The Application of Recombinant Human Collagen in Tissue Engineering

Collagen is the main structural protein in vertebrates. It plays an essential role in providing a scaffold for cellular support and thereby affecting cell attachment, migration, proliferation, differentiation, and survival. As such, it also plays an important role in numerous approaches to the engineering of human tissues for medical applications related to tissue, bone, and skin repair and reconstruction. Currently, the collagen used in tissue engineering applications is derived from animal tissues, creating concerns related to the quality, purity, and predictability of its performance. It also carries the risk of transmission of infectious agents and precipitating immunological reactions. The recent development of recombinant sources of human collagen provides a reliable, predictable and chemically defined source of purified human collagens that is free of animal components. The triple-helical collagens made by recombinant technology have the same amino acid sequence as human tissue-derived collagen. Furthermore, by achieving the equivalent extent of proline hydroxylation via coexpression of genes encoding prolyl hydroxylase with the collagen genes, one can produce collagens with a similar degree of stability as naturally occurring material. The recombinant production process of collagen involves the generation of single triple-helical molecules that are then used to construct more complex three-dimensional structures. If one loosely defines tissue engineering as the use of a biocompatible scaffold combined with a biologically active agent (be it a gene or gene construct, growth factor or other biologically active agent) to induce tissue regeneration, then the production of recombinant human collagen enables the engineering of human tissue based on a human matrix or scaffold. Recombinant human collagens are an efficient scaffold for bone repair when combined with a recombinant bone morphogenetic protein in a porous, sponge-like format, and when presented as a membrane, sponge or gel can serve as a basis for the engineering of skin, cartilage and periodontal ligament, depending on the specific requirements of the chosen application.

[1]  B. Kheirabadi,et al.  Comparative study of the efficacy of the common topical hemostatic agents with fibrin sealant in a rabbit aortic anastomosis model. , 2002, The Journal of surgical research.

[2]  Luigi Vitagliano,et al.  Recent progress on collagen triple helix structure, stability and assembly. , 2002, Protein and peptide letters.

[3]  R. Cohen,et al.  The etiology and prevalence of gingival recession. , 2003, Journal of the American Dental Association.

[4]  D. Symmons,et al.  The clinical management of rheumatoid arthritis and osteoarthritis: strategies for improving clinical effectiveness. , 1998, British journal of rheumatology.

[5]  E Bell,et al.  Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

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

[7]  Katsutoshi Yoshizato,et al.  Transgenic silkworms produce recombinant human type III procollagen in cocoons , 2003, Nature Biotechnology.

[8]  K. Kivirikko,et al.  Coexpression with collagen markedly increases the half-life of the recombinant human prolyl 4-hydroxylase tetramer in the yeast Pichia pastoris. , 1999, Matrix biology : journal of the International Society for Matrix Biology.

[9]  M. Brittberg,et al.  Autologous chondrocytes used for articular cartilage repair: an update. , 2001, Clinical orthopaedics and related research.

[10]  N. Browse,et al.  Prospective randomized trial of woven versus collagen‐impregnated knitted prosthetic Dacron grafts in aortoiliac surgery , 1998, The British journal of surgery.

[11]  J. Feijen,et al.  In vitro degradation of dermal sheep collagen cross-linked using a water-soluble carbodiimide. , 1996, Biomaterials.

[12]  H. Helminen,et al.  Apoptosis of chondrocytes in transgenic mice lacking collagen II. , 1997, Experimental cell research.

[13]  Makarand V Risbud,et al.  Tissue engineering: advances in in vitro cartilage generation. , 2002, Trends in biotechnology.

[14]  G. Chisholm,et al.  Production of Human Type I Collagen in Yeast Reveals Unexpected New Insights into the Molecular Assembly of Collagen Trimers* , 2001, The Journal of Biological Chemistry.

[15]  G. Charriere,et al.  Bovine collagen induced systemic symptoms: antibody formation against bovine and human collagen. , 1996, The Journal of rheumatology.

[16]  M E Nimni,et al.  Collagen: structure, function, and metabolism in normal and fibrotic tissues. , 1983, Seminars in arthritis and rheumatism.

