Molecular insights into prolyl and lysyl hydroxylation of fibrillar collagens in health and disease

Critical Reviews in Biochemistry and Molecular Biology

Volumn 52, Issue 1, 2017, Pages 74-95

  Gjaltema, Rutger A F ^a   Bank, Ruud A ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Bruck syndrome; Collagen; connective tissue disorders; Ehlers Danlos syndrome; fibrosis; lysyl hydroxylation; osteogenesis imperfecta; prolyl hydroxylation

Indexed keywords

CYCLOPHILIN B; FIBRILLAR COLLAGEN; LYSINE DERIVATIVE; PROCOLLAGEN LYSINE 2 OXOGLUTARATE 5 DIOXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLINE DERIVATIVE; PROTEIN DISULFIDE ISOMERASE; HYDROXYLYSINE; HYDROXYPROLINE; LYSINE; PROLINE;

ALPHA CHAIN; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CELL TRANSPORT; CHONDROCYTE; COLLAGEN FIBRIL; COMPLEX FORMATION; CROSS LINKING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; GLYCOSYLATION; HUMAN; HYDROXYLATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; SYNAPTONEMAL COMPLEX; THERMOSTABILITY; TRIPLE HELIX; ANIMAL; ARTHROGRYPOSIS; CONNECTIVE TISSUE DISEASE; EHLERS DANLOS SYNDROME; METABOLISM; OSTEOGENESIS IMPERFECTA; PATHOLOGY;

ANIMALS; ARTHROGRYPOSIS; CONNECTIVE TISSUE DISEASES; EHLERS-DANLOS SYNDROME; FIBRILLAR COLLAGENS; GLYCOSYLATION; HUMANS; HYDROXYLATION; HYDROXYLYSINE; HYDROXYPROLINE; LYSINE; OSTEOGENESIS IMPERFECTA; PROLINE; PROTEIN FOLDING;

EID: 85009460249     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.1080/10409238.2016.1269716     Document Type: Review

References (183)

1. Acil Y, Vetter U, Brenner R, et al. (1995). Ehlers-Danlos syndrome type VI:cross-link pattern in tissue and urine sample as a diagnostic marker. J Am Acad Dermatol 33:522–4.
2. Alanay Y, Avaygan H, Camacho N, et al. (2010). Mutations in the gene encoding the RER protein FKBP65 cause autosomal-recessive osteogenesis imperfecta. Am J Hum Genet 86:551–9.
3. Aldeeri AA, Alazami AM, Hijazi H, et al. (2014). Excessively redundant umbilical skin as a potential early clinical feature of Morquio syndrome and FKBP14-related Ehlers-Danlos syndrome. Clin Genet 86:469–72.
4. Amor IM, Rauch F, Gruenwald K, et al. (2011). Severe osteogenesis imperfecta caused by a small in-frame deletion in CRTAP. Am J Med Gene A 155A:2865–70.
5. Annunen P, Autio-Harmainen H, Kivirikko KI., (1998). The novel type II prolyl 4-hydroxylase is the main enzyme form in chondrocytes and capillary endothelial cells, whereas the type I enzyme predominates in most cells. J Biol Chem 273:5989–92.
6. Annunen P, Helaakoski T, Myllyharju J, et al. (1997). Cloning of the human prolyl 4-hydroxylase alpha subunit isoform alpha(II) and characterization of the type II enzyme tetramer. The alpha(I) and alpha(II) subunits do not form a mixed alpha(I)alpha(II)beta2 tetramer. J Biol Chem 272:17342–8.
7. Bachinger HP, Morris NP, Davis JM., (1993). Thermal stability and folding of the collagen triple helix and the effects of mutations in osteogenesis imperfecta on the triple helix of type I collagen. Am J Med Genet 45:152–62.
8. Backlund J, Carlsen S, Hoger T, et al. (2002). Predominant selection of T cells specific for the glycosylated collagen type II epitope (263–270) in humanized transgenic mice and in rheumatoid arthritis. Proc Natl Acad Sci USA 99:9960–5.
9. Baldridge D, Schwarze U, Morello R, et al. (2008). CRTAP and LEPRE1 mutations in recessive osteogenesis imperfecta. Hum Mutat 29:1435–42.
10. Banerjee S, Isaacman-Beck J, Schneider VA, Granato M., (2013). A novel role for Lh3 dependent ECM modifications during neural crest cell migration in zebrafish. PLoS One 8:e54609.
11. Bank RA, Robins SP, Wijmenga C, et al. (1999a). Defective collagen crosslinking in bone, but not in ligament or cartilage, in Bruck syndrome:indications for a bone-specific telopeptide lysyl hydroxylase on chromosome 17. Proc Natl Acad Sci USA 96:1054–8.
12. Bank RA, Tekoppele JM, Oostingh G, et al. (1999b). Lysylhydroxylation and non-reducible crosslinking of human supraspinatus tendon collagen:changes with age and in chronic rotator cuff tendinitis. Ann Rheum Dis 58:35–41.
