Abnormal Type I Collagen Post-translational Modification and Crosslinking in a Cyclophilin B KO Mouse Model of Recessive Osteogenesis Imperfecta

English version České info

Osteogenesis imperfecta (OI), or brittle bone disease, is characterized by susceptibility to fractures from minimal trauma and growth deficiency. Deficiency of components of the collagen prolyl 3-hydroxylation complex, CRTAP, P3H1 and CyPB, cause recessive types VII, VIII and IX OI, respectively. We have previously shown that mutual protection within the endoplasmic reticulum accounts for the overlapping severe phenotype of patients with CRTAP and P3H1 mutations. However, the bone dysplasia in patients with CyPB deficiency is distinct in terms of phenotype and type I collagen biochemistry. Using a knock-out mouse model of type IX OI, we have demonstrated that CyPB is the major, although not unique, peptidyl prolyl cis-trans isomerase that catalyzes the rate-limiting step in collagen folding. CyPB is also required for activity of the collagen prolyl 3-hydroxylation complex; collagen α1(I) P986 modification is lost in the absence of CyPB. Unexpectedly, CyPB was found to also influence collagen helical lysyl hydroxylation in a tissue-, cell- and residue-specific manner. Thus CyPB facilitates collagen folding directly, but also indirectly regulates collagen hydroxylation, glycosylation, crosslinking and fibrillogenesis through its interactions with other collagen modifying enzymes in the endoplasmic reticulum.

Vyšlo v časopise: Abnormal Type I Collagen Post-translational Modification and Crosslinking in a Cyclophilin B KO Mouse Model of Recessive Osteogenesis Imperfecta. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004465
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004465

Souhrn

Zdroje

1. MyllyharjuJ, KivirikkoKI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33–43.

2. KnottL, BaileyAJ (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22: 181–187.

3. Eyre DR, Wu J (2005) Collagen Cross-Links. In: Brinckmann J, Notbohm H, Muller PK, Eds. Collagen: Primer in Structure, Processing and Assembly. Berlin: Springer Berlin Heidelberg. pp. 207–229.

4. MariniJC, ForlinoA, CabralWA, BarnesAM, San AntonioJD, et al. (2007) Consortium for osteogenesis imperfecta mutations in the helical domain of type I collagen: regions rich in lethal mutations align with collagen binding sites for integrins and proteoglycans. Hum Mutat 28: 209–221.

5. ForlinoA, CabralWA, BarnesAM, MariniJC (2011) New perspectives on osteogenesis imperfecta. Nat Rev Endocrinol 7: 540–557.

6. MariniJC, CabralWA, BarnesAM, ChangW (2007) Components of the collagen prolyl 3-hydroxylation complex are crucial for normal bone development. Cell Cycle 6: 1675–1681.

7. VrankaJA, SakaiLY, BachingerHP (2004) Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J Biol Chem 279: 23615–23621.

8. MorelloR, BertinTK, ChenY, HicksJ, TonachiniL, et al. (2006) CRTAP is required for prolyl 3- hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127: 291–304.

9. IshikawaY, WirzJ, VrankaJA, NagataK, BachingerHP (2009) Biochemical characterization of the prolyl 3-hydroxylase 1/CRTAP/cyclophilin B complex. J Biol Chem 284: 17641–17647.

10. CabralWA, ChangW, BarnesAM, WeisM, ScottMA, et al. (2007) Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39: 359–365.

11. van DijkFS, NesbittIM, ZwikstraEH, NikkelsPG, PiersmaSR, et al. (2009) PPIB mutations cause severe osteogenesis imperfecta. Am J Hum Genet 85: 521–527.

12. ChangW, BarnesAM, CabralWA, BodurthaJN, MariniJC (2009) Prolyl 3-hydroxylase 1 and CRTAP are mutually stabilizing in the endoplasmic reticulum collagen prolyl 3-hydroxylation complex. Hum Mol Genet 19: 223–234.

13. GalatA (2003) Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity–targets–functions. Curr Top Med Chem 3: 1315–1347.

14. GothelSF, MarahielMA (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55: 423–436.

15. MeunierL, UsherwoodYK, ChungKT, HendershotLM (2002) A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13: 4456–4469.