[17]  I. K. Cohen,et al.  Wound Healing: Biochemical & Clinical Aspects , 1992 .

[18]  K. Kivirikko,et al.  Expression of wild-type and modified proalpha chains of human type I procollagen in insect cells leads to the formation of stable [alpha1(I)]2alpha2(I) collagen heterotrimers and [alpha1(I)]3 homotrimers but not [alpha2(I)]3 homotrimers. , 1997, The Journal of biological chemistry.

[19]  R. Burgeson,et al.  α1(XX) Collagen, a New Member of the Collagen Subfamily, Fibril-associated Collagens with Interrupted Triple Helices* , 2001, The Journal of Biological Chemistry.

[20]  K. Kivirikko,et al.  Prolyl 4-hydroxylase and its role in collagen synthesis. , 1991, Journal of hepatology.

[21]  R. Cohen,et al.  Collagen as an implantable material in medicine and dentistry. , 2002, The Journal of oral implantology.

[22]  William C. Chapman,et al.  A novel collagen-based composite offers effective hemostasis for multiple surgical indications: Results of a randomized controlled trial. , 2001, Surgery.

[23]  J. Ramshaw,et al.  The collagen triple-helix structure. , 1997, Matrix biology : journal of the International Society for Matrix Biology.

[24]  K. Csiszȧr,et al.  Lysyl oxidases: a novel multifunctional amine oxidase family. , 2001, Progress in nucleic acid research and molecular biology.

[25]  P. D. Kemp.  Tissue engineering and cell-populated collagen matrices. , 2009, Methods in molecular biology.

[26]  M. Béné,et al.  Immunogenicity of injectable collagen implants. , 1987, The Journal of dermatologic surgery and oncology.

[27]  F. Silver,et al.  Cell growth on collagen: a review of tissue engineering using scaffolds containing extracellular matrix. , 1992, Journal of long-term effects of medical implants.

[28]  T. Pihlajaniemi,et al.  Co-expression of the alpha subunit of human prolyl 4-hydroxylase with BiP polypeptide in insect cells leads to the formation of soluble and insoluble complexes. Soluble alpha-subunit-BiP complexes have no prolyl 4-hydroxylase activity. , 1996, The Biochemical journal.

[29]  K. Kivirikko,et al.  Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. , 1998, Advances in enzymology and related areas of molecular biology.

[30]  J. Werkmeister,et al.  Production of recombinant hydroxylated human type III collagen fragment in Saccharomyces cerevisiae. , 1998, DNA and cell biology.

[31]  J. McPherson,et al.  Collagen fibrillogenesis in vitro: a characterization of fibril quality as a function of assembly conditions. , 1985, Collagen and related research.

[32]  J. Aubin,et al.  Mineralized bone nodules formedin vitro from enzymatically released rat calvaria cell populations , 1986, Calcified Tissue International.

[33]  C. Radziejewski,et al.  Binding of discoidin domain receptor 2 to collagen I: an atomic force microscopy investigation. , 2002, Biochemistry.

[34]  J. Gergely,et al.  Zero-length crosslinking procedure with the use of active esters. , 1990, Analytical biochemistry.

[35]  R. Rohwer,et al.  Inactivation of viral and prion pathogens by γ‐irradiation under conditions that maintain the integrity of human albumin , 2003, Vox sanguinis.

[36]  Linda G Griffith,et al.  Emerging Design Principles in Biomaterials and Scaffolds for Tissue Engineering , 2002, Annals of the New York Academy of Sciences.

[37]  D. Tuckwell.  Identification and analysis of collagen α1(XXI), a novel member of the FACIT collagen family , 2002 .

[38]  L. Ala‐Kokko,et al.  Synthesis of recombinant human procollagen II in a stably transfected tumour cell line (HT1080). , 1994, The Biochemical journal.

[39]  G. Vunjak‐Novakovic,et al.  Growth factors for sequential cellular de- and re-differentiation in tissue engineering. , 2002, Biochemical and biophysical research communications.

