Collagen pp 81-110 | Cite as

Restraining Cross-Links Responsible for the Mechanical Properties of Collagen Fibers: Natural and Artificial

  • N.C. Avery
  • A.J. Bailey


The mechanical properties of collagen fibers primarily depend on the formation of head to tail Schiff base cross-links between end-overlapped collagen molecules within the fiber induced by the enzyme lysyl oxidase. Inhibition of these cross-links results in the complete loss of mechanical strength of the fiber. During maturation these initial divalent cross-links react further with molecules in register from an adjacent fiber forming stable trivalent cross-links and further increasing its mechanical strength. This system of cross-linking is well established and exists throughout the animal kingdom from sponges to man, but there remain a number of unidentified cross-links known to be present in some tissues. In addition, there are some unusual cross-links in certain invertebrates. The nature of the collagen cross-linking is tissue specific rather than species specific and depends on the extent of hydroxylation of both the telopeptide and triple helical lysines involved in the cross-link and on the rate of collagen metabolism. The cross-link profile of collagen fibers therefore varies considerably within and between tissues, for example in different bones. Recent studies indicate that pyrrole cross-links rather than pyridinoline cross-links correlate with mechanical strength of avian bones. The profile can change between normal loading and extreme exercise and these differences appear to relate to their particular function, but further studies to identify whether a particular cross-link is responsible remain to be carried out.

Following maturation the low turnover of collagen allows the non-enzymic random accumulation of glucose oxidation products, some of which form intermolecular cross-links, ultimately rendering the fiber too stiff for normal function. The significance of the major glycation cross-link, believed to be glucosepane, remains to be confirmed. The successful use of inhibitors of this glycation reaction and of specific glycation cross-link breakers should lead to a reduction in this deleterious effect in both aging and diabetes mellitus.

The high mechanical strength and resistance to heat and bacterial degradation of collagen fibers has been utilized industrially. Additional chemical cross-linking in vitro has been employed historically to attain specific mechanical and thermal properties, for example tanning skin to leather, and more recently in medical and cosmetic products with low cytotoxic effects. The resultant increases in denaturation temperature have recently been correlated with reduced water content of the fiber. A wide range of cross-linking agents are available for modification of collagen to provide a product with specific properties.


Triple Helix Collagen Molecule Denaturation Temperature Bone Collagen Lysyl Oxidase 
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  1. Aeschlimann D and Paulsson M (1991) Cross-linking of laminin-nidogen complexes by tissue transglutaminase – a novel mechanism for basement membrane stabilization. J Biol. Chem. 266 15308–15317.Google Scholar
  2. Aeschlimann D and Thomazy V (2000) Protein cross-links in assembly and remodelling of extracellular matrices. The role of transglutaminase. Connect. Res. 41 1–27.CrossRefGoogle Scholar
  3. Akagawa M, Sasaki T and Suyama K (2002) Oxidative deamination of lysine residues in plasma proteins of diabetic rats. Novel mechanism via the Maillard reaction. Eur. J. Biochem. 269 5451–5420.CrossRefGoogle Scholar
  4. Alexander R McN (1988) Elastic Mechanisms in Animal Movement. Cambridge University Press, Cambridge UK.Google Scholar
