Collagen diversity, synthesis and assembly

Collagen: Structure and Mechanics

Volumn , Issue , 2008, Pages 15-47

  Hulmes, D J S ^a  

^a CNRS Lyon   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84886130799     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-73906-9_2     Document Type: Chapter

References (113)

1. Baldock C, Sherratt MJ, Shuttleworth CA, Kielty CM (2003) The supramolecular organization of collagen VI microfibrils. J Mol Biol 330: 297-307.
2. Barik S (2006) Immunophilins: for the love of proteins. Cell Mol Life Sci 63: 2889-2900.
3. Beck K, Brodsky B (1998) Supercoiled protein motifs: The collagen triple-helix and the alpha-helical coiled coil. J Struct Biol 122: 17-29.
4. Birk DE, Bruckner P (2005) Collagen superstuctures. Top Curr Chem 247: 185-205.
5. Birk DE, Trelstad RL (1986) Extracellular compartments in tendon morphogenesis: Collagen fibril, bundle, and macroaggregate formation. J Cell Biol 103: 231-240.
6. Birk DE, Fitch JM, Babiarz JP, Doane KJ, Linsenmayer TF (1990) Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J Cell Sci 95 (Pt 4): 649-657.
7. Birk DE, Nurminskaya MV, Zycband EI (1995) Collagen fibrillogenesis in situ: Fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev Dyn 202: 229-243.
8. Birk DE, Zycband EI, Winkelmann DA, Trelstad RL (1989) Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly. Proc Natl Acad Sci U S A 86: 4549-4553.
9. Blaschke UK, Eikenberry EF, Hulmes DJS, Galla HJ, Bruckner P (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J Biol Chem 275: 10370-10378.
10. Bonfanti L, Mironov AA, Jr., MartÆnez-Mençrguez JA, Martella O, Fusella A, Baldassarre M, Buccione R, Geuze HJ, Mironov AA, Luini A (1998) Procollagen traverses the Golgi stack without leaving the lumen of Cisternae: Evidence for cisternal maturation. Cell 95: 993-1003.
11. Borel A, Eichenberger D, Farjanel J, Kessler E, Gleyzal C, Hulmes DJS, Sommer P, Font B (2001) Lysyl oxidase-like protein from bovine aorta. Isolation and maturation to an active form by bone morphogenetic protein-1. J Biol Chem 276: 48944-48949.
12. Bottomley MJ, Batten MR, Lumb RA, Bulleid NJ (2001) Quality control in the endoplasmic retic-ulum. PDI mediates the ER retention of unassembled procollagen C-propeptides. Curr Biol 11: 1114-1118.
13. Brittingham R, Uitto J, Fertala A (2006) High-affinity binding of the NC1 domain of collagen VII to laminin 5 and collagen IV. Biochem Biophys Res Commun 343: 692-699.
14. Brodsky B, Persikov AV (2005) Molecular structure of the collagen triple helix. Adv Protein Chem 70: 301-339.
15. Cabral WA, Chang W, Barnes AM, Weis M, Scott MA, Leikin S, Makareeva E, Kuznetsova NV, Rosenbaum KN, Tifft CJ, Bulas DI, Kozma C, Smith PA, Eyre DR, Marini JC (2007) Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39: 359-365.
16. Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118: 1341-1353.
17. Canty EG, Lu Y, Meadows RS, Shaw MK, Holmes DF, Kadler KE (2004) Coalignment of plasma membrane channels and protrusions (fibripositors) specifies the parallelism of tendon. J Cell Biol 165: 553-563.
18. Chakravarti S, Magnuson T, Lass JH, Jepsen KJ, LaMantia C, Carroll H (1998) Lumican regulates collagen fibril assembly: Skin fragility and corneal opacity in the absence of lumican. J Cell Biol 141: 1277-1286.
19. Chiquet M, Renedo AS, Huber F, Fluck M (2003) How do fibroblasts translate mechanical signals into changes in extracellular matrix production? Matrix Biol 22: 73-80.
