Genetic engineering of fibrous proteins: spider dragline silk and collagen.

Various strategies have been employed to genetically engineer fibrous proteins. Two examples, the subject of this review, include spider dragline silk from Nephila clavipes and collagen. These proteins are highlighted because of their unique mechanical and biological properties related to controlled release, biomaterials and tissue engineering. Cloning and expression of native genes and synthetic artificial variants of the consensus sequence repeats from the native genes has been accomplished. Expression of recombinant silk and collagen proteins has been reported in a variety of host systems, including bacteria, yeast, insect cells, plants and mammalian cells. Future utility for these proteins for biomedical materials is expected to increase as needs expand for designer materials with tailored mechanical properties and biological interactions to elicit specific responses in vitro and in vivo.

[1]  F. Gwazdauskas,et al.  Transgenic pigs produce functional human factor VIII in milk , 1997, Nature Biotechnology.

[2]  Winkler,et al.  Controlling beta-sheet assembly in genetically engineered silk by enzymatic Phosphorylation/Dephosphorylation, by , 2000, Biochemistry.

[3]  K. Tasanen,et al.  Molecular cloning of the beta‐subunit of human prolyl 4‐hydroxylase. This subunit and protein disulphide isomerase are products of the same gene. , 1987, The EMBO journal.

[4]  J. Pachence,et al.  Collagen-based devices for soft tissue repair. , 1996, Journal of biomedical materials research.

[5]  Maurille J. Fournier,et al.  Protein engineering for materials applications , 1991 .

[6]  J. Cappello Protein engineering for biomaterials applications , 1992 .

[7]  V. Conticello,et al.  Genetically directed synthesis and spectroscopic analysis of a protein polymer derived from a flagelliform silk sequence. , 2001, Biomacromolecules.

[8]  K. Kivirikko Hydroxylation of proline and lysine residues in collagens and other animal and plant proteins , 1992 .

[9]  C. Kielty,et al.  The Collagen Family: Structure, Assembly, and Organization in the Extracellular Matrix , 2003 .

[10]  D. Kaplan,et al.  Self-Organization (Assembly) in Biosynthesis of Silk Fibers - A Hierarchical Problem , 1991 .

[11]  Stephen Stinson,et al.  Biotechnology Providing Springboard To New Functional Materials: Protein chemists are using repetitive amino acid sequences to make polymers useful for cell growth research and medical, dental needs , 1990 .

[12]  D J Prockop,et al.  Collagens: molecular biology, diseases, and potentials for therapy. , 1995, Annual review of biochemistry.

[13]  David L. Kaplan,et al.  Protein-Based Materials , 1997, Bioengineering of Materials.

[14]  M. E. van der Rest,et al.  Collagen family of proteins , 1991, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  M. Tuite,et al.  Protein disulphide isomerase: building bridges in protein folding. , 1994, Trends in biochemical sciences.

[16]  M B McCarthy,et al.  Functionalized silk-based biomaterials for bone formation. , 2001, Journal of biomedical materials research.

[17]  D. Foster,et al.  High-level expression of recombinant human fibrinogen in the milk of transgenic mice , 1996, Nature Biotechnology.

[18]  R. Lewis,et al.  Expression and purification of a spider silk protein: a new strategy for producing repetitive proteins. , 1996, Protein expression and purification.

[19]  D. Kirschner,et al.  Designing recombinant spider silk proteins to control assembly. , 1999, International journal of biological macromolecules.

[20]  Ivan Martin,et al.  Silk matrix for tissue engineered anterior cruciate ligaments. , 2002, Biomaterials.

[21]  T. Pihlajaniemi,et al.  Two new collagen subgroups: membrane-associated collagens and types XV and XVII. , 1995, Progress in nucleic acid research and molecular biology.

[22]  M. E. Demont,et al.  Spider silk as rubber , 1984, Nature.

[23]  J. A. Chapman,et al.  Collagen fibril formation. , 1996, The Biochemical journal.

[24]  N. Bulleid,et al.  Identification of the molecular recognition sequence which determines the type‐specific assembly of procollagen , 1997, The EMBO journal.

[25]  M. Theisen,et al.  Triple helix assembly and processing of human collagen produced in transgenic tobacco plants , 2000, FEBS letters.

[26]  M B Hinman,et al.  Synthetic spider silk: a modular fiber. , 2000, Trends in biotechnology.

[27]  M B Hinman,et al.  Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. , 1992, The Journal of biological chemistry.

[28]  D. Kaplan,et al.  Construction, cloning, and expression of synthetic genes encoding spider dragline silk. , 1995, Biochemistry.

[29]  R. Lewis,et al.  Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. , 1998, Journal of molecular biology.