13. Bank RA, Verzijl N, Lafeber FP, Tekoppele JM., (2002). Putative role of lysyl hydroxylation and pyridinoline cross-linking during adolescence in the occurrence of osteoarthritis at old age. Osteoarthr Cartil 10:127–34.
14. Barnes AM, Cabral WA, Weis M, et al. (2012). Absence of FKBP10 in recessive type XI osteogenesis imperfecta leads to diminished collagen cross-linking and reduced collagen deposition in extracellular matrix. Hum Mutat 33:1589–98.
15. Barnes AM, Carter EM, Cabral WA, et al. (2010). Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding. N Engl J Med 362:521–8.
16. Barnes AM, Chang W, Morello R, et al. (2006). Deficiency of cartilage-associated protein in recessive lethal osteogenesis imperfecta. N Engl J Med 355:2757–64.
17. Barnes AM, Duncan G, Weis M, et al. (2013). Kuskokwim syndrome, a recessive congenital contracture disorder, extends the phenotype of FKBP10 mutations. Hum Mutat 34:1279–88.
18. Basak T, Vega-Montoto L, Zimmerman LJ, et al. (2016). Comprehensive characterization of glycosylation and hydroxylation of basement membrane collagen IV by high-resolution mass spectrometry. J Proteome Res 15:245–58.
19. Batge B, Winter C, Notbohm H, et al. (1997). Glycosylation of human bone collagen I in relation to lysylhydroxylation and fibril diameter. J Biochem 122:109–15.
20. Baumann M, Giunta C, Krabichler B, et al. (2012). Mutations in FKBP14 cause a variant of Ehlers-Danlos syndrome with progressive kyphoscoliosis, myopathy, and hearing loss. Am J Hum Genet 90:201–16.
21. Berg RA, Prockop DJ., (1973). The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. Biochem Biophys Res Commun 52:115–20.
22. Bhadriraju K, Chung KH, Spurlin TA, et al. (2009). The relative roles of collagen adhesive receptor DDR2 activation and matrix stiffness on the downregulation of focal adhesion kinase in vascular smooth muscle cells. Biomaterials 30:6687–94.
23. Boudko SP, Ishikawa Y, Lerch TF, et al. (2012). Crystal structures of wild-type and mutated cyclophilin B that causes hyperelastosis cutis in the American quarter horse. BMC Res Notes 5:626.
24. Boudko SP, Ishikawa Y, Nix J, et al. (2014). Structure of human peptidyl-prolyl cis-trans isomerase FKBP22 containing two EF-hand motifs. Protein Sci 23:67–75.
25. Boute N, Exposito JY, Boury-Esnault N, et al. (1996). Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol Cell 88:37–44.
26. Breslau-Siderius EJ, Engelbert RH, Pals G, Van Der Sluijs JA., (1998). Bruck syndrome:a rare combination of bone fragility and multiple congenital joint contractures. J Pediatr Orthop B 7:35–8.
27. Brinckmann J, Notbohm H, Tronnier M, et al. (1999). Overhydroxylation of lysyl residues is the initial step for altered collagen cross-links and fibril architecture in fibrotic skin. J Invest Dermatol 113:617–21.
28. Bunt S, Denholm B, Skaer H., (2011). Characterisation of the Drosophila procollagen lysyl hydroxylase, dPlod. Gene Expr Patterns 11:72–8.
29. Byers PH, Pyott SM., (2012). Recessively inherited forms of osteogenesis imperfecta. Annu Rev Genet 46:475–97.
30. Cabral WA, Chang W, Barnes AM, et al. (2007). Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39:359–65.
31. Cabral WA, Perdivara I, Weis M, et al. (2014). Abnormal type I collagen post-translational modification and crosslinking in a cyclophilin B KO mouse model of recessive osteogenesis imperfecta. PLoS Genet 10:e1004465.
32. Caparros-Martin JA, Valencia M, Pulido V, et al. (2013). Clinical and molecular analysis in families with autosomal recessive osteogenesis imperfecta identifies mutations in five genes and suggests genotype-phenotype correlations. Am J Med Genet a 161A:1354–69.
33. Capellini TD, Dunn MP, Passamaneck YJ, et al. (2008). Conservation of notochord gene expression across chordates:insights from the Leprecan gene family. Genesis 46:683–96.
34. Chang W, Barnes AM, Cabral WA, et al. (2010). Prolyl 3-hydroxylase 1 and CRTAP are mutually stabilizing in the endoplasmic reticulum collagen prolyl 3-hydroxylation complex. Hum Mol Genet 19:223–34.
35. Chen Y, Terajima M, Yang Y, et al. (2015). Lysyl hydroxylase 2 induces a collagen cross-link switch in tumor stroma. J Clin Invest 125:1147–62.
36. Cheung KL, Bates M, Ananthanarayanan VS., (2010). Effect of FKBP65, a putative elastin chaperone, on the coacervation of tropoelastin in vitro. Biochem Cell Biol 88:917–25.
37. Choi JW, Sutor SL, Lindquist L, et al. (2009). Severe osteogenesis imperfecta in cyclophilin B-deficient mice. PLoS Genet 5:e1000750.