20. Colige A, Beschin A, Samyn B, Goebels Y, van Beeumen J, Nusgens BV, Lapiere CM (1995) Characterization and partial amino acid sequencing of a 107-kDa procollagen I N-proteinase purified by affinity chromatography on immobilized type XIV collagen. J Biol Chem 270: 16724-16730.
21. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743.
22. Ellgaard L, Ruddock LW (2005) The human protein disulphide isomerase family: Substrate interactions and functional properties. EMBO Rep 6: 28-32.
23. Eyre DR, Pietka T, Weis MA, Wu JJ (2004) Covalent cross-linking of the NC1 domain of collagen type IX to collagen type II in cartilage. J Biol Chem 279: 2568-2574.
24. Fields GB, Lauer JL, Dori Y, Forns P, Yu YC, Tirrell M (1998) Protein-like molecular architecture: Biomaterial applications for inducing cellular receptor binding and signal transduction. Biopolymers 47: 143-151.
25. Fleischmajer R, MacDonald ED, Perlish JS, Burgeson RE, Fisher LW (1990) Dermal collagen fibrils are hybrids of type I and type III collagen molecules. J Struct Biol 105: 162-169.
26. Franzke CW, Bruckner P, Bruckner-Tuderman L (2005) Collagenous transmembrane proteins: recent insights into biology and pathology. J Biol Chem 280: 4005-4008.
27. Fromme JC, Schekman R (2005) COPII-coated vesicles: flexible enough for large cargo? Curr Opin Cell Biol 17: 345-352.
28. Ge G, Seo NS, Liang X, Hopkins DR, Hook M, Greenspan DS (2004) Bone morphogenetic protein-1/tolloid-related metalloproteinases process osteoglycin and enhance its ability to regulate collagen fibrillogenesis. J Biol Chem 279: 41626-41633.
29. Ghai R, Waters P, Roumenina LT, Gadjeva M, Kojouharova MS, Reid KB, Sim RB, Kishore U (2007) C1q and its growing family. Immunobiology 212: 253-266.
30. Giraud-Guille MM (1992) Liquid crystallinity in condensed type I collagen solutions. A clue to the packing of collagen in extracellular matrices. J Mol Biol 224: 861-873.
31. Giraud-Guille MM (1996) Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int Rev Cytol 166: 59-101.
32. Graham HK, Holmes DF, Watson RB, Kadler KE (2000) Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on unipolar fibrils and is regulated by collagen-proteoglycan interaction. J Mol Biol 295: 891-902.
33. Grenard P, Bresson-Hadni S, El Alaoui S, Chevallier M, Vuitton DA, Ricard-Blum S (2001) Transglutaminase-mediated cross-linking is involved in the stabilization of extracellular matrix in human liver fibrosis. J Hepatol 35: 367-375.
34. Halasz K, Kassner A, Morgelin M, Heinegard D (2007) COMP acts as a catalyst in collagen fibril-logenesis. J Biol Chem, 282: 31166-31173.
35. Holmes DF, Capaldi MJ, Chapman JA (1986) Reconstitution of collagen fibrils in vitro; the assembly process depends on the initiating procedure. Int J Biol Macromol 8: 161-166.
36. Holmes DF, Chapman JA, Prockop DJ, Kadler KE (1992) Growing tips of type-I collagen fibrils formed in vitro are near-paraboloidal in shape, implying a reciprocal relationship between accretion and diameter. Proc Nat Acad Sci U S A 89: 9855-9859.
37. Holmes DF, Watson RB, Chapman JA, Kadler KE (1996) Enzymic control of collagen fibril shape. J Mol Biol 261: 93-97.
38. Holmskov U, Thiel S, Jensenius JC (2003) Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21: 547-578.
39. Hopkins DR, Keles S, Greenspan DS (2007) The bone morphogenetic protein 1/Tolloid-like met-alloproteinases. Matrix Biol, 26: 508-523.
40. Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG (2003) Alport's syndrome, Goodpas-ture's syndrome, and type IV collagen. N Engl J Med 348: 2543-2556.
41. Hulmes DJS (2002) Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137: 2-10.
42. Hulmes DJS, Bruns RR, Gross J (1983) On the state of aggregation of newly secreted procollagen. Proc Natl Acad Sci U S A 80: 388-392.
43. Hulmes DJS, Kadler KE, Mould AP, Hojima Y, Holmes DF, Cummings C, Chapman JA, Prockop DJ (1989) Pleomorphism in type I collagen fibrils produced by persistence of the procollagen N-propeptide. J Mol Biol 210: 337-345.
44. Iozzo RV (1999) The biology of the small leucine-rich proteoglycans-Functional network of interactive proteins. J Biol Chem 274: 18843-18846.
45. Ishida Y, Kubota H, Yamamoto A, Kitamura A, Bachinger HP, Nagata K (2006) Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol Biol Cell 17: 2346-2355.
46. Kadler KE (1995) Extracellular matrix 1: fibril-forming collagens. Protein Profile 2: 491-619.
47. Kadler KE, Holmes DF, Trotter JA, Chapman JA (1996) Collagen fibril formation. Biochem J 316: 1-11.
48. Kadler KE, Baldock C, Bella J, Boot-Handford RP (2007) Collagens at a glance. J Cell Sci 120: 1955-1958.
49. Kar K, Amin P, Bryan MA, Persikov AV, Mohs A, Wang YH, Brodsky B (2006) Self-association of collagen triple helix peptides into higher order structures. J Biol Chem 281: 33283-33290.
50. Knupp C, Squire JM (2005) Molecular packing in network-forming collagens. Adv Protein Chem 70: 375-403.
51. Koch M, Schulze J, Hansen U, Ashwodt T, Keene DR, Brunken WJ, Burgeson RE, Bruckner P, Bruckner-Tuderman L (2004) A novel marker of tissue junctions: collagen XXII. J Biol Chem 279: 22514-22521.
52. Koide T (2005) Triple helical collagen-like peptides: engineering and applications in matrix biology. Connect Tissue Res 46: 131-141.
53. Koide T, Nagata K (2005) Collagen biosynthesis. Top Curr Chem 247: 85-114.
54. Koide T, Homma DL, Asada S, Kitagawa K (2005) Self-complementary peptides for the formation of collagen-like triple helical supramolecules. Bioorg Med Chem Lett 15: 5230-5233.
55. Kotch FW, Raines RT (2006) Self-assembly of synthetic collagen triple helices. Proc Natl Acad Sci U S A 103: 3028-3033.
56. Kuhn K (1987) The classical collagens: types I, II and III. In Structure and Function of Collagen Ty pe s, Mayne R, Burgeson RE (eds) pp. 1-42. Academic Press: Orlando.
57. Kvist AJ, Johnson AE, Morgelin M, Gustafsson E, Bengtsson E, Lindblom K, Aszodi A, Fassler R, Sasaki T, Timpl R, Aspberg A (2006) Chondroitin sulfate perlecan enhances collagen fibril formation. Implications for perlecan chondrodysplasias. J Biol Chem 281: 33127-33139.
58. Kwan APL, Cummings CE, Chapman JA, Grant ME (1991) Macromolecular organization of chicken type X collagen in vitro. J Cell Biol 114: 597-604.
59. Lees JF, Tasab M, Bulleid NJ (1997) Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J 16: 908-916.
60. Le Goff C, Somerville RP, Kesteloot F, Powell K, Birk DE, Colige AC, Apte SS (2006) Regulation of procollagen amino-propeptide processing during mouse embryogenesis by specialization of homologous ADAMTS proteases: insights on collagen biosynthesis and dermatosparaxis. Development 133: 1587-1596.