[40]  T. Fujita,et al.  A Novel Human Serum Lectin with Collagen- and Fibrinogen-like Domains That Functions as an Opsonin (*) , 1996, The Journal of Biological Chemistry.

[41]  R. Cohen,et al.  Treatment of gingival recession. , 2002, Journal of the American Dental Association.

[42]  T. Durham,et al.  Application of INSTAT hemostat in the control of gingival hemorrhage in the patient with thrombocytopenia. A case report. , 1991, Oral surgery, oral medicine, and oral pathology.

[43]  Kenneth M. Yamada,et al.  Taking Cell-Matrix Adhesions to the Third Dimension , 2001, Science.

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

[45]  K. Kadler,et al.  Recombinant expression systems for the production of collagen. , 2000, Biochemical Society transactions.

[46]  K. Kivirikko,et al.  Accumulation of properly folded human type III procollagen molecules in specific intracellular membranous compartments in the yeast Pichia pastoris. , 2000, Matrix biology : journal of the International Society for Matrix Biology.

[47]  K. Kivirikko.  Chapter 9 Posttranslational processing of collagens , 1996 .

[48]  R. Cohen,et al.  Collagen: An Overview , 2002, Implant dentistry.

[49]  M. Theisen,et al.  Hydroxylated human homotrimeric collagen I in Agrobacterium tumefaciens‐mediated transient expression and in transgenic tobacco plant , 2002, FEBS letters.

[50]  F. Hernández,et al.  [Integra Artificial dermis in pediatric reconstructive surgery]. , 2002, Cirugía pediátrica.

[51]  J. Heino.  The collagen receptor integrins have distinct ligand recognition and signaling functions. , 2000, Matrix biology : journal of the International Society for Matrix Biology.

[52]  T. Fujita,et al.  Ficolins and the lectin complement pathway , 2001, Immunological reviews.

[53]  D. Eyre,et al.  Collagen: molecular diversity in the body's protein scaffold , 1980, Science.

[54]  R. Berisio,et al.  Crystal structure of the collagen triple helix model [(Pro‐Pro‐Gly)10]3 , 2002, Protein science : a publication of the Protein Society.

[55]  J. Sugar,et al.  Expression of type XII collagen and hemidesmosome-associated proteins in keratoconus corneas , 2001, Current eye research.

[56]  K. Kivirikko,et al.  Substrate specificity of human prolyl-4-hydroxylase. , 1998, Bioorganic & medicinal chemistry letters.

[57]  David L Kaplan,et al.  Silk-based biomaterials. , 2003, Biomaterials.

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

[59]  P. Trinder,et al.  The collagen‐like component of the complement system, C1q, is recognized by 7 S autoantibodies and is functionally impaired in synovial fluids of patients with rheumatoid arthritis , 1996, Immunology.

[60]  W. Walsh,et al.  Mechanical and Histologic Evaluation of Collagraft® in an Ovine Lumbar Fusion Model , 2000, Clinical orthopaedics and related research.

[61]  D. Eyre,et al.  Structural Analysis of Cross-linking Domains in Cartilage Type XI Collagen , 1995, The Journal of Biological Chemistry.

[62]  G. Charriere,et al.  Immunogenicity of injectable collagen implants. , 1990, The Journal of dermatologic surgery and oncology.

[63]  James M. Roberts,et al.  Fibrillar Collagen Inhibits Arterial Smooth Muscle Proliferation through Regulation of Cdk2 Inhibitors , 1996, Cell.

[64]  J. Lotz,et al.  Use of a Collagen‐Hydroxyapatite Matrix in Spinal Fusion: A Rabbit Model , 1998, Spine.

[65]  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.

[66]  R. Burgeson,et al.  Collagen XXIV, a Vertebrate Fibrillar Collagen with Structural Features of Invertebrate Collagens , 2003, Journal of Biological Chemistry.

[67]  D. Herbage,et al.  Collagen-based biomaterials as 3D scaffold for cell cultures: applications for tissue engineering and gene therapy , 2000, Medical and Biological Engineering and Computing.

[68]  R. Timpl,et al.  The collagen superfamily. , 1995, International archives of allergy and immunology.