38. Corthay A, Backlund J, Broddefalk J, et al. (1998). Epitope glycosylation plays a critical role for T cell recognition of type II collagen in collagen-induced arthritis. Eur J Immunol 28:2580–90.
39. Curino AC, Engelholm LH, Yamada SS, et al. (2005). Intracellular collagen degradation mediated by uPARAP/Endo180 is a major pathway of extracellular matrix turnover during malignancy. J Cell Biol 169:977–85.
40. Davis EC, Broekelmann TJ, Ozawa Y, Mecham RP., (1998). Identification of tropoelastin as a ligand for the 65-kD FK506-binding protein, FKBP65, in the secretory pathway. J Cell Biol 140:295–303.
41. De Jong L, Van Der Kraan I, De Waal A., (1991). The kinetics of the hydroxylation of procollagen by prolyl 4-hydroxylase. Proposal for a processive mechanism of binding of the dimeric hydroxylating enzyme in relation to the high kcat/Km ratio and a conformational requirement for hydroxylation of -X-Pro-Gly- sequences. Biochimica Et Biophysica Acta 1079:103–11.
42. Duran I, Nevarez L, Sarukhanov A, et al. (2015). HSP47 and FKBP65 cooperate in the synthesis of type I procollagen. Hum Mol Genet 24:1918–28.
43. Eisinger-Mathason TS, Zhang M, Qiu Q, et al. (2013). Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Discov 3:1190–205.
44. Exposito JY, Valcourt U, Cluzel C, Lethias C., (2010). The fibrillar collagen family. Int J Mol Sci 11:407–26.
45. Eyre DR, Weis M, Hudson DM, et al. (2011). A novel 3-hydroxyproline (3Hyp)-rich motif marks the triple-helical C terminus of tendon type I collagen. J Biol Chem 286:7732–6.
46. Eyre DR, Weis MA., (2013). Bone collagen:new clues to its mineralization mechanism from recessive osteogenesis imperfecta. Calcif Tissue Int 93:338–47.
47. Fernandes RJ, Farnand AW, Traeger GR, et al. (2011). A role for prolyl 3-hydroxylase 2 in post-translational modification of fibril-forming collagens. J Biol Chem 286:30662–9.
48. Forlino A, Marini JC., (2016). Osteogenesis imperfecta. Lancet 387:1657–71.
49. Gilkes DM, Bajpai S, Wong CC, et al. (2013). Procollagen lysyl hydroxylase 2 is essential for hypoxia-induced breast cancer metastasis. Mol Cancer Res 11:456–66.
50. Giunta C, Elcioglu NH, Albrecht B, et al. (2008). Spondylocheiro dysplastic form of the Ehlers-Danlos syndrome–an autosomal-recessive entity caused by mutations in the zinc transporter gene SLC39A13. Am J Hum Genet 82:1290–305.
51. Gjaltema RA, van der Stoel MM, Boersema M, Bank RA., (2016). Disentangling mechanisms involved in collagen pyridinoline cross-linking:the immunophilin FKBP65 is critical for dimerization of lysyl hydroxylase 2. Proc Natl Acad Sci USA. 113:7142–7.
52. Grafe I, Yang T, Alexander S, et al. (2014). Excessive transforming growth factor-beta signaling is a common mechanism in osteogenesis imperfecta. Nat Med 20:670–5.
53. Grimmer C, Balbus N, Lang U, et al. (2006). Regulation of type II collagen synthesis during osteoarthritis by prolyl-4-hydroxylases:possible influence of low oxygen levels. Am J Pathol 169:491–502.
54. Guo H, Tong P, Peng Y, et al. (2014). Homozygous loss-of-function mutation of the LEPREL1 gene causes severe non-syndromic high myopia with early-onset cataract. Clin Genet 86:575–9.
55. Ha-Vinh R, Alanay Y, Bank RA, et al. (2004). Phenotypic and molecular characterization of Bruck syndrome (osteogenesis imperfecta with contractures of the large joints) caused by a recessive mutation in PLOD2. Am J Med Genet a 131:115–20.
56. Heard ME, Besio R, Weis M, et al. (2016). Sc65-null mice provide evidence for a novel endoplasmic reticulum complex regulating collagen lysyl hydroxylation. PLoS Genet 12:e1006002.
57. Heikkinen J, Risteli M, Lampela O, et al. (2011). Dimerization of human lysyl hydroxylase 3 (LH3) is mediated by the amino acids 541-547. Matrix Biol 30:27–33.
58. Heikkinen J, Risteli M, Wang C, et al. (2000). Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J Biol Chem 275:36158–63.
59. Hieta R, Kukkola L, Permi P, et al. (2003). The peptide-substrate-binding domain of human collagen prolyl 4-hydroxylases. Backbone assignments, secondary structure, and binding of proline-rich peptides. J Biol Chem 278:34966–74.
60. Holster T, Pakkanen O, Soininen R, et al. (2007). Loss of assembly of the main basement membrane collagen, type IV, but not fibril-forming collagens and embryonic death in collagen prolyl 4-hydroxylase I null mice. J Biol Chem 282:2512–19.