16. JansenG, MaattanenP, DenisovAY, ScarffeL, SchadeB, et al. (2012) An interaction map of endoplasmic reticulum chaperones and foldases. Mol Cell Proteomics 11: 710–723.

17. SteinmannB, BrucknerP, Superti-FurgaA (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: 1299–1303.

18. BachingerHP, BrucknerP, TimplR, ProckopDJ, EngelJ (1980) Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Role of disulfide bridges and peptide bond isomerization. Eur J Biochem 106: 619–632.

19. BarnesAM, CarterEM, CabralWA, WeisM, ChangW, et al. (2010) Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding. N Engl J Med 362: 521–528.

20. PyottSM, SchwarzeU, ChristiansenHE, PepinMG, LeistritzDF, 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: 1595–1609.

21. IshikawaY, VrankaJA, BoudkoSP, PokidyshevaE, MizunoK, 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: 22253–22265.

22. VrankaJA, PokidyshevaE, HayashiL, ZientekK, MizunoK, et al. (2010) Prolyl 3-hydroxylase 1 null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones. J Biol Chem 285: 17253–17262.

23. BarnesAM, ChangW, MorelloR, CabralWA, WeisM, et al. (2006) Deficiency of cartilage-associated protein in recessive lethal osteogenesis imperfecta. N Engl J Med 355: 2757–2764.

24. SricholpechM, PerdivaraI, NagaokaH, YokoyamaM, TomerKB, et al. (2011) Lysyl hydroxylase 3 glucosylates galactosylhydroxylysine residues in type I collagen in osteoblast culture. J Biol Chem 286: 8846–8856.

25. SricholpechM, PerdivaraI, YokoyamaM, NagaokaH, TerajimaM, et al. (2012) Lysyl hydroxylase 3-mediated glucosylation in type I collagen: molecular loci and biological significance. J Biol Chem 287: 22998–23009.

26. ScheggB, HulsmeierAJ, RutschmannC, MaagC, HennetT (2009) Core glycosylation of collagen is initiated by two beta(1-O)galactosyltransferases. Mol Cell Biol 29: 943–952.

27. HeikkinenJ, RisteliM, WangC, LatvalaJ, RossiM, et al. (2000) Lysyl hydroxylase 3 is a multifunctional protein possessing collagen glucosyltransferase activity. J Biol Chem 275: 36158–36163.

28. SaloAM, CoxH, FarndonP, MossC, GrindulisH, et al. (2008) A connective tissue disorder caused by mutations of the lysyl hydroxylase 3 gene. Am J Hum Genet 83: 495–503.

29. MyllylaR, WangC, HeikkinenJ, JufferA, LampelaO, et al. (2007) Expanding the lysyl hydroxylase toolbox: new insights into the localization and activities of lysyl hydroxylase 3 (LH3). J Cell Physiol 212: 323–329.

30. ChoiJW, SutorSL, LindquistL, EvansGL, MaddenBJ, et al. (2009) Severe osteogenesis imperfecta in cyclophilin B-deficient mice. PLoS Genet 5: e1000750.

31. BaldridgeD, LenningtonJ, WeisM, HomanEP, JiangMM, et al. (2010) Generalized connective tissue disease in Crtap−/− mouse. PLoS One 5: e10560.

32. PokidyshevaE, ZientekKD, IshikawaY, MizunoK, VrankaJA, et al. (2013) Posttranslational Modifications in Type I Collagen from Different Tissues extracted from wild type and Prolyl 3-hydroxylase 1 Null Mice. J Biol Chem 288: 24742–24752.

33. RaghunathM, BrucknerP, SteinmannB (1994) Delayed triple helix formation of mutant collagen from patients with osteogenesis imperfecta. J Mol Biol 236: 940–949.