[69]  K. Kivirikko,et al.  Collagen biosynthesis: a mini-review cluster. , 1998, Matrix biology : journal of the International Society for Matrix Biology.

[70]  N. Arakawa,et al.  The effect of L-ascorbic acid on age-related changes of pyridinoline in cartilage collagen of guinea pigs. , 1998, Journal of nutritional science and vitaminology.

[71]  D. Prockop,et al.  Expression of human COL1A1 gene in stably transfected HT1080 cells: the production of a thermostable homotrimer of type I collagen in a recombinant system. , 1993, Matrix.

[72]  D. Tuckwell.  Identification and analysis of collagen alpha 1(XXI), a novel member of the FACIT collagen family. , 2002, Matrix biology : journal of the International Society for Matrix Biology.

[73]  C T Laurencin,et al.  Tissue engineered bone-regeneration using degradable polymers: the formation of mineralized matrices. , 1996, Bone.

[74]  D. Eyre,et al.  Structural characteristics of cross-linking sites in type V collagen of bone. Chain specificities and heterotypic links to type I collagen. , 1994, European journal of biochemistry.

[75]  S. Ricard-Blum,et al.  Unconventional collagens : types VI, VII, VIII, IX, X, XII, XIV, XVI, and XIX , 2000 .

[76]  G. Charriere,et al.  Reactions to a bovine collagen implant. Clinical and immunologic study in 705 patients. , 1989, Journal of the American Academy of Dermatology.

[77]  K. Kivirikko,et al.  Characterization of Three Fragments That Constitute the Monomers of the Human Lysyl Hydroxylase Isoenzymes 1–3 , 2002, The Journal of Biological Chemistry.

[78]  L Cooperman,et al.  The immunogenicity of injectable collagen. I. A 1-year prospective study. , 1984, Journal of the American Academy of Dermatology.

[79]  David R. Olsen,et al.  Recombinant collagen and gelatin for drug delivery. , 2003, Advanced drug delivery reviews.

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

[81]  D. Eyre,et al.  Two-dimensional peptide mapping of cross-linked type IX collagen in human cartilage. , 2000, Archives of biochemistry and biophysics.

[82]  D. Wisser,et al.  Skin replacement with a collagen based dermal substitute, autologous keratinocytes and fibroblasts in burn trauma. , 2003, Burns : journal of the International Society for Burn Injuries.

[83]  K. Reid,et al.  C1q: structure, function, and receptors. , 2000, Immunopharmacology.

[84]  M J Lysaght,et al.  The growth of tissue engineering. , 2001, Tissue engineering.

[85]  J. Lu,et al.  Ficolins and the fibrinogen-like domain. , 1998, Immunobiology.

[86]  I. Kanazawa,et al.  CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC‐P/collagen type XXV , 2002, The EMBO journal.

[87]  C. Vincent,et al.  Adventitious agents from animal-derived raw materials and production systems. , 1996, Developments in biological standardization.

[88]  M. Bissell,et al.  Multi‐faceted regulation of cell differentiation by extracellular matrix , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[89]  D. Eyre.  Articular cartilage and changes in Arthritis: Collagen of articular cartilage , 2001, Arthritis research.

[90]  M. Schwartz.  Integrin signaling revisited. , 2001, Trends in cell biology.

[91]  W. Chapman,et al.  Effective Management of Bleeding during Tumor Resection with a Collagen-Based Hemostatic Agent , 2002, The American surgeon.

[92]  F. D. de Wolf,et al.  Secreted production of a custom-designed, highly hydrophilic gelatin in Pichia pastoris. , 2001, Protein engineering.

[93]  D. Prockop,et al.  Procollagen N-proteinase. Properties of the enzyme purified from chick embryo tendons. , 1982, European journal of biochemistry.

[94]  E Bell,et al.  Recipes for reconstituting skin. , 1991, Journal of biomechanical engineering.

[95]  Hak-Sun Kim,et al.  Simple Carrier Matrix Modifications Can Enhance Delivery of Recombinant Human Bone Morphogenetic Protein-2 for Posterolateral Spine Fusion , 2003, Spine.