61. Homan EP, Lietman C, Grafe I, et al. (2014). Differential effects of collagen prolyl 3-hydroxylation on skeletal tissues. PLoS Genet 10:e1004121.
62. Hudson DM, Joeng KS, Werther R, et al. (2015). Post-translationally abnormal collagens of prolyl 3-hydroxylase-2 null mice offer a pathobiological mechanism for the high myopia linked to human LEPREL1 mutations. J Biol Chem 290:8613–22.
63. Hudson DM, Weis M, Eyre DR., (2011). Insights on the evolution of prolyl 3-hydroxylation sites from comparative analysis of chicken and Xenopus fibrillar collagens. PLoS One 6:e19336.
64. Hyland J, Ala-Kokko L, Royce P, et al. (1992). A homozygous stop codon in the lysyl hydroxylase gene in two siblings with Ehlers-Danlos syndrome type VI. Nat Genet 2:228–31.
65. Ihme A, Krieg T, Nerlich A, et al. (1984). Ehlers-Danlos syndrome type VI:collagen type specificity of defective lysyl hydroxylation in various tissues. J Invest Dermatol 83:161–5.
66. Ishikawa Y, Bachinger HP., (2013a). An additional function of the rough endoplasmic reticulum protein complex prolyl 3-hydroxylase 1.cartilage-associated protein.cyclophilin B:the CXXXC motif reveals disulfide isomerase activity in vitro. J Biol Chem 288:31437–46.
67. Ishikawa Y, Bachinger HP., (2013b). A molecular ensemble in the rER for procollagen maturation. Biochim Biophys Acta 1833:2479–91.
68. Ishikawa Y, Bachinger HP., (2014). A substrate preference for the rough endoplasmic reticulum resident protein FKBP22 during collagen biosynthesis. J Biol Chem 289:18189–201.
69. Ishikawa Y, Boudko S, Bachinger HP., (2015). Ziploc-ing the structure:Triple helix formation is coordinated by rough endoplasmic reticulum resident PPIases. Biochim Biophys Acta 1850:1983–93.
70. Ishikawa Y, Vranka J, Wirz J, et al. (2008). The rough endoplasmic reticulum-resident FK506-binding protein FKBP65 is a molecular chaperone that interacts with collagens. J Biol Chem 283:31584–90.
71. Ishikawa Y, Vranka JA, Boudko SP, et al. (2012). Mutation in cyclophilin B that causes hyperelastosis cutis in American Quarter Horse does not affect peptidylprolyl cis-trans isomerase activity but shows altered cyclophilin B-protein interactions and affects collagen folding. J Biol Chem 287:22253–65.
72. Ishikawa Y, Wirz J, Vranka JA, et al. (2009). Biochemical characterization of the prolyl 3-hydroxylase 1.cartilage-associated protein.cyclophilin B complex. J Biol Chem 284:17641–7.
73. Jeong J, Walker JM, Wang F, et al. (2012). Promotion of vesicular zinc efflux by ZIP13 and its implications for spondylocheiro dysplastic Ehlers-Danlos syndrome. Proc Natl Acad Sci USA 109:E3530–8.
74. Jurgensen HJ, Johansson K, Madsen DH, et al. (2014). Complex determinants in specific members of the mannose receptor family govern collagen endocytosis. J Biol Chem 289:7935–47.
75. Jurgensen HJ, Madsen DH, Ingvarsen S, et al. (2011). A novel functional role of collagen glycosylation:interaction with the endocytic collagen receptor uparap/ENDO180. J Biol Chem 286:32736–48.
76. Keene DR, San Antonio JD, Mayne R, et al. (2000). Decorin binds near the C terminus of type I collagen. J Biol Chem 275:21801–4.
77. Kelley BP, Malfait F, Bonafe L, et al. (2011). Mutations in FKBP10 cause recessive osteogenesis imperfecta and Bruck syndrome. J Bone Miner Res 26:666–72.
78. Kivirikko KI, Myllyharju J., (1998). Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 16:357–68.
79. Kivirikko KI, Pihlajaniemi T., (1998). Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. Adv Enzymol Relat Areas Mol Biol 72:325–98.
80. Kivirikko KI, Suga K, Kishida Y, et al. (1971). Asymmetry in the hydroxylation of (Pro-Pro-Gly) 5 by protocollagen proline hydroxylase. Biochem Biophys Res Commun 45:1591–6.
81. Kukkola L, Hieta R, Kivirikko KI, et al. (2003a). Identification and characterization of a third human, rat, and mouse collagen prolyl 4-hydroxylase isoenzyme. J Biol Chem 278:47685–93.
82. Kukkola L, Hieta R, Kivirikko KI, et al. (2003b). Identification and characterization of a third human, rat, and mouse collagen prolyl 4-hydroxylase isoenzyme. J Biol Chem 278:47685–93.
83. Lamberg A, Jauhiainen M, Metso J, et al. (1996). The role of protein disulphide isomerase in the microsomal triacylglycerol transfer protein does not reside in its isomerase activity. Biochem J 315:533–6.
84. Lauer-Fields JL, Malkar NB, Richet G, et al. (2003). Melanoma cell CD44 interaction with the alpha 1(IV)1263-1277 region from basement membrane collagen is modulated by ligand glycosylation. J Biol Chem 278:14321–30.