  5. Amiel D, Frank C, Harwood F, Fronek J and Akeson W (1984) Tendons and ligaments; a morphological and biochemical comparison. J. Ortho. Res. 1 257–265.CrossRefGoogle Scholar
  6. Andreassen T T, Seyer-Hansen K and Bailey A J (1981) Thermal stability, mechanical properties and reducible cross-links of rat tail tendon in experimental diabetes. Biochim. Biophys. Acta. 677 313–317.Google Scholar
  7. Avery N C and Bailey A J (2005) Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to ageing and exercise. Scand. J. Med. Sci. Sports. 15 231–240.CrossRefGoogle Scholar
  8. Bailey A J (1968) Effects of ionizing radiation on connective tissue components. Int. Rev. Connect. Tissue Res. 4 233–281.Google Scholar
  9. Bailey A J and Peach C M (1968) Isolation and structural identification of a labile intermolecular cross-link in collagen. Biochem. Biophys. Res. Commun. 33 812–819.CrossRefGoogle Scholar
  10. Bailey A J and Shimokomaki M S (1971) Age related changes in the reducible cross-links of collagen. FEBS Lett. 16 86–88.CrossRefGoogle Scholar
  11. Bailey A J and Robins S P (1972) Embryonic skin collagen replacement of the type of aldimine cross-link during the early growth period. FEBS Lett. 21 330–334.CrossRefGoogle Scholar
  12. Bailey A J, Gathercole L J, Dlugosz J, Keller A and Voyle C A (1982) Proposed resolution of the paradox of extensive cross-linking and low tensile strength of the cuvierian tubules collagen from the sea cucumber Holothuria forskali. Int. J. Biol. Macromol. 4 329–334.CrossRefGoogle Scholar
  13. Bailey A J, Light N D and Atkins E D T (1980) Chemical cross-linking restrictions on models for the molecular organization of the collagen fibre. Nature (Lond) 288 408–410.CrossRefGoogle Scholar
  14. Bailey A J, Wotton S F, Sims T J and Thompson P W (1992) Post-translational modification in the collagen of human osteoporotic femoral head. Biochem. Biophys. Res. Commun. 185 801–805.CrossRefGoogle Scholar
  15. Banse X, Sims T J and Bailey A J (2002a) Mechanical properties of vertebral cancellous bone: Correlation with intermolecular cross-links. J. Bone Miner. Res. 17 1621–1628.Google Scholar
  16. Banse X, Devogelaer J P, Lafasse A. Grynpas M, Sims T J and Bailey A J (2002b) The cross-link profile of bone collagen correlates with the structural organization of the trabeculae. Bone 31 70–76.Google Scholar
  17. Batge B, Diebold J, Stein H, Bodo M and Muller P K (1992) Compositional analysis of the collagenous bone matrix: a study on adult normal and osteopenic bone tissue. Eur. J. Clin. Invest. 22 805–812.CrossRefGoogle Scholar
  18. Baynes J W (2003) Chemical modification of proteins by lipids in diabetes. Clin. Chem. Lab. Med. 41 1159–1165.CrossRefGoogle Scholar
  19. Bella J, Brodsky B and Berman H M (1995) Hydration structure of a collagen peptide. Structure 3 893–966.CrossRefGoogle Scholar
  20. Bernstein P H and Mechanic G L (1980) A natural histidine-based imminium cross-link in collagen and its location. J. Biol. Chem. 255 10414–10422.Google Scholar
  21. Biemel K M, Reihl O, Conrad J and Lederer M O (2001) Formation pathways for lysine-arginine cross-links derived from hexoses and pentoses by the Maillard process. J. Biol. Chem. 276 23405–23412.CrossRefGoogle Scholar
  22. Bierhaus A, Humpert P M, Morcos M, Wenet T, Chavakis T, Arnold B, Stern D M and Nawroth P P (2005) Understanding RAGE, the receptor for advanced glycation end-products. J. Mol. Med. 83 876–886.CrossRefGoogle Scholar
  23. Birch H L, McLaughlin L, Smith R K and Goodship A E (1999) Treadmill exercise-induced tendon hypertrophy: assessment of tendons with different mechanical function. Equine Vet. J. 30 222–236.Google Scholar
  24. Bohak Z (1968) N (dl-2-amino-2-carboxyethyl)-1-lysine: a new amino acid formed on alkaline treatment of proteins. J. Biol. Chem. 239 2878.Google Scholar
