellular phenotype. This underscores the importance of the fibrillin amino-terminus in normal microfibrillar assembly and suggests that expression of the human extreme 5' fibrillin coding sequence may be sufficient, in isolation, to produce an animal model of MFS. Lastly, this substantiation of a dominant-negative effect offers mutant allele knockout as a potential strategy for gene therapy.

[1]  U. Francke,et al.  Quantitative differences in biosynthesis and extracellular deposition of fibrillin in cultured fibroblasts distinguish five groups of Marfan syndrome patients and suggest distinct pathogenetic mechanisms. , 1994, The Journal of clinical investigation.

[2]  C. Kielty,et al.  The role of calcium in the organization of fibrillin microfibrils , 1993, FEBS letters.

[3]  H. Helminen,et al.  Mutations in Type 1 Procollagen That Cause Osteogenesis Imperfecta: Effects of the Mutations on the Assembly of Collagen into Fibrils, the Basis of Phenotypic Variations, and Potential Antisense Therapies , 1993, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[4]  U. Francke,et al.  Missense mutations impair intracellular processing of fibrillin and microfibril assembly in Marfan syndrome. , 1993, Human molecular genetics.

[5]  F. Ramirez,et al.  The fibrillin‐marfan syndrome connection , 1993, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  H. Dietz,et al.  Four novel FBN1 mutations: significance for mutant transcript level and EGF-like domain calcium binding in the pathogenesis of Marfan syndrome. , 1993, Genomics.

[7]  H. Dietz,et al.  Fibrillin binds calcium and is coded by cDNAs that reveal a multidomain structure and alternatively spliced exons at the 5' end. , 1993, Genomics.

[8]  B. Sykes,et al.  A novel fibrillin mutation in the Marfan syndrome which could disrupt calcium binding of the epidermal growth factor-like module. , 1993, Human molecular genetics.

[9]  E. Puffenberger,et al.  Marfan phenotype variability in a family segregating a missense mutation in the epidermal growth factor-like motif of the fibrillin gene. , 1992, The Journal of clinical investigation.

[10]  R. Glanville,et al.  Purification and partial characterization of fibrillin, a cysteine-rich structural component of connective tissue microfibrils. , 1991, The Journal of biological chemistry.

[11]  R. Glanville,et al.  Partial sequence of a candidate gene for the Marfan syndrome , 1991, Nature.

[12]  M. Mattei,et al.  Linkage of Marfan syndrome and a phenotypically related disorder to two different fibrillin genes , 1991, Nature.

[13]  Ada Hamosh,et al.  Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene , 1991, Nature.

[14]  I. D. Campbell,et al.  Key residues involved in calcium-binding motifs in EGF-like domains , 1991, Nature.

[15]  R. Glanville,et al.  Extraction of extendable beaded structures and their identification as fibrillin-containing extracellular matrix microfibrils. , 1991, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[16]  L. Peltonen,et al.  Location on chromosome 15 of the gene defect causing Marfan syndrome. , 1990, The New England journal of medicine.

[17]  L. Maquat,et al.  Translation to near the distal end of the penultimate exon is required for normal levels of spliced triosephosphate isomerase mRNA , 1990, Molecular and cellular biology.

[18]  R. Pyeritz,et al.  Immunohistologic abnormalities of the microfibrillar-fiber system in the Marfan syndrome. , 1990, The New England journal of medicine.

[19]  Davis Cg,et al.  The many faces of epidermal growth factor repeats. , 1990 .

[20]  R. Glanville,et al.  Connective tissue microfibrils. Isolation and characterization of three large pepsin-resistant domains of fibrillin. , 1989, The Journal of biological chemistry.

[21]  R. Pyeritz,et al.  Association of mitral valve prolapse and systemic abnormalities of connective tissue. A phenotypic continuum. , 1989, JAMA.

[22]  L. Chasin,et al.  Nonsense mutations in the dihydrofolate reductase gene affect RNA processing , 1989, Molecular and cellular biology.

[23]  E. Engvall,et al.  Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils , 1986, The Journal of cell biology.

[24]  V. McKusick,et al.  The Marfan syndrome: diagnosis and management. , 1979, The New England journal of medicine.

[25]  E. Southern Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[26]  P. Byers,et al.  Marfan syndrome: defective synthesis, secretion, and extracellular matrix formation of fibrillin by cultured dermal fibroblasts. , 1992, The Journal of clinical investigation.

[27]  C. Davis,et al.  The many faces of epidermal growth factor repeats. , 1990, The New biologist.

[28]  I. Campbell,et al.  The solution structure of human epidermal growth factor , 1987, Nature.

[29]  Victor A. McKusick,et al.  Heritable disorders of connective tissue , 1972 .