85. Leitinger B., (2014). Discoidin domain receptor functions in physiological and pathological conditions. Int Rev Cell Mol Biol 310:39–87.
86. Liefhebber JM, Punt S, Spaan WJ, Van Leeuwen HC., (2010). The human collagen beta(1-O)galactosyltransferase, GLT25D1, is a soluble endoplasmic reticulum localized protein. BMC Cell Biol 11:33.
87. Lietman CD, Rajagopal A, Homan EP, et al. (2014). Connective tissue alterations in Fkbp10-/- mice. Hum Mol Genet 23:4822–31.
88. Luther KB, Hulsmeier AJ, Schegg B, et al. (2011). Mimivirus collagen is modified by bifunctional lysyl hydroxylase and glycosyltransferase enzyme. J Biol Chem 286:43701–9.
89. Marini JC, Cabral WA, Barnes AM, Chang W., (2007). Components of the collagen prolyl 3-hydroxylation complex are crucial for normal bone development. Cell Cycle 6:1675–81.
90. Martinez-Glez V, Valencia M, Caparros-Martin JA, et al. (2012). Identification of a mutation causing deficient BMP1/mTLD proteolytic activity in autosomal recessive osteogenesis imperfecta. Human Mutation 33:343–50.
91. Mercer DK, Nicol PF, Kimbembe C, Robins SP., (2003a). Identification, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307:803–9.
92. Mercer DK, Nicol PF, Kimbembe C, Robins SP., (2003b). Identification, expression, and tissue distribution of the three rat lysyl hydroxylase isoforms. Biochem Biophys Res Commun 307:803–9.
93. Miao M, Reichheld SE, Muiznieks LD, et al. (2013). Elastin binding protein and FKBP65 modulate in vitro self-assembly of human tropoelastin. Biochemistry 52:7731–41.
94. Michaelsson E, Malmstrom V, Reis S, et al. (1994). T cell recognition of carbohydrates on type II collagen. J Exp Med 180:745–9.
95. Moravej H, Karamifar H, Karamizadeh Z, et al. (2015). Bruck syndrome - a rare syndrome of bone fragility and joint contracture and novel homozygous FKBP10 mutation. Endokrynol Pol 66:170–4.
96. Mordechai S, Gradstein L, Pasanen A, et al. (2011). High myopia caused by a mutation in LEPREL1, encoding prolyl 3-hydroxylase 2. Am J Hum Genet 89:438–45.
97. Morello R, Bertin TK, Chen Y, et al. (2006). CRTAP is required for prolyl 3- hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127:291–304.
98. Murray ML, Yang M, Fauth C, Byers PH., (2014). FKBP14-related Ehlers-Danlos syndrome:expansion of the phenotype to include vascular complications. Am J Med Genet A 164A:1750–5.
99. Myers LK, Myllyharju J, Nokelainen M, et al. (2004). Relevance of posttranslational modifications for the arthritogenicity of type II collagen. J Immunol 172:2970–5.
100. Myllyharju J., (2003). Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 22:15–24.
101. Myllyharju J, Kivirikko KI., (2004). Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20:33–43.
102. Myllyharju J, Nokelainen M, Vuorela A, Kivirikko KI., (2000). Expression of recombinant human type I-III collagens in the yeast pichia pastoris. Biochem Soc Trans 28:353–7.
103. Nietfeld JJ, Van Der Kraan I, Kemp A., (1981). Dissociation and reassociation of prolyl 4-hydroxylase subunits after cross-linking of monomers. Biochim Biophys Acta 661:21–7.
104. Nissi R, Autio-Harmainen H, Marttila P, et al. (2001). Prolyl 4-hydroxylase isoenzymes I and II have different expression patterns in several human tissues. J Histochem Cytochem 49:1143–53.
105. Nokelainen M, Helaakoski T, Myllyharju J, et al. (1998). Expression and characterization of recombinant human type II collagens with low and high contents of hydroxylysine and its glycosylated forms. Matrix Biol 16:329–38.
106. Nokelainen M, Tu H, Vuorela A, et al. (2001). High-level production of human type I collagen in the yeast Pichia pastoris. Yeast 18:797–806.
107. Norman KR, Moerman DG., (2000). The let-268 locus of Caenorhabditis elegans encodes a procollagen lysyl hydroxylase that is essential for type IV collagen secretion. Dev Biol 227:690–705.
108. Passoja K, Rautavuoma K, Ala-Kokko L, et al. (1998). Cloning and characterization of a third human lysyl hydroxylase isoform. Proc Natl Acad Sci USA 95:10482–6.
109. Perdivara I, Yamauchi M, Tomer KB., (2013). Molecular characterization of collagen hydroxylysine O-glycosylation by mass spectrometry:current status. Aust J Chem 66:760–9.
110. Perrin-Tricaud C, Rutschmann C, Hennet T., (2011). Identification of domains and amino acids essential to the collagen galactosyltransferase activity of GLT25D1. PLoS One 6:e29390.