  25. Brady J D and Robins S P (2001) Structural characterization of pyrrole cross-links in type I collagen of human bone. J. Biol. Chem. 276 18812–18818.CrossRefGoogle Scholar
  26. Brinkmann E, Degenhardt T P, Thorpe S R and Baynes J W (1998) Role of the Maillard reaction in aging of tissue proteins. Advanced glycation end-product-dependent increase in imidazolium cross-links in human lens capsules. J. Biol. Chem. 273 18714–18719.CrossRefGoogle Scholar
  27. Brownlee M, Vlassara H, Kooney A, Ulrich P and Cerami A (1986) Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science. 232 1629–1632.CrossRefGoogle Scholar
  28. Buckingham B and Reiser K M (1990) Relationship between the extent of lysyl oxidase-dependent cross-links in skin collagen, non-enzymatic glycosylation and long-term complications of type I diabetes mellitus. J. Clin. Invest. 86 1946–1054.CrossRefGoogle Scholar
  29. Burjanadze T V and Kisirya E L (1982) Dependence of thermal stability on the number of hydrogen-bonds in water-bridged collagen structure. Biopolymers 21 1695–1701.CrossRefGoogle Scholar
  30. Cerami C, Founds H, Nicholl I D, Mitsuhashi T, Giordano D, Vanpatten S, Lee A Al-Abed Y, Vlassara H, Bucala R and Cerami A (1997) Tobacco smoke is a source of toxic reactive glycation products. Proc. Natl. Acad. Sci. USA 94 13915–13920.CrossRefGoogle Scholar
  31. Chen S S and Humphrey J D (1998) Heat-induced change in the mechanics of a collagenous tissue: pseudo elastic behaviour at 37ˆC. J. Biomech. 31 211–216.CrossRefGoogle Scholar
  32. Chen R N, Ho H O and Sheu M T (2005) Characterization of collagen matrices cross-linked using microbial transglutaminase. Biomat. 26 4229–4235.CrossRefGoogle Scholar
  33. Covington A D 1997 Modern tanning chemistry. Chem. Soc. Rev. 26 111–126.CrossRefGoogle Scholar
  34. Curwin S L, Vailas A C and Wood J (1988) Immature tendon adaptation to strenuous exercise. J. Appl. Physiol. 65 2297–2301.Google Scholar
  35. Damink L H H O, Dijkstra P J, vanLuyn M J A, Vanwachem P B, Nieuwenhuis P and Feijen J (1995) Cross-linking of dermal sheep collagen using hexamethylene diisocyanate. J. Mater. Sci. Mater. MED. 6 429–434.CrossRefGoogle Scholar
  36. Damink L H H O, Dijkstra P J, vanLuyn M J A, Vanwachem P B, Nieuwenhuis D and Feijen J (1996) Cross-linking of dermal sheep collagen using a water soluble carbodiimide. Biomaterials 16 1003–1008.Google Scholar
  37. Doblar D (2008) PhD Thesis. University of Essex, UK.Google Scholar
  38. Draper E R C, Morris M D, Camacho N P, Matousek P, Towrie M, Parker A W and Goodship A E (2005) Novel assessment of bone using time-resolved transcutaneous Raman Spectroscopy. J. Bone Miner. Res. 20 1968–1972.CrossRefGoogle Scholar
  39. Eriksen H A, Sharp C A, Robins S P, Sassi M-L, Risteli L and Risteli J (2004) Differently cross-linked and uncross-linked carboxy-terminal telopeptides of type I collagen in human mineralised bone. Bone 34 720–727.CrossRefGoogle Scholar
  40. Eyre D R and Oguchi H (1980) The hydroxypyridinolinium cross-links of skeletal collagen: their measurement, properties and proposed pathway of formation. Biochem. Biophys. Res. Commun. 92 403–410.CrossRefGoogle Scholar
  41. Eyre D R, Shao P, Weis M A and Steinmann B (2002) The kyphoscoliotic type of Ehlers-Danlos syndrome (type VI); differential effects on hydroxylation of lysines in collagens I and II revealed by analysis of cross-linked telopeptides from urine. Mol. Genet. and Metab. 76 211–216.CrossRefGoogle Scholar
  42. Foerder C A and Shapiro B M (1977) Release of ovoperoxidase from sea-urchin eggs hardens the fertilization membrane with di-tyrosine cross-links Proc. Natl. Acad. Sci. USA 74 4214–4218.CrossRefGoogle Scholar