[96]  Yugyung Lee,et al.  Biomedical applications of collagen. , 2001, International journal of pharmaceutics.

[97]  K. Reid,et al.  Structures and functions of mammalian collectins. , 2001, Results and problems in cell differentiation.

[98]  M S Chapekar,et al.  Tissue engineering: challenges and opportunities. , 2000, Journal of biomedical materials research.

[99]  K. Kivirikko,et al.  Collagens and collagen-related diseases , 2001, Annals of medicine.

[100]  Gordana Vunjak-Novakovic,et al.  Differential effects of growth factors on tissue-engineered cartilage. , 2002, Tissue engineering.

[101]  L. Wünsch,et al.  A cell-seeded biocomposite for cartilage repair. , 2002, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

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

[103]  T. Kase,et al.  Recombinant bovine conglutinin, lacking the N-terminal and collagenous domains, has less conglutination activity but is able to inhibit haemagglutination by influenza A virus. , 1996, The Biochemical journal.

[104]  S. Bernocco,et al.  Control of Heterotypic Fibril Formation by Collagen V Is Determined by Chain Stoichiometry* , 2001, The Journal of Biological Chemistry.

[105]  A. Minamide,et al.  Evaluation of Carriers of Bone Morphogenetic Protein for Spinal Fusion , 2001, Spine.

[106]  G. Davis,et al.  Affinity of integrins for damaged extracellular matrix: alpha v beta 3 binds to denatured collagen type I through RGD sites. , 1992, Biochemical and biophysical research communications.

[107]  P. Huguet,et al.  Burned breast reconstructive surgery with Integra dermal regeneration template. , 2003, British journal of plastic surgery.

[108]  D. Heimbach,et al.  Artificial Dermis for Major Burns: A Multi‐Center Randomized Clinical Trial , 1988, Annals of surgery.

[109]  S. Jimenez,et al.  Collagen II containing a Cys substitution for Arg-alpha1-519: abnormal interactions of the mutated molecules with collagen IX. , 2001, Biochemistry.

[110]  S. Eisig,et al.  Alveolar ridge augmentation using titanium micromesh: an experimental study in dogs. , 2003, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[111]  M. Humphries,et al.  Integrin structure. , 2000, Biochemical Society transactions.

[112]  H L Wang,et al.  Collagen membranes: a review. , 2001, Journal of periodontology.

[113]  G. Vunjak‐Novakovic,et al.  Bioreactor studies of native and tissue engineered cartilage. , 2002, Biorheology.

[114]  S. Jimenez,et al.  Expression of a human cartilage procollagen gene (COL2A1) in mouse 3T3 cells. , 1991, The Journal of biological chemistry.

[115]  A. Sclafani,et al.  Injectable fillers for facial soft tissue enhancement. , 2000, Facial plastic surgery : FPS.

[116]  Heino Jyrki.  THE COLLAGEN RECEPTOR INTEGRINS , 2003 .

[117]  C. Whitehead.  Bone Biology and Skeletal Disorders in Poultry , 1992 .

[118]  D. Eyre,et al.  Recent developments in cartilage research: matrix biology of the collagen II/IX/XI heterofibril network. , 2001, Biochemical Society transactions.

[119]  C. Overall.  Molecular determinants of metalloproteinase substrate specificity , 2002, Molecular biotechnology.

[120]  J. Whitsett,et al.  The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. , 2002, The Journal of clinical investigation.

[121]  M. Humphries,et al.  The Year 2000 Integrin Model , 2000 .

[122]  C. Laane,et al.  Endogenous prolyl 4-hydroxylation in Hansenula polymorpha and its use for the production of hydroxylated recombinant gelatin. , 2002, FEMS yeast research.

[123]  D. Eyre,et al.  Assembly of collagen types II, IX and XI into nascent hetero-fibrils by a rat chondrocyte cell line. , 2003, European journal of biochemistry.

[124]  M. Danesh-Meyer,et al.  Digital subtraction radiographic analysis of GTR in human intrabony defects. , 2002, The International journal of periodontics & restorative dentistry.