[30]  M. Tsukada,et al.  Attachment and growth of cultured fibroblast cells on silk protein matrices. , 1995, Journal of biomedical materials research.

[31]  M. Tsukada,et al.  Synthesis of poly(ethylene glycol)-silk fibroin conjugates and surface interaction between L-929 cells and the conjugates. , 1997, Biomaterials.

[32]  M. Denny,et al.  The structure and properties of spider silk , 1986 .

[33]  K. Vuori,et al.  Characterization of the human prolyl 4-hydroxylase tetramer and its multifunctional protein disulfide-isomerase subunit synthesized in a baculovirus expression system. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Kaplan,et al.  Initial characterization of Nephila clavipes dragline protein , 1994 .

[35]  M. Jacquet,et al.  Fine organization of Bombyx mori fibroin heavy chain gene. , 2000, Nucleic acids research.

[36]  K. Kivirikko,et al.  Protein hydroxylation: prolyl 4‐hydroxylase, an enzyme with four cosubstrates and a multifunctional subunit , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  M. Rest,et al.  Collagens: diversity at the molecular and supramolecular levels , 1993 .

[38]  Beat Steinmann,et al.  Connective tissue and its heritable disorders —Molecular, genetic and medical aspects , 1993 .

[39]  Steven Arcidiacono,et al.  Spider Silk Fibers Spun from Soluble Recombinant Silk Produced in Mammalian Cells , 2002, Science.

[40]  D. Ginzinger,et al.  Silk Properties Determined by Gland-Specific Expression of a Spider Fibroin Gene Family , 1996, Science.

[41]  R Langer,et al.  Collagen in tissue‐engineered cartilage: Types, structure, and crosslinks , 1998, Journal of cellular biochemistry.

[42]  K. Kivirikko,et al.  High‐level production of human type I collagen in the yeast Pichia pastoris , 2001, Yeast.

[43]  N. Bulleid,et al.  Cell‐free synthesis and assembly of prolyl 4‐hydroxylase: the role of the beta‐subunit (PDI) in preventing misfolding and aggregation of the alpha‐subunit. , 1993, The EMBO journal.

[44]  R. Lewis,et al.  Mechanical and Chemical Properties of Certain Spider Silks , 1993 .

[45]  K. Piez,et al.  Collagen fibril formation. Evidence for a multistep process. , 1979, The Journal of biological chemistry.

[46]  D. Kaplan,et al.  Reduction-oxidation control of beta-sheet assembly in genetically engineered silk. , 2000, Biomacromolecules.

[47]  Yu-Qing Zhang Natural silk fibroin as a support for enzyme immobilization , 1998 .

[48]  R. Mayne,et al.  New members of the collagen superfamily. , 1993, Current opinion in cell biology.

[49]  R. Beckwitt,et al.  Sequence conservation in the C-terminal region of spider silk proteins (Spidroin) from Nephila clavipes (Tetragnathidae) and Araneus bicentenarius (Araneidae). , 1994, The Journal of biological chemistry.

[50]  G. Freddi,et al.  In vitro evaluation of the inflammatory potential of the silk fibroin. , 1999, Journal of biomedical materials research.

[51]  H. Heslot Artificial fibrous proteins: a review. , 1998, Biochimie.

[52]  G. Daniels,et al.  Production of recombinant human type I procollagen homotrimer in the mammary gland of transgenic mice , 2004, Transgenic Research.

[53]  William C. Raschke,et al.  Recent Advances in the Expression of Foreign Genes in Pichia pastoris , 1993, Bio/Technology.

[54]  E. Hood,et al.  Plant-based production of xenogenic proteins. , 1999, Current opinion in biotechnology.

[55]  K. Vuori,et al.  Molecular cloning of the alpha-subunit of human prolyl 4-hydroxylase: the complete cDNA-derived amino acid sequence and evidence for alternative splicing of RNA transcripts. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[56]  M. Marquet,et al.  Genetic Engineering of Structural Protein Polymers , 1990, Biotechnology progress.

[57]  M. Elson Dermal filler materials. , 1993, Dermatologic clinics.

[58]  D. Kaplan,et al.  Purification and characterization of recombinant spider silk expressed in Escherichia coli , 1998, Applied Microbiology and Biotechnology.

[59]  S. Fahnestock,et al.  Synthetic spider dragline silk proteins and their production in Escherichia coli , 1997, Applied Microbiology and Biotechnology.

[60]  K. Kivirikko,et al.  Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. , 1982, Methods in enzymology.

[61]  R. Lewis,et al.  Structure of a protein superfiber: spider dragline silk. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[62]  F. Delustro,et al.  Clinical use of injectable bovine collagen: a decade of experience. , 1992, Clinical materials.