  43. Fujimoto D, Ishida T and Hayashi H (1978) The structure of pyridinoline, a collagen cross-link. Biochem. Biophys. Res. Commun. 84 52–57.CrossRefGoogle Scholar
  44. Glimcher M J, Shapiro F, Ellis R D and Eyre D R (1980) Changes in tissue morphology and collagen composition during the repair of cortical bone in the adult chicken. J. Bone Joint Surg. 62A 964–973.Google Scholar
  45. Goldberg T, Cai W, Peppa M, Dardaine V, Baliga B S, Uribarri J and Vlassara H (2004) Advanced glycoxidation end-products in commonly consumed foods. J. Am. Diet Assoc. 104 1287–1291.CrossRefGoogle Scholar
  46. Goldin A, Beckman J A, Schmidt A M and Creager M A (2006) Advanced glycation end-products: sparking the development of diabetic vascular injury. Circulation 114 597–605.CrossRefGoogle Scholar
  47. Grenard P, Bresson-Hadni S, EI Alaoui S, Chevallier M, Vuitton DA and Ricard-Blum S (2001) Transglutaminase-mediated cross-linking is involved in the stabilization of the extra-cellular matrix in human liver fibrosis. J. Hepatol. 35 367–375.CrossRefGoogle Scholar
  48. Hanson D A and Eyre D R (1996) Molecular specificity of pyridinoline and pyrrole cross-links in type I collagen of human bone. J. Biol. Chem. 271 26508–26516.CrossRefGoogle Scholar
  49. Henle T (2005) Protein-bound advanced glycation end-products (AGEs) as bioactive amino acid derivatives in foods. Amino Acids 29 313–322.CrossRefGoogle Scholar
  50. Holmgren S K, Taylor K M, Bretscher L E and Raines R T (1998) Code for collagen’s stability deciphered. Nature 392 666–667.CrossRefGoogle Scholar
  51. Hinton D J S and Ames J M (2006) Site specificity of glycation and carboxymethylation of BSA by fructose Amino Acids. 30 425–433.CrossRefGoogle Scholar
  52. Hipkiss A R (2005) Glycation ageing and carnosine: are carnivorous diets beneficial? Mech. Ageing Dev. 126(10) 1034–1039CrossRefGoogle Scholar
  53. Hudson B G and Schmidt A M (2004) RAGE: a novel target for drug intervention in diabetic vascular disease. Pharm. Res. 21 1079–1086.CrossRefGoogle Scholar
  54. Johansen M B, Kiemer L and Brunak S (2006) Analysis and prediction of mammalian protein glycation. Glycobiology 16 844–853.CrossRefGoogle Scholar
  55. Kato Y, Nishikawa T and Kawakishi S (1995) Formation of protein-bound 3,4 dihydroxyphenylalanine in collagen types I and IV exposed to ultraviolet light. Photochem. Photobiol. 61 367–372.CrossRefGoogle Scholar
  56. Kent M J C, Light N D and Bailey A J (1985) Evidence for glucose-mediated covalent cross-linking of collagen after glycosylation in vitro. Biochem. J. 225 745–752.Google Scholar
  57. Kielty C M, Baldock, C, Sherratt M J, Rock M J, Lee D and Shuttleworth C A (2003) Fibrillin; from microfibril assembly to biomechanical function. In Elastomeric Proteins (Eds. P R Shewry, A S Tatham A S and A J Bailey) Cambridge University Press, Cambridge UK. pp 94–114.Google Scholar
  58. Kleman J-P, Aeschlimann D, Paulson M and van der Rest M (1995) Transglutaminase-catalysed cross-linking of fibrils of collagen V/XI in A204 Rhabdomyosarcoma cells. Biochemistry 34 13768–13775.CrossRefGoogle Scholar
  59. Kirsch E, Kreig T, Remberger K, Fendel H, Bruckner P and Muller P K (1981) Disorder of collagen-metabolism in a patient with osteogenesis imperfecta (lethal type)- increased degree of hydroxylation of lysine in collagen type I and type III. Eur. J. Clin. Invest. 11 38–47.CrossRefGoogle Scholar
  60. Knott L, Whitehead C C, Fleming R H and Bailey A J (1995) The biochemistry of the collagenous matrix of osteoporotic avian bone. Biochem. J. 310 1045–1051.Google Scholar
  61. Knott L, Tarlton J F and Bailey A J (1997) The chemistry of collagen cross-links. Biochemical changes in collagen during partial mineralization of turkey leg tendon. Biochem. J. 322 535–542.Google Scholar