61. Leighton M, Kadler KE (2003) Paired basic/Furin-like proprotein convertase cleavage of Pro-BMP-1 in the trans-Golgi network. J Biol Chem 278: 18478-18484.
62. Leikina E, Mertts MV, Kuznetsova N, Leikin S (2002) Type I collagen is thermally unstable at body temperature. Proc Natl Acad Sci U S A 99: 1314-1318.
63. Li Y, Lacerda DA, Warman ML, Beier DR, Yoshioka H, Ninomiya Y, Oxford JT, Morris NP, Andrikopoulos K, Ramirez F, Wardell BB, Lifferth GD, Teuscher C, Woodward SR, Taylor BA, Seegmiller RE, Olsen BR (1995) A fibrillar collagen gene, Col11a1, is essential for skeletal morphogenesis. Cell 80: 423-430.
64. Li S, Van Den DC, D'Souza SJ, Chan BM, Pickering JG (2003) Vascular smooth muscle cells orchestrate the assembly of type I collagen via alpha2beta1 integrin, RhoA, and fibronectin polymerization. Am J Pathol 163: 1045-1056.
65. Linsenmayer TF, Fitch JM, Gordon MK, Cai CX, Igoe F, Marchant JK, Birk DE (1998) Development and roles of collagenous matrices in the embryonic avian cornea. Prog Retin Eye Res 17: 231-265.
66. Liu X, Wu H, Byrne M, Krane S, Jaenisch R (1997) Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development. Proc Natl Acad Sci U S A 94: 1852-1856.
67. Lucero HA, Kagan HM (2006) Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol Life Sci 63: 2304-2316.
68. MacBeath JR, Shackleton DR, Hulmes DJS (1993) Tyrosine-rich acidic matrix protein (TRAMP) accelerates collagen fibril formation in vitro. J Biol Chem 268: 19826-19832.
69. Martin R, Farjanel J, Eichenberger D, Colige A, Kessler E, Hulmes DJS, Giraud-Guille MM (2000) Liquid crystalline ordering of procollagen as a determinant of three-dimensional extracellular matrix architecture. J Mol Biol 301: 11-17.
70. Martin R, Waldmann L, Kaplan DL (2003) Supramolecular assembly of collagen triblock peptides. Biopolymers 70: 435-444.
71. McAlinden A, Smith TA, Sandell LJ, Ficheux D, Parry DAD, Hulmes DJS (2003) a-helical coiled-coil oligomerization domains are almost ubiquitous in the collagen superfamily. J Biol Chem 278: 42200-42207.
72. McEwan PA, Scott PG, Bishop PN, Bella J (2006) Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans. J Struct Biol 155: 294-305.
73. Minamitani T, Ikuta T, Saito Y, Takebe G, Sato M, Sawa H, Nishimura T, Nakamura F, Takahashi K, Ariga H, Matsumoto K (2004) Modulation of collagen fibrillogenesis by tenascin-X and type VI collagen. Exp Cell Res 298: 305-315.
74. Mironov AA, Mironov AA, Jr., Beznoussenko GV, Trucco A, Lupetti P, Smith JD, Geerts WJ, Koster AJ, Burger KN, Martone ME, Deerinck TJ, Ellisman MH, Luini A (2003) ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev Cell 5: 583-594.
75. Moali C, Font B, Ruggiero F, Eichenberger D, Rousselle P, Francois V, Oldberg A, Bruckner-Tuderman L, Hulmes DJS (2005) Substrate-specific modulation of a multisubstrate proteinase. C-terminal processing of fibrillar procollagens is the only BMP-1-dependent activity to be enhanced by PCPE-1. J Biol Chem 280: 24188-24194.
76. Molnar J, Fong KS, He QP, Hayashi K, Kim Y, Fong SF, Fogelgren B, Szauter KM, Mink M, Csiszar K (2003) Structural and functional diversity of lysyl oxidase and the LOX-like proteins. Biochim Biophys Acta 1647: 220-224.