34. BachingerHP, MorrisNP, DavisJM (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: 152–162.

35. ZengB, MacDonaldJR, BannJG, BeckK, GambeeJE, 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(Pt 1): 109–114.

36. BarnesAM, CabralWA, WeisM, MakareevaE, MertzEL, 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: 1589–1598.

37. SchwarzeU, CundyT, PyottSM, ChristiansenHE, HegdeMR, 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.

38. BarnesAM, DuncanG, WeisM, PatonW, CabralWA, et al. (2013) Kuskokwim Syndrome, a Recessive Congenital Contracture Disorder, Extends the Phenotype of FKBP10 Mutations. Hum Mutat 34: 1279–1288.

39. BaumannM, GiuntaC, KrabichlerB, RuschendorfF, ZoppiN, 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: 201–216.

40. EyreD, ShaoP, WeisMA, SteinmannB (2002) The kyphoscoliotic type of Ehlers-Danlos syndrome (type VI): differential effects on the hydroxylation of lysine in collagens I and II revealed by analysis of cross-linked telopeptides from urine. Mol Genet Metab 76: 211–216.

41. UzawaK, GrzesikWJ, NishiuraT, KuznetsovSA, RobeyPG, 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: 1272–1280.

42. UzawaK, YeowellHN, YamamotoK, MochidaY, TanzawaH, et al. (2003) Lysine hydroxylation of collagen in a fibroblast cell culture system. Biochem Biophys Res Commun 305: 484–487.

43. van der SlotAJ, ZuurmondAM, BardoelAF, WijmengaC, PruijsHE, et al. (2003) Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 278: 40967–40972.

44. EyreDR, GlimcherMJ (1972) Reducible crosslinks in hydroxylysine-deficient collagens of a heritable disorder of connective tissue. Proc Natl Acad Sci U S A 69: 2594–2598.

45. PasqualiM, StillMJ, ValesT, RosenRI, EvingerJD, et al. (1997) Abnormal formation of collagen cross-links in skin fibroblasts cultured from patients with Ehlers-Danlos syndrome type VI. Proc Assoc Am Physicians 109: 33–41.

46. PinnellSR, KraneSM, KenzoraJE, GlimcherMJ (1972) A heritable disorder of connective tissue. Hydroxylysine-deficient collagen disease. N Engl J Med 286: 1013–1020.

47. PassojaK, RautavuomaK, Ala-KokkoL, KosonenT, KivirikkoKI (1998) Cloning and characterization of a third human lysyl hydroxylase isoform. Proc Natl Acad Sci U S A 95: 10482–10486.

48. WangC, LuosujarviH, HeikkinenJ, RisteliM, UittoL, et al. (2002) The third activity for lysyl hydroxylase 3: galactosylation of hydroxylysyl residues in collagens in vitro. Matrix Biol 21: 559–566.

49. RisteliM, NiemitaloO, LankinenH, JufferAH, MyllylaR (2004) Characterization of collagenous peptides bound to lysyl hydroxylase isoforms. J Biol Chem 279: 37535–37543.

50. SipilaL, RuotsalainenH, SormunenR, BakerNL, LamandeSR, et al. (2007) Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines. J Biol Chem 282: 33381–33388.

51. VetterU, WeisMA, MorikeM, EanesED, EyreDR (1993) Collagen crosslinks and mineral crystallinity in bone of patients with osteogenesis imperfecta. J Bone Miner Res 8: 133–137.

52. BankRA, TekoppeleJM, JanusGJ, WassenMH, PruijsHE, et al. (2000) Pyridinium cross-links in bone of patients with osteogenesis imperfecta: evidence of a normal intrafibrillar collagen packing. J Bone Miner Res 15: 1330–1336.

53. FujiiK, TanzerML (1977) Osteogenesis imperfecta: biochemical studies of bone collagen. Clin Orthop Relat Res 271–277.

54. EyreDR, WeisMA (2013) Bone Collagen: New Clues to Its Mineralization Mechanism from Recessive Osteogenesis Imperfecta. Calcif Tissue Int 93: 338–347.

55. HudsonDM, KimLS, WeisM, CohnDH, EyreDR (2012) Peptidyl 3-hydroxyproline binding properties of type I collagen suggest a function in fibril supramolecular assembly. Biochemistry 51: 2417–2424.

56. TakaluomaK, HyryM, LanttoJ, SormunenR, BankRA, et al. (2007) Tissue-specific changes in the hydroxylysine content and cross-links of collagens and alterations in fibril morphology in lysyl hydroxylase 1 knock-out mice. J Biol Chem 282: 6588–6596.