  62. Knott L and Bailey A J (1998) Collagen cross-links in mineralising tissues: a review of their biochemistry, function and clinical relevance. Bone 22 181–187.CrossRefGoogle Scholar
  63. Knott L and Bailey A J (1999) The collagen biochemistry of avian bone: a comparison of bone type and skeletal site. Brit. J. Poultry Sci. 40 371–379.CrossRefGoogle Scholar
  64. Kopp J, Sale P and Bonnet Y (1977) Apparatus for measuring contraction devised for studying physical properties of collagen fibres- isometric tension, extent of cross-linking, relaxation. Can. I. Food Sc. Tech. J. 10 69–72.Google Scholar
  65. Kupyers R, Tyler M, Kurth L B, Jenkins I D, and Horgan D J (1992) Identification of the loci of the collagen associated Ehrlich chromogen in type I collagen confirms its role as a trivalent cross-link. Biochem. J. 283 129–136.Google Scholar
  66. Li B H and Aspden R M (1997) Composition and mechanical properties of cancellous bone from the femoral head of patients with osteoporosis and osteoarthritis. J. Bone Mineral Res. 12 541–651.CrossRefGoogle Scholar
  67. Light N D and Bailey A J (1985) Collagen Cross-links: location of pyridinoline in type I collagen. FEBS Lett. 182 503–508.CrossRefGoogle Scholar
  68. Lucero HA and Kagan HM (2006) Lysyl oxidase; an oxidative enzyme and effector of cell function. Cell. Mol. Life Sci. 63 2604–2316.CrossRefGoogle Scholar
  69. Mansell J P and Bailey A J (1998) Abnormal cancellous bone collagen metabolism in osteoarthritis. J Clin. Invest. 101 1596–1603.CrossRefGoogle Scholar
  70. McDowell L M, Burzio L A, Waite J H and Schaefer J (1999) Rotational echo double resonance detection of cross-links formed in mussel byssus under high flow stress. J. Biol. Chem. 274 20293–20295.CrossRefGoogle Scholar
  71. Miles C A, Knott L, Sumner I G and Bailey A J (1998) Differences between the thermal stabilities of the three triple helical domains of type IX collagen. J. Mol. Biol. 27 135–144.CrossRefGoogle Scholar
  72. Miles C A, Sionkowska A, Hulin S, Sims T J, Avery N C and Bailey A J (2000) Identification of an intermediate state in the helix coil degradation of collagen by UV light. J. Biol. Chem. 275 33014–33020.CrossRefGoogle Scholar
  73. Miles C A and Ghelashvili M (1999) Polymer-in-a-box mechanism for the thermal stabilization of collagen molecules in fibres. Biophys. J. 76 3243–3252.CrossRefGoogle Scholar
  74. Miles C A, Avery N C, Rodin V and Bailey A J (2005) The increase in denaturation temperature following cross-linking is caused by dehydration of the fibres. J. Mol. Biol. 346 551–556.CrossRefGoogle Scholar
  75. Monnier V M and Cerami A (1981) Non-enzymatic browning in vivo, possible process for aging of long-lived proteins. Science 211 491–493.CrossRefGoogle Scholar
  76. Monnier V M, Mustata T G, Biemel K L, Reihl O, Lederer M O, Zhenyo D and Sell D R (2005) Cross-linking of the extracellular matrix by Maillard reaction in aging and diabetes: an update on “a puzzle nearing resolution”. Ann. NY Acad. Sci. 1043 533–544.CrossRefGoogle Scholar
  77. Notbohm H, Nokelainen M, Myllyharju J, Fietzek P P, Muller P K and Kivirikko K I (1999) Recombinant human type II collagens with low and high levels of hydroxylysine and its glycosylated forms show marked differences in fibrillogenesis in vitro. J. Biol. Chem. 274 8988–8993.CrossRefGoogle Scholar
  78. Odani H, Shinzato T, Usami J, Matsumoto Y, Brinkmann Frye E, Baynes JW and Maeda K (1998) Imidazolium crosslinks derived from reaction of lysine with glyoxal and methylglyoxal are increased in serum proteins of uremic patients; evidence of increased oxidative stress in uremia. FEBS Lett. 427 (3) 381–385CrossRefGoogle Scholar
  79. Ogawa T, Ono T, Tsuda M, Kawanishi Y (1982) A novel fluorphore in insoluble collagen: a cross-linking moiety in collagen molecule. Biochem. Biophys. Res. Commun. 107 1252–1257.CrossRefGoogle Scholar