[63]  M Cronin-Golomb,et al.  Surface organization and nanopatterning of collagen by dip-pen nanolithography , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[64]  R. Schwartz,et al.  Collagen Uses in Dermatology – An Update , 1999, Dermatology.

[65]  Hideki Sezutsu,et al.  Dynamic Rearrangement Within the Antheraea pernyi Silk Fibroin Gene Is Associated with Four Types of Repetitive Units , 2000, Journal of Molecular Evolution.

[66]  D. Wallace,et al.  Description of collagen fibril formation by a theory of polymer crystallization , 1983, Biopolymers.

[67]  K. Vuori,et al.  Cloning, baculovirus expression, and characterization of a second mouse prolyl 4-hydroxylase alpha-subunit isoform: formation of an alpha 2 beta 2 tetramer with the protein disulfide-isomerase/beta subunit. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[68]  K. Kivirikko,et al.  Expression of Wild-Type and Modified Proα Chains of Human Type I Procollagen in Insect Cells Leads to the Formation of Stable [α1(I)]2α2(I) Collagen Heterotrimers and [α1(I)]3 Homotrimers but Not [α2(I)]3 Homotrimers* , 1997, The Journal of Biological Chemistry.

[69]  J. Scheller,et al.  Production of spider silk proteins in tobacco and potato , 2001, Nature Biotechnology.

[70]  D. Kaplan,et al.  Conformational transitions in model silk peptides. , 2000, Biophysical journal.

[71]  D. Kaplan,et al.  Molecular biology of spider silk. , 2000, Journal of biotechnology.

[72]  K. Kivirikko,et al.  Assembly of human prolyl 4‐hydroxylase and type III collagen in the yeast Pichia pastoris: formation of a stable enzyme tetramer requires coexpression with collagen and assembly of a stable collagen requires coexpression with prolyl 4‐hydroxylase , 1997, The EMBO journal.

[73]  E. K. Tillinghast,et al.  The alkaline proteases of Argiope and their possible role in web digestion , 1977 .

[74]  K. Tasanen,et al.  A single polypeptide acts both as the beta subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase. , 1987, The Journal of biological chemistry.

[75]  A. Kind,et al.  Expression of an engineered form of recombinant procollagen in mouse milk , 1999, Nature Biotechnology.

[76]  F. Ruggiero,et al.  Human recombinant alpha1(V) collagen chain. Homotrimeric assembly and subsequent processing. , 1997, The Journal of biological chemistry.

[77]  L. Bedzyk,et al.  Production of synthetic spider dragline silk protein in Pichia pastoris , 1997, Applied Microbiology and Biotechnology.

[78]  K. Kivirikko,et al.  Cloning of the Human Prolyl 4-Hydroxylase α Subunit Isoform α(II) and Characterization of the Type II Enzyme Tetramer , 1997, The Journal of Biological Chemistry.

[79]  K. Kivirikko,et al.  Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[80]  M. Tsukada,et al.  Effect of the chemical modification of the arginyl residue in Bombyx mori silk fibroin on the attachment and growth of fibroblast cells. , 1998, Journal of biomedical materials research.

[81]  H. Weiner,et al.  Effects of oral administration of type II collagen on rheumatoid arthritis. , 1993, Science.

[82]  David L. Kaplan,et al.  Mechanical and thermal properties of dragline silk from the spider Nephila clavipes , 1994 .

[83]  S. Peltonen,et al.  Characterization of Human Type III Collagen Expressed in a Baculovirus System , 1996, The Journal of Biological Chemistry.

[84]  R. Krishna,et al.  Post-Translational Modifications of Proteins , 1993 .

[85]  J. Cappello,et al.  The biological production of protein polymers and their use. , 1990, Trends in biotechnology.

[86]  D. Kaplan,et al.  Methionine Redox Controlled Crystallization of Biosynthetic Silk Spidroin , 1999 .

[87]  G. Chisholm,et al.  Production of Recombinant Human Type I Procollagen Trimers Using a Four-gene Expression System in the Yeast Saccharomyces cerevisiae * , 2000, The Journal of Biological Chemistry.

[88]  R. Lewis,et al.  Molecular architecture and evolution of a modular spider silk protein gene. , 2000, Science.

[89]  K. Kivirikko,et al.  Involvement of Prolyl 4-Hydroxylase in the Assembly of Trimeric Minicollagen XII , 1996, The Journal of Biological Chemistry.

[90]  Y. Fukushima Genetically engineered syntheses of tandem repetitive polypeptides consisting of glycine-rich sequence of spider dragline silk. , 1998, Biopolymers.