57. SteinmannB, EyreDR, ShaoP (1995) Urinary pyridinoline cross-links in Ehlers-Danlos syndrome type VI. Am J Hum Genet 57: 1505–1508.

58. YamauchiM, NoyesC, KubokiY, MechanicGL (1982) Collagen structural microheterogeneity and a possible role for glycosylated hydroxylysine in type I collagen. Proc Natl Acad Sci U S A 79: 7684–7688.

59. EyreDR, GlimcherMJ (1973) Analysis of a crosslinked peptide from calf bone collagen: evidence that hydroxylysyl glycoside participates in the crosslink. Biochem Biophys Res Commun 52: 663–671.

60. AmblardD, Lafage-ProustMH, ChamsonA, RattnerA, ColletP, et al. (2003) Lower bone cellular activities in male and female mature C3H/HeJ mice are associated with higher bone mass and different pyridinium crosslink profiles compared to C57BL/6J mice. J Bone Miner Metab 21: 377–387.

61. BanseX, DevogelaerJP, LafosseA, SimsTJ, GrynpasM, et al. (2002) Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 31: 70–76.

62. BanseX, SimsTJ, BaileyAJ (2002) Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res 17: 1621–1628.

63. StrykeD, KawamotoM, HuangCC, JohnsSJ, KingLA, et al. (2003) BayGenomics: a resource of insertional mutations in mouse embryonic stem cells. Nucleic Acids Res 31: 278–281.

64. McLeodMJ (1980) Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22: 299–301.

65. SinderBP, EddyMM, OminskyMS, CairdMS, MariniJC, et al. (2013) Sclerostin antibody improves skeletal parameters in a Brtl/+ mouse model of osteogenesis imperfecta. J Bone Miner Res 28: 73–80.

66. BakkerAD, Klein-NulendJ (2012) Osteoblast isolation from murine calvaria and long bones. Methods Mol Biol 816: 19–29.

67. BonadioJ, HolbrookKA, GelinasRE, JacobJ, ByersPH (1985) Altered triple helical structure of type I procollagen in lethal perinatal osteogenesis imperfecta. J Biol Chem 260: 1734–1742.

68. MakareevaE, MertzEL, KuznetsovaNV, SutterMB, DeRidderAM, et al. (2008) Structural heterogeneity of type I collagen triple helix and its role in osteogenesis imperfecta. J Biol Chem 283: 4787–4798.

69. YamauchiM, KatzEP (1993) The post-translational chemistry and molecular packing of mineralizing tendon collagens. Connect Tissue Res 29: 81–98.

70. YamauchiM, ShiibaM (2008) Lysine hydroxylation and cross-linking of collagen. Methods Mol Biol 446: 95–108.

71. EyreD (1987) Collagen cross-linking amino acids. Methods Enzymol 144: 115–139.

72. ForlinoA, D'AmatoE, ValliM, CameraG, HopkinsE, et al. (1997) Phenotypic comparison of an osteogenesis imperfecta type IV proband with a de novo alpha2(I) Gly922 → Ser substitution in type I collagen and an unrelated patient with an identical mutation. Biochem Mol Med 62: 26–35.

73. CabralWA, MerttsMV, MakareevaE, ColigeA, TekinM, et al. (2003) Type I collagen triplet duplication mutation in lethal osteogenesis imperfecta shifts register of alpha chains throughout the helix and disrupts incorporation of mutant helices into fibrils and extracellular matrix. J Biol Chem 278: 10006–10012.

74. BatemanJF, GolubSB (1994) Deposition and selective degradation of structurally-abnormal type I collagen in a collagen matrix produced by osteogenesis imperfecta fibroblasts in vitro. Matrix Biol 14: 251–262.

75. CabralWA, MakareevaE, ColigeA, LetochaAD, TyJM, et al. (2005) Mutations near amino end of alpha1(I) collagen cause combined osteogenesis imperfecta/Ehlers-Danlos syndrome by interference with N-propeptide processing. J Biol Chem 280: 19259–19269.