  80. Paul R G and Bailey A J (2003) Chemical stabilization of collagen as a biomimetric. Sci. World J. 3 138–155.Google Scholar
  81. Paschalis E P, Verdelis K, Doty S B, Boskey A L, Mendelsohn R and Yamauchi M (2001) Spectoscopic characterisation of collagen cross-links in bone. J. Bone Mineral. Res. 16 1821–1828.CrossRefGoogle Scholar
  82. Passoja K, Rautavuoma K, Ala-Kokko L, Kosonen T and Kivirikko K I (1998) Cloning and characterization of a third human lysyl hydroxylase isoform. Proc. Natl. Acad. Sci. USA 95 10482–10486.CrossRefGoogle Scholar
  83. Petite H, Duval L L, Frei V, Abdulmalak N, Sigotluizard M F and Herbage D (1995) Cytocompatability of calf pericardium treated by glutaraldehyde and by acyl azide methods in an organotypic culture model. Biomaterials 16 1003–1008.CrossRefGoogle Scholar
  84. Price DL. Rhett P M, Thorpe S R and Baynes J W (2001) Chelating activity of advanced Glycation End-product inhibitors J. Biol. Chem. 276 48967–48972.CrossRefGoogle Scholar
  85. Ramachandran G N, Bansal M, and Bhatnaga R S (1973) A hypothesis on the role of hydroxyproline in stabilizing collagen structure. Biochem. Biophys. Acta 322 166–171.Google Scholar
  86. Roberts H C, Knott L, Avery N C, Cox T M, Evans M J and Hayman A R (2007) Altered collagen in tartrate-resistant acid phosphatase deficient mice: a role for TRACP in bone collagen metabolism. Calcif. Tissue Intl. 80 400–410.CrossRefGoogle Scholar
  87. Robins S P and Bailey A J (1972) Age-related changes in collagen: the identification of reducible lysine-carbohydrate condensation products. Biochem. Biophys. Res. Communs. 48 76–84.CrossRefGoogle Scholar
  88. Robins S P and Bailey A J (1973) The chemistry of the collagen cross-links. The characterization of Fraction C, a possible artifact produced during the reduction of collagen fibres with borohydride. Biochem J. 135 657–665.Google Scholar
  89. Robins S P and Bailey A J (1975) The chemistry of collagen cross-links. The mechanism of stabilization of the reducible intermediate cross-links. Biochem J. 149 381–385.Google Scholar
  90. Robins S P and Duncan A (1983) Location of pyridinoline in bovine articular cartilage at two sites of the molecules Biochem. J. 215 175–182.Google Scholar
  91. Sell D R and Monnier V M (1989) Structure elucidation of a senescent cross-link from human extracellular matrix. Implications of pentoses in the aging process. J. Biol. Chem. 264 21597–21602.Google Scholar
  92. Sell D R, Biemel K M, Reihl O, Lederer M O, Strauch C M and Monnier V M (2005) Glucosepane is a major protein cross-link of the senescent human extracellular matrix. J. Biol. Chem. 280 12310–12315.CrossRefGoogle Scholar
  93. Sims T J, Avery N C and Bailey A J (2000) Quantitative determination of collagen cross-links. In Methods in Molecular Biology (Eds. C. Strueli and M E Grant) Vol 139 Extracellular Matrix Protocols. Humana Press, Totowa, NJ.Google Scholar
  94. Sionkowska A and Kaminska A (1999) Thermal helix-coil transition in UV irradiated collagen from rat tail tendon. Int. J. Biol. Macromol. 24 337–340.CrossRefGoogle Scholar
  95. Slatter D A, Paul R G, Murray M and Bailey A J (1999) Reaction of lipid-derived malondialdehyde with collagen. J. Biol. Chem. 274 19661–19669.CrossRefGoogle Scholar
  96. Slatter D A, Bolton C H and Bailey A J (2000) The role of lipid-derived malondialdehyde in diabetes mellitus. Diabetologia 43 550–557.CrossRefGoogle Scholar
  97. Slatter D A, Avery N C and Bailey A J (2008) Collagen in the fibrillar state is protected from glycation. Int. J. Biochem. Cell Biol. In press.Google Scholar
  98. Spoerl E. Wollensak G and Seiler T (2004) Increased resistance of cross-linked cornea against enzymatic digestion. Current Eye Res. 29 35–40.CrossRefGoogle Scholar