111. Pokidysheva E, Tufa S, Bresee C, et al. (2013a). Prolyl 3-hydroxylase-1 null mice exhibit hearing impairment and abnormal morphology of the middle ear bone joints. Matrix Biol 32:39–44.
112. Pokidysheva E, Zientek KD, Ishikawa Y, et al. (2013b). Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice. J Biol Chem 288:24742–52.
113. Pornprasertsuk S, Duarte WR, Mochida Y, Yamauchi M., (2004). Lysyl hydroxylase-2b directs collagen cross-linking pathways in MC3T3-E1 cells. J Bone Miner Res 19:1349–55.
114. Puig-Hervas MT, Temtamy S, Aglan M, et al. (2012). Mutations in PLOD2 cause autosomal-recessive connective tissue disorders within the Bruck syndrome–osteogenesis imperfecta phenotypic spectrum. Hum Mutat 33:1444–9.
115. Pyott SM, Schwarze U, Christiansen HE, et al. (2011). Mutations in PPIB (cyclophilin B) delay type I procollagen chain association and result in perinatal lethal to moderate osteogenesis imperfecta phenotypes. Hum Mol Genet 20:1595–609.
116. Rauch F, Fahiminiya S, Majewski J, et al. (2015). Cole-Carpenter syndrome is caused by a heterozygous missense mutation in P4HB. Am J Hum Genet 96:425–31.
117. Rautavuoma K, Takaluoma K, Passoja K, et al. (2002). Characterization of three fragments that constitute the monomers of the human lysyl hydroxylase isoenzymes 1-3. The 30-kDa N-terminal fragment is not required for lysyl hydroxylase activity. J Biol Chem 277:23084–91.
118. Rautavuoma K, Takaluoma K, Sormunen R, et al. (2004). Premature aggregation of type IV collagen and early lethality in lysyl hydroxylase 3 null mice. Proc Natl Acad Sci USA 101:14120–5.
119. Ricard-Blum S, Esterre P, Grimaud JA., (1993). Collagen cross-linking by pyridinoline occurs in non-reversible skin fibrosis. Cell Mol Biol (Noisy-Le-Grand) 39:723–7.
120. Risteli J, Bachinger HP, Engel J, et al. (1980a). 7-S collagen:characterization of an unusual basement membrane structure. Eur J Biochem 108:239–50.
121. Risteli L, Risteli J, Ihme A, et al. (1980b). Preferential hydroxylation of type IV collagen by lysyl hydroxylase from Ehlers-Danlos syndrome type VI fibroblasts. Biochem Biophys Res Commun 96:1778–84.
122. Risteli M, Niemitalo O, Lankinen H, et al. (2004). Characterization of collagenous peptides bound to lysyl hydroxylase isoforms. J Biol Chem 279:37535–43.
123. Risteli M, Ruotsalainen H, Salo AM, et al. (2009). Reduction of lysyl hydroxylase 3 causes deleterious changes in the deposition and organization of extracellular matrix. J Biol Chem 284:28204–11.
124. Ruotsalainen H, Risteli M, Wang C, et al. (2012). The activities of lysyl hydroxylase 3 (LH3) regulate the amount and oligomerization status of adiponectin. PLoS One 7:e50045
125. Ruotsalainen H, Sipila L, Kerkela E, et al. (1999). Characterization of cDNAs for mouse lysyl hydroxylase 1, 2 and 3, their phylogenetic analysis and tissue-specific expression in the mouse. Matrix Biol 18:325–9.
126. Ruotsalainen H, Sipila L, Vapola M, et al. (2006). Glycosylation catalyzed by lysyl hydroxylase 3 is essential for basement membranes. J Cell Sci 119:625–35.
127. Ruotsalainen H, Vanhatupa S, Tampio M, et al. (2001). Complete genomic structure of mouse lysyl hydroxylase 2 and lysyl hydroxylase 3/collagen glucosyltransferase. Matrix Biol 20:137–46.
128. Salo AM, Cox H, Farndon P, et al. (2008). A connective tissue disorder caused by mutations of the lysyl hydroxylase 3 gene. Am J Hum Genet 83:495–503.
129. Salo AM, Sipila L, Sormunen R, et al. (2006a). The lysyl hydroxylase isoforms are widely expressed during mouse embryogenesis, but obtain tissue- and cell-specific patterns in the adult. Matrix Biol 25:475–83.
130. Salo AM, Sipila L, Sormunen R, et al. (2006b). The lysyl hydroxylase isoforms are widely expressed during mouse embryogenesis, but obtain tissue- and cell-specific patterns in the adult. Matrix Biol 25:475–83.
131. Salo AM, Wang C, Sipila L, et al. (2006c). Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J Cell Physiol 207:644–53.
132. Sarkar SK, Young PE, Sullivan CE, Torchia DA., (1984). Detection of cis and trans X-Pro peptide bonds in proteins by 13C NMR:application to collagen. Proc Natl Acad Sci USA 81:4800–3.
133. Schegg B, Hulsmeier AJ, Rutschmann C, et al. (2009). Core glycosylation of collagen is initiated by two beta(1-O)galactosyltransferases. Mol Cell Biol 29:943–52.