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

[126]  F. Silver,et al.  Immunogenicity of collagenous implants. , 1990, Biomaterials.

[127]  David L Kaplan,et al.  Genetic engineering of fibrous proteins: spider dragline silk and collagen. , 2002, Advanced drug delivery reviews.

[128]  Yoshimitsu Kuroyanagi,et al.  Design of artificial skin , 1996 .

[129]  D. Eyre,et al.  Collagen type IX from human cartilage: a structural profile of intermolecular cross-linking sites. , 1996, The Biochemical journal.

[130]  J. Burkus,et al.  Radiographic Assessment of Interbody Fusion Using Recombinant Human Bone Morphogenetic Protein Type 2 , 2003, Spine.

[131]  J. Verhaar,et al.  Growth factors in cartilage tissue engineering. , 2002, Biorheology.

[132]  R. Wind,et al.  High‐yield secretion of recombinant gelatins by Pichia pastoris , 1999, Yeast.

[133]  I. Yannas,et al.  Design of an artificial skin. I. Basic design principles. , 1980, Journal of biomedical materials research.

[134]  R. Cohen,et al.  Cellular inflammatory response to porcine collagen membranes. , 2003, Journal of periodontal research.

[135]  S. Wolfe,et al.  Use of Skin Substitutes in Pediatric Patients , 2003, The Journal of craniofacial surgery.

[136]  A. Atala,et al.  In Vitro Systems for Tissue Engineering , 2002, Annals of the New York Academy of Sciences.

[137]  N. Adzick,et al.  Wound Healing: Biochemical and Clinical Aspects , 1992 .

[138]  B. Zetter,et al.  Type XXIII Collagen, a New Transmembrane Collagen Identified in Metastatic Tumor Cells* , 2003, Journal of Biological Chemistry.

[139]  J. Werkmeister,et al.  Collagen-based biomaterials. , 1996, Biotechnology & genetic engineering reviews.

[140]  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.

[141]  J. Heino,et al.  alpha 11beta 1 integrin recognizes the GFOGER sequence in interstitial collagens. , 2003, The Journal of biological chemistry.

[142]  E. Ehlers,et al.  Characteristics of human chondrocytes, osteoblasts and fibroblasts seeded onto a type I/III collagen sponge under different culture conditions. A light, scanning and transmission electron microscopy study. , 2000, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[143]  K. Reid.  Structure/function relationships in the collectins (mammalian lectins containing collagen-like regions). , 1994, Biochemical Society transactions.

[144]  Chunguang Wang,et al.  Lysyl Hydroxylase 3 Is a Multifunctional Protein Possessing Collagen Glucosyltransferase Activity* , 2000, The Journal of Biological Chemistry.

[145]  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.

[146]  S. Boden,et al.  The Use of rhBMP-2 in Interbody Fusion Cages: Definitive Evidence of Osteoinduction in Humans: A Preliminary Report , 2000, Spine.

[147]  R. Friedman,et al.  A novel human cDNA with a predicted protein similar to lysyl oxidase maps to chromosome 15q24-q25. , 1993, The Journal of biological chemistry.

[148]  J. Bateman,et al.  A new FACIT of the collagen family: COL21A1 , 2001, FEBS letters.

[149]  R. Hynes,et al.  Integrins in vascular development. , 1999, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[150]  B L Currier,et al.  Biodegradable Polymer Scaffolds for Cartilage Tissue Engineering , 2001, Clinical orthopaedics and related research.

[151]  H. Kurata,et al.  Role of the collagen-like domain of the human serum mannan-binding protein in the activation of complement and the secretion of this lectin. , 1993, Biochemical and biophysical research communications.

[152]  D. West,et al.  Evaluation of Tissue‐Engineered Skin (Human Skin Substitute) and Secondary Intention Healing in the Treatment of Full Thickness Wounds after Mohs Micrographic or Excisional Surgery , 2002, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[153]  U. Puistola,et al.  Studies on the lysyl hydroxylase reaction. II. Inhibition kinetics and the reaction mechanism. , 1980, Biochimica et biophysica acta.