  99. Takaluoma K, Lantto J, and Myllyharju J (2007) Lysyl hydroxylase-2 is a specific telopeptide hydroxylase, while all three isoenzymes hydroxylate collagenous sequences. Matrix Biol. 26 396–403.CrossRefGoogle Scholar
  100. Thornalley P J (1996) Advance glycation and development of diabetic complications: unifying the involvement of glucose, methyl glyoxal and oxidative stress. Endocrin. Metabol. 3 149–166.Google Scholar
  101. Torre-Blanco A, Adachi E, Hojima Y, Wotton J A M, Minor R R and Prockop D J (1992) Temperature induced post-translational over-modification of type I collagen. Effects of over modification of the protein on the rate of cleavage by procollagen N-proteinase and on self-assembly of collagen into fibrils. J. Biol. Chem. 267 2650–2655.Google Scholar
  102. Vanacore R M, Friedman D B, Ham A J L, Sundaramoorthy M and Hudson B G (2005) Identification of S-hydroxylysyl-methionine as the covalent crosslink of the non-collagenous (NC1) hexamer of the alpha 1 alpha 1alpha 2 collagen IV network – A role for the post-translational modification of lysine 211 to hydroxylysine 211 in hexamer assembly. J.Biol.Chem. 280 (32) 29300–29310.CrossRefGoogle Scholar
  103. Vasan S, Foiles P and Founds H (2003) Therapeutic potential of breakers of advanced glycation end-products – protein cross-links. Arch. Biochem. Biophys. 419 89–96.CrossRefGoogle Scholar
  104. Viidik A (1986) Adaptability of connective tissue. in Biochemistry of Exercise: Human Kinetics (Ed. A Salton) Champaign Ill. USA.Google Scholar
  105. Vlassara H, Brownlee M and Cerami A (1985) High-affinity-receptor-mediated uptake and degradation of glucose modified proteins: a potential mechanism for the removal of senescent macromolecules. Proc. Natl. Acad. Sci. USA 82 5588–5592.CrossRefGoogle Scholar
  106. Vlassara H, Striker L J, Teichberg S, Fuh H, Li Y M and Steffes M (1994) Advanced glycation end-products induce glomerular sclerosis and albuminurea in normal rats. Proc. Natl. Acad. Sci. USA. 91 11704–11708.CrossRefGoogle Scholar
  107. Voziyan P A and Hudson B G (2005) Pyridoxamine. The many virtues of a Maillard Reaction inhibitor. Ann. NY Acad. Sci. USA 1043 807–816.CrossRefGoogle Scholar
  108. Waite J H, Housley T J and Tanzer M L (1985) Peptide repeats in mussel glue protein. Theme and Variations Biochem 24 5010–5014.Google Scholar
  109. Waite J H, Qin X X and Coyne K J (1998) The peculiar collagens of mussel byssus. Matrix Biol 17 93–106.CrossRefGoogle Scholar
  110. Waite J H, Vaccaro E , Sun C and Lucas J (2003) Collagens with elastin and silk-like domains. In Elastomeric Proteins (Eds. P R Shewry, A S Tatham and A J Bailey) Cambridge University Press, Cambridge, UK, pp 189–212.Google Scholar
  111. Wolfenbuttle B H R, Boulanger C M, Crjins F R L, Huijberts M S P, Poitevin P, Swennen G N M, Vasan S, Egan J J, Ulrich P, Cerami A and Levy B I (1998) Breakers of advanced glycation end-products restore large artery properties in experimental diabetes. Proc. Natl. Acad. Sci. USA 95 4630–4640.CrossRefGoogle Scholar
  112. Woo S L Y, Gomez M A, Woo Y K and Akeson W K (1982) Mechanical properties of tendons and ligaments II. The relationships of immobilization and exercise on tissue remodelling. Biorheology 19 397–408.Google Scholar
  113. Yamauchi M. London R E, Guenat C, Hashimoto F and Mechanic G L (1987) Structure and formation of a stable histidine-based trifunctional cross-link in skin. J Biol. Chem. 262 11428–11434.Google Scholar
  114. Yamauchi M, Prisayanh P Haque Z and Woodley D T (1991) Collagen cross-linking in sun exposed and unexposed sites of aged human skin. J. Invest. Dermatol. 97 938–941.CrossRefGoogle Scholar

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  • N.C. Avery
  • A.J. Bailey

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