134. Schneider VA, Granato M., (2006). The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50:683–95.
135. Schumacher MA, Mizuno K, Bachinger HP., (2006). The crystal structure of a collagen-like polypeptide with 3(S)-hydroxyproline residues in the Xaa position forms a standard 7/2 collagen triple helix. J Biol Chem 281:27566–74.
136. Schwarze U, Cundy T, Pyott SM, et al. (2013). Mutations in FKBP10, which result in Bruck syndrome and recessive forms of osteogenesis imperfecta, inhibit the hydroxylation of telopeptide lysines in bone collagen. Hum Mol Genet 22:1–17.
137. Seth P, Walker LC, Yeowell HN., (2011). Identification of exonic cis-elements regulating the alternative splicing of scleroderma-associated lysyl hydroxylase 2 mRNA. J Investig Dermatol 131:537–9.
138. Seth P, Yeowell HN., (2010). Fox-2 protein regulates the alternative splicing of scleroderma-associated lysyl hydroxylase 2 messenger RNA. Arthritis Rheum 62:1167–75.
139. Setijowati ED, van Dijk FS, Cobben JM, et al. (2012). A novel homozygous 5 bp deletion in FKBP10 causes clinically Bruck syndrome in an Indonesian patient. Eur J Med Genet 55:17–21.
140. Shaheen R, Al-Owain M, Faqeih E, et al. (2011). Mutations in FKBP10 cause both Bruck syndrome and isolated osteogenesis imperfecta in humans. Am J Med Genet A 155A:1448–52.
141. Shaheen R, Al-Owain M, Sakati N, et al. (2010). FKBP10 and Bruck syndrome:phenotypic heterogeneity or call for reclassification? Am J Hum Genet 87:306–7.
142. Sipila L, Ruotsalainen H, Sormunen R, et al. (2007). Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines. J Biol Chem 282:33381–8.
143. Sricholpech M, Perdivara I, Nagaoka H, et al. (2011). Lysyl hydroxylase 3 glucosylates galactosylhydroxylysine residues in type I collagen in osteoblast culture. J Biol Chem 286:8846–56.
144. Sricholpech M, Perdivara I, Yokoyama M, et al. (2012). Lysyl hydroxylase 3-mediated glucosylation in type I collagen:molecular loci and biological significance. J Biol Chem 287:22998–3009.
145. Stawikowski MJ, Aukszi B, Stawikowska R, et al. (2014). Glycosylation modulates melanoma cell α2β1 and α3β1 integrin interactions with type IV collagen. J Biol Chem 289:21591–604.
146. Steinlein OK, Aichinger E, Trucks H, Sander T., (2011). Mutations in FKBP10 can cause a severe form of isolated osteogenesis imperfecta. BMC Med Genet 12:152.
147. Steinmann B, Bruckner P, Superti-Furga A., (1991). Cyclosporin A slows collagen triple-helix formation in vivo:indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase. J Biol Chem 266:1299–303.
148. Steinmann B, Eyre DR, Shao P., (1995). Urinary pyridinoline cross-links in Ehlers-Danlos syndrome type VI. Am J Hum Genet 57:1505–8.
149. Takaluoma K, Lantto J, Myllyharju J., (2007). Lysyl hydroxylase 2 is a specific telopeptide hydroxylase, while all three isoenzymes hydroxylate collagenous sequences. Matrix Biol 26:396–403.
150. Terajima M, Perdivara I, Sricholpech M, et al. (2014). Glycosylation and cross-linking in bone type I collagen. J Biol Chem 289:22636–47.
151. Terajima M, Taga Y, Chen Y, et al. (2016). Cyclophilin-B modulates collagen cross-linking by differentially affecting lysine hydroxylation in the helical and telopeptidyl domains of tendon type I collagen. J Biol Chem 291:9501–12.
152. Tiainen P, Pasanen A, Sormunen R, Myllyharju J., (2008a). Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J Biol Chem 283:19432–9.
153. Tiainen P, Pasanen A, Sormunen R, Myllyharju J., (2008b). Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J Biol Chem 283:19432–9.
154. Uzawa K, Grzesik WJ, Nishiura T, et al. (1999). Differential expression of human lysyl hydroxylase genes, lysine hydroxylation, and cross-linking of type I collagen during osteoblastic differentiation in vitro. J Bone Miner Res 14:1272–80.
155. Van Den Diepstraten C, Papay K, Bolender Z, et al. (2003). Cloning of a novel prolyl 4-hydroxylase subunit expressed in the fibrous cap of human atherosclerotic plaque. Circulation 108:508–11.
156. Van Der Slot AJ, Van Dura EA, De Wit EC, et al. (2005). Elevated formation of pyridinoline cross-links by profibrotic cytokines is associated with enhanced lysyl hydroxylase 2b levels. Biochim Biophys Acta 1741:95–102.
157. Van Der Slot AJ, Zuurmond AM, Bardoel AF, et al. (2003). Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 278:40967–72.
158. Van Der Slot AJ, Zuurmond AM, Van Den Bogaerdt AJ, et al. (2004). Increased formation of pyridinoline cross-links due to higher telopeptide lysyl hydroxylase levels is a general fibrotic phenomenon. Matrix Biol 23:251–7.