77. Morello R, Bertin TK, Chen Y, Hicks J, Tonachini L, Monticone M, Castagnola P, Rauch F, Glorieux FH, Vranka J, Bachinger HP, Pace JM, Schwarze U, Byers PH, Weis M, Fernandes RJ, Eyre DR, Yao Z, Boyce BF, Lee B (2006) CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127: 291-304.
78. Mould AP, Hulmes DJS, Holmes DF, Cummings C, Sear CH, Chapman JA (1990) D-periodic assemblies of type I procollagen. J Mol Biol 211: 581-594.
79. Myllyharju J (2005) Intracellular post-translational modifications of collagens. Top Curr Chem 247: 115-247.
80. Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33-43.
81. Myllyla R, Wang C, Heikkinen J, Juffer A, Lampela O, Risteli M, Ruotsalainen H, Salo A, Sipila L (2007) Expanding the lysyl hydroxylase toolbox: new insights into the localization and activities of lysyl hydroxylase 3 (LH3). J Cell Physiol 212: 323-329.
82. Neame PJ, Kay CJ, McQuillan DJ, Beales MP, Hassell JR (2000) Independent modulation of collagen fibrillogenesis by decorin and lumican. Cell Mol Life Sci 57: 859-863.
83. Paramonov SE, Gauba V, Hartgerink JD (2005) Synthesis of collagen-like peptide polymers by native chemical ligation. Macromolecules 38: 7555-7561.
84. Parkinson J, Kadler KE, Brass A (1994) Simple physical model of collagen fibrillogenesis based on diffusion limited aggregation. J Mol Biol 247: 823-831.
85. Parry DA (2005) Structural and functional implications of sequence repeats in fibrous proteins. Adv Protein Chem 70: 11-35.
86. Peinado H, Del Carmen Iglesias-de la Cruz M, Olmeda D, Csiszar K, Fong KS, Vega S, Nieto MA, Cano A, Portillo F (2005) A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J 24: 3446-3458.
87. Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, Thornton DJ, Briggs MD, Boot-Handford RP (2007) Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem 282: 12791-12795.
88. Porter S, Clark IM, Kevorkian L, Edwards DR (2005) The ADAMTS metalloproteinases. Biochem J 386: 15-27.
89. Prockop DJ, Fertala A (1998) Inhibition of the self-assembly of collagen I into fibrils with synthetic peptides-Demonstration that assembly is driven by specific binding sites on the monomers. J Biol Chem 273: 15598-15604.
90. Rentz TJ, Poobalarahi F, Bornstein P, Sage EH, Bradshaw AD (2007) SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 282: 22062-22071.
91. Ricard-Blum S, Dublet B, van der Rest M (2000) Unconventional Collagens. Oxford University Press: Oxford
92. Ricard-Blum S, Ruggiero F, van der Rest M (2005) The collagen superfamily. Top Curr Chem 247: 35-84.
93. Richardson SH, Starborg T, Lu Y, Humphries SM, Meadows RS, Kadler KE (2007) Tendon development requires regulation of cell condensation and cell shape via cadherin-11-mediated cell-cell junctions. Mol Cell Biol 27: 6218-6228.
94. Romanic AM, Adachi E, Kadler KE, Hojima Y, Prockop DJ (1991) Copolymerization of pNcola-gen III and collagen I. J Biol Chem 266: 12703-12709.
95. Ruotsalainen H, Sipila L, Vapola M, Sormunen R, Salo AM, Uitto L, Mercer DK, Robins SP, Risteli M, Aszodi A, Fassler R, Myllyla R (2006) Glycosylation catalyzed by lysyl hydroxylase 3 is essential for basement membranes. J Cell Sci 119: 625-635.
96. Scott PG, McEwan PA, Dodd CM, Bergmann EM, Bishop PN, Bella J (2004) Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc Natl Acad Sci U S A 101: 15633-15638.