[154]  M. Chapman,et al.  Multicenter Trial of Collagraft as Bone Graft Substitute , 1991, Journal of orthopaedic trauma.

[155]  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.

[156]  George E. Davis,et al.  Affinity of integrins for damaged extracellular matrix: αvβ3 binds to denatured collagen type I through RGD sites , 1992 .

[157]  A. Papp,et al.  A collagen based dermal substitute and the modified Meek technique in extensive burns. Report of three cases. , 2003, Burns : journal of the International Society for Burn Injuries.

[158]  K. Yoshizato,et al.  Formation of recombinant human procollagen I heterotrimers in a baculovirus expression system. , 1997, Journal of biochemistry.

[159]  K. Okuda,et al.  Molded bone augmentation by a combination of barrier membrane and recombinant human bone morphogenetic protein-2. , 2001, Oral diseases.

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

[161]  Y. Nishimune,et al.  Type XXVI Collagen, a New Member of the Collagen Family, Is Specifically Expressed in the Testis and Ovary* , 2002, The Journal of Biological Chemistry.

[162]  K. Kivirikko,et al.  Expression of recombinant human type I-III collagens in the yeast pichia pastoris. , 2000, Biochemical Society transactions.

[163]  D. Eyre,et al.  Recent developments in cartilage research , 2002 .

[164]  D. Asher.  The transmissible spongiform encephalopathy agents: concerns and responses of United States regulatory agencies in maintaining the safety of biologics. , 1999, Developments in biological standardization.

[165]  U. Seybold,et al.  Gelatine production, the six steps to maximum safety. , 1993, Developments in biological standardization.

[166]  P. Trackman,et al.  Properties and function of lysyl oxidase. , 1991, American journal of respiratory cell and molecular biology.

[167]  D. Hulmes,et al.  The collagen superfamily--diverse structures and assemblies. , 1992, Essays in biochemistry.

[168]  Shan S. Wong,et al.  Chemistry of Protein Conjugation and Cross Linking , 1991 .

[169]  K. Kivirikko,et al.  Cloning, baculovirus expression, and characterization of the alpha subunit of prolyl 4-hydroxylase from the nematode Caenorhabditis elegans. This alpha subunit forms an active alpha beta dimer with the human protein disulfide isomerase/beta subunit. , 1994, The Journal of biological chemistry.

[170]  D. Eyre,et al.  Matrix deposition of tryptophan-containing allelic variants of type IX collagen in developing human cartilage. , 2003, Matrix biology : journal of the International Society for Matrix Biology.

[171]  J. Feijen,et al.  Tissue Regenerating Capacity of Carbodiimide-Crosslinked Dermal Sheep Collagen during Repair of the Abdominal Wall , 1994, The International journal of artificial organs.

[172]  K. Reid,et al.  Complement component C1 and the collectins--first-line defense molecules in innate and acquired immunity. , 2002, Trends in immunology.

[173]  K. Shakesheff,et al.  Recent advances in tissue engineering: an invited review. , 2002, Journal of long-term effects of medical implants.

[174]  R. Balderston,et al.  Clinical and Radiographic Outcomes of Anterior Lumbar Interbody Fusion Using Recombinant Human Bone Morphogenetic Protein-2 , 2002, Spine.

[175]  W. Vogel,et al.  Collagen-receptor signaling in health and disease. , 2001, European journal of dermatology : EJD.

[176]  R. Poulsom,et al.  A Novel and Highly Conserved Collagen (proα1(XXVII)) with a Unique Expression Pattern and Unusual Molecular Characteristics Establishes a New Clade within the Vertebrate Fibrillar Collagen Family* , 2003, Journal of Biological Chemistry.

[177]  K. Yoshizato,et al.  Production of EGF-collagen chimeric protein which shows the mitogenic activity. , 2001, Biochimica et biophysica acta.

[178]  G. Fields,et al.  Matrix metalloproteinases and collagen catabolism. , 2002, Biopolymers.

[179]  F. Phillips,et al.  Collagen Crosslinks in Human Lumbar Intervertebral Disc Aging , 1998, Spine.