159. Van Der Slot-Verhoeven AJ, Van Dura EA, Attema J, et al. (2005). The type of collagen cross-link determines the reversibility of experimental skin fibrosis. Biochim Biophys Acta 1740:60–7.
160. Venables JP, Lapasset L, Gadea G, et al. (2013). MBNL1 and RBFOX2 cooperate to establish a splicing programme involved in pluripotent stem cell differentiation. Nat Commun 4:2480.
161. Venturi G, Monti E, Carbonare LD, et al. (2012). A novel splicing mutation in FKBP10 causing osteogenesis imperfecta with a possible mineralization defect. Bone 50:343–9.
162. Vogel W, Gish GD, Alves F, Pawson T., (1997). The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1:13–23.
163. Vranka J, Stadler HS, Bachinger HP., (2009). Expression of prolyl 3-hydroxylase genes in embryonic and adult mouse tissues. Cell Struct Funct 34:97–104.
164. Vranka JA, Sakai LY, Bachinger HP., (2004). Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J Biol Chem 279:23615–21.
165. Vuori K, Pihlajaniemi T, Marttila M, Kivirikko KI., (1992a). Characterization of the human prolyl 4-hydroxylase tetramer and its multifunctional protein disulfide-isomerase subunit synthesized in a baculovirus expression system. Proc Natl Acad Sci USA 89:7467–70.
166. Vuori K, Pihlajaniemi T, Marttila M, Kivirikko KI., (1992b). Characterization of the human prolyl 4-hydroxylase tetramer and its multifunctional protein disulfide-isomerase subunit synthesized in a baculovirus expression system. Proc Natl Acad Sci USA 89:7467–70.
167. Vuori K, Pihlajaniemi T, Myllyla R, Kivirikko KI., (1992c). Site-directed mutagenesis of human protein disulphide isomerase:effect on the assembly, activity and endoplasmic reticulum retention of human prolyl 4-hydroxylase in Spodoptera frugiperda insect cells. EMBO J 11:4213–17.
168. Walker LC, Overstreet MA, Yeowell HN., (2005). Tissue-specific expression and regulation of the alternatively-spliced forms of lysyl hydroxylase 2 (LH2) in human kidney cells and skin fibroblasts. Matrix Biol 23:515–23.
169. Wang C, Kovanen V, Raudasoja P, et al. (2009). The glycosyltransferase activities of lysyl hydroxylase 3 (LH3) in the extracellular space are important for cell growth and viability. J Cell Mol Med 13:508–21.
170. Wang C, Luosujarvi H, Heikkinen J, et al. (2002a). The third activity for lysyl hydroxylase 3:galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21:559–66.
171. Wang C, Risteli M, Heikkinen J, et al. (2002b). Identification of amino acids important for the catalytic activity of the collagen glucosyltransferase associated with the multifunctional lysyl hydroxylase 3 (LH3). J Biol Chem 277:18568–73.
172. Wang C, Ristiluoma MM, Salo AM, et al. (2012). Lysyl hydroxylase 3 is secreted from cells by two pathways. J. Cell. Physiol 227:668–75.
173. Weis MA, Hudson DM, Kim L, et al. (2010a). Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly. J Biol Chem 285:2580–90.
174. Weis MA, Hudson DM, Kim L, et al. (2010b). Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly. J Biol Chem 285:2580–90.
175. Wenstrup RJ, Willing MC, Starman BJ, Byers PH., (1990). Distinct biochemical phenotypes predict clinical severity in nonlethal variants of osteogenesis imperfecta. Am J Hum Genet 46:975–82.
176. Yamauchi M, Sricholpech M., (2012). Lysine post-translational modifications of collagen. Essays Biochem 52:113–33.
177. Yang C, Niu C, Bodo M, et al. (1993). Fulvic acid supplementation and selenium deficiency disturb the structural integrity of mouse skeletal tissue. An animal model to study the molecular defects of Kashin-Beck disease. Biochem J 289:829–35.
178. Yang CL, Bodo M, Notbohm H, et al. (1991). Fulvic acid disturbs processing of procollagen II in articular cartilage of embryonic chicken and may also cause Kashin-Beck disease. Eur J Biochem 202:1141–6.
179. Yeowell HN, Walker LC., (1999). Tissue specificity of a new splice form of the human lysyl hydroxylase 2 gene. Matrix Biol 18:179–87.
180. 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 71:212–24.
181. Yeowell HN, Walker LC, Mauger DM, et al. (2009). TIA nuclear proteins regulate the alternate splicing of lysyl hydroxylase 2. J Invest Dermatol 129:1402–11.
182. Zeng B, Macdonald JR, Bann JG, et al. (1998). Chicken FK506-binding protein, FKBP65, a member of the FKBP family of peptidylprolyl cis-trans isomerases, is only partially inhibited by FK506. Biochem J 330:109–14.
183. Zhou P, Liu Y, Lv F, et al. (2014). Novel mutations in FKBP10 and PLOD2 cause rare Bruck syndrome in Chinese patients. PLoS One 9:e107594.