97. Seidah NG, Prat A (2005) Proprotein convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem 38: 79-94.
98. Snellman A, Tuomisto A, Koski A, Latvanlehto A, Pihlajaniemi T (2007) The role of disulfide bonds and alpha-helical coiled-coils in the biosynthesis of type XIII collagen and other collagenous transmembrane proteins. J Biol Chem 282: 14898-14905.
99. Speranza ML, Valentini G, Calligaro A (1987) Influence of fibronectin on the fibrillogenesis of type I and type III collagen. Coll Relat Res 7: 115-123.
100. Stephan S, Sherratt MJ, Hodson N, Shuttleworth CA, Kielty CM (2004) Expression and supramolecular assembly of recombinant alpha1(viii) and alpha2(viii) collagen homotrimers. J Biol Chem 279: 21469-21477.
101. Sullivan MM, Barker TH, Funk SE, Karchin A, Seo NS, Hook M, Sanders J, Starcher B, Wight TN, Puolakkainen P, Sage EH (2006) Matricellular hevin regulates decorin production and collagen assembly. J Biol Chem 281: 27621-27632.
102. Svensson L, Aszùdi A, Reinholt FP, Fèssler R, Heinegard D, Oldberg A (1999) Fibromodulin-null mice have abnormal collagen fibrils, tissue organization, and altered lumican deposition in tendon. J Biol Chem 274: 9636-9647.
103. van der Slot AJ, Zuurmond AM, Bardoel AF, Wijmenga C, Pruijs HE, Sillence DO, Brinckmann J, Abraham DJ, Black CM, Verzijl N, DeGroot J, Hanemaaijer R, TeKoppele JM, Huizinga TW, Bank RA (2003) Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 278: 40967-40972.
104. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S (2002) Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem 277: 37377-37381.
105. Verderio EA, Johnson TS, Griffin M (2005) Transglutaminases in wound healing and inflammation. Prog Exp Tumor Res 38: 89-114.
106. Walmsley AR, Batten MR, Lad U, Bulleid NJ (1999) Intracellular retention of procollagen within the endoplasmic reticulum is mediated by prolyl 4-hydroxylase. J Biol Chem 274: 14884-14892.
107. Wang WM, Lee S, Steiglitz BM, Scott IC, Lebares CC, Allen ML, Brenner MC, Takahara K, Greenspan DS (2003) Transforming growth factor-beta induces secretion of activated ADAMTS-2. A procollagen III N-proteinase. J Biol Chem 278: 19549-19557.
108. Ward NP, Hulmes DJS, Chapman JA (1986) Collagen self-assembly in vitro: electron microscopy of initial aggregates formed during the lag phase. J Mol Biol 190: 107-112.
109. Wenstrup RJ, Florer JB, Brunskill EW, Bell SM, Chervoneva I, Birk DE (2004) Type V collagen controls the initiation of collagen fibril assembly. J Biol Chem 279: 53331-53337.
110. Wenstrup RJ, Florer JB, Davidson JM, Phillips CL, Pfeiffer BJ, Menezes DW, Chervoneva I, Birk DE (2006) Murine model of the Ehlers-Danlos syndrome. col5a1 haploinsufficiency disrupts collagen fibril assembly at multiple stages. J Biol Chem 281: 12888-12895.
111. Williams BR, Gelman RA, Poppke DC, Piez KA (1978) Collagen fibril formation: optimal in vitro conditions and preliminary kinetic results. J Biol Chem 235: 6578-6585.
112. Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, Bonadio J, Boskey A, Heegaard AM, Sommer B, Satomura K, Dominguez P, Zhao C, Kulkarni AB, Robey PG, Young MF (1998) Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet 20: 78-82.
113. Yeowell HN, Walker LC (2000) Mutations in the lysyl hydroxylase 1 gene that result in enzyme deficiency and the clinical phenotype of Ehlers-Danlos syndrome type VI. Mol Genet Metab 71: 212-224.