Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice

Elena Pokidysheva, Keith D. Zientek, Yoshihiro Ishikawa, Kazunori Mizuno, Janice Vranka, Nathan T. Montgomery, Douglas R. Keene, Tatsuya Kawaguchi, Kenji Okuyama, Hans Peter Bächinger

Research output: Contribution to journalArticle

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Abstract

Background: 3-Hydroxylation of proline residues in type I collagen is rare but important. Results: 3-Hyp sites have been identified in both chains of mouse type I collagen in wild type and P3H1 null mice. Conclusion: The absence of 3-Hyp does not alter the D-period of collagen fibrils, but alters the lateral growth of the fibrils. Significance: Type I collagen prolyl 3-hydroxylation is tissue-specific. Type I collagen extracted from tendon, skin, and bone of wild type and prolyl 3-hydroxylase 1 (P3H1) null mice shows distinct patterns of 3-hydroxylation and glycosylation of hydroxylysine residues. The A1 site (Pro-986) in the α1-chain of type I collagen is almost completely 3-hydroxylated in every tissue of the wild type mice. In contrast, no 3-hydroxylation of this proline residue was found in P3H1 null mice. Partial 3-hydroxylation of the A3 site (Pro-707) was present in tendon and bone, but absent in skin in both α-chains of the wild type animals. Type I collagen extracted from bone of P3H1 null mice shows a large reduction in 3-hydroxylation of the A3 site in bothα-chains, whereas type I collagen extracted from tendon of P3H1 null mice shows little difference as compared with wild type. These results demonstrate that the A1 site in type I collagen is exclusively 3-hydroxylated by P3H1, and presumably, this enzyme is required for the 3-hydroxylation of the A3 site of both α-chains in bone but not in tendon. The increase in glycosylation of hydroxylysine in P3H1 null mice in bone was found to be due to an increased occupancy of normally glycosylated sites. Despite the severe disorganization of collagen fibrils in adult tissues, the D-period of the fibrils is unchanged. Tendon fibrils of newborn P3H1 null mice are well organized with only a slight increase in diameter. The absence of 3-hydroxyproline and/or the increased glycosylation of hydroxylysine in type I collagen disturbs the lateral growth of the fibrils.

Original languageEnglish (US)
Pages (from-to)24742-24752
Number of pages11
JournalJournal of Biological Chemistry
Volume288
Issue number34
DOIs
StatePublished - Aug 23 2013
Externally publishedYes

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Post Translational Protein Processing
Collagen Type I
Hydroxylation
Tissue
Tendons
Hydroxylysine
Bone
Glycosylation
Bone and Bones
Proline
Skin
Collagen
2-oxoglutarate 3-dioxygenase proline
Wild Animals
Growth
Animals
Enzymes

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

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Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice. / Pokidysheva, Elena; Zientek, Keith D.; Ishikawa, Yoshihiro; Mizuno, Kazunori; Vranka, Janice; Montgomery, Nathan T.; Keene, Douglas R.; Kawaguchi, Tatsuya; Okuyama, Kenji; Bächinger, Hans Peter.

In: Journal of Biological Chemistry, Vol. 288, No. 34, 23.08.2013, p. 24742-24752.

Research output: Contribution to journalArticle

Pokidysheva, E, Zientek, KD, Ishikawa, Y, Mizuno, K, Vranka, J, Montgomery, NT, Keene, DR, Kawaguchi, T, Okuyama, K & Bächinger, HP 2013, 'Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice', Journal of Biological Chemistry, vol. 288, no. 34, pp. 24742-24752. https://doi.org/10.1074/jbc.M113.464156
Pokidysheva, Elena ; Zientek, Keith D. ; Ishikawa, Yoshihiro ; Mizuno, Kazunori ; Vranka, Janice ; Montgomery, Nathan T. ; Keene, Douglas R. ; Kawaguchi, Tatsuya ; Okuyama, Kenji ; Bächinger, Hans Peter. / Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice. In: Journal of Biological Chemistry. 2013 ; Vol. 288, No. 34. pp. 24742-24752.
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abstract = "Background: 3-Hydroxylation of proline residues in type I collagen is rare but important. Results: 3-Hyp sites have been identified in both chains of mouse type I collagen in wild type and P3H1 null mice. Conclusion: The absence of 3-Hyp does not alter the D-period of collagen fibrils, but alters the lateral growth of the fibrils. Significance: Type I collagen prolyl 3-hydroxylation is tissue-specific. Type I collagen extracted from tendon, skin, and bone of wild type and prolyl 3-hydroxylase 1 (P3H1) null mice shows distinct patterns of 3-hydroxylation and glycosylation of hydroxylysine residues. The A1 site (Pro-986) in the α1-chain of type I collagen is almost completely 3-hydroxylated in every tissue of the wild type mice. In contrast, no 3-hydroxylation of this proline residue was found in P3H1 null mice. Partial 3-hydroxylation of the A3 site (Pro-707) was present in tendon and bone, but absent in skin in both α-chains of the wild type animals. Type I collagen extracted from bone of P3H1 null mice shows a large reduction in 3-hydroxylation of the A3 site in bothα-chains, whereas type I collagen extracted from tendon of P3H1 null mice shows little difference as compared with wild type. These results demonstrate that the A1 site in type I collagen is exclusively 3-hydroxylated by P3H1, and presumably, this enzyme is required for the 3-hydroxylation of the A3 site of both α-chains in bone but not in tendon. The increase in glycosylation of hydroxylysine in P3H1 null mice in bone was found to be due to an increased occupancy of normally glycosylated sites. Despite the severe disorganization of collagen fibrils in adult tissues, the D-period of the fibrils is unchanged. Tendon fibrils of newborn P3H1 null mice are well organized with only a slight increase in diameter. The absence of 3-hydroxyproline and/or the increased glycosylation of hydroxylysine in type I collagen disturbs the lateral growth of the fibrils.",
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AU - Ishikawa, Yoshihiro

AU - Mizuno, Kazunori

AU - Vranka, Janice

AU - Montgomery, Nathan T.

AU - Keene, Douglas R.

AU - Kawaguchi, Tatsuya

AU - Okuyama, Kenji

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N2 - Background: 3-Hydroxylation of proline residues in type I collagen is rare but important. Results: 3-Hyp sites have been identified in both chains of mouse type I collagen in wild type and P3H1 null mice. Conclusion: The absence of 3-Hyp does not alter the D-period of collagen fibrils, but alters the lateral growth of the fibrils. Significance: Type I collagen prolyl 3-hydroxylation is tissue-specific. Type I collagen extracted from tendon, skin, and bone of wild type and prolyl 3-hydroxylase 1 (P3H1) null mice shows distinct patterns of 3-hydroxylation and glycosylation of hydroxylysine residues. The A1 site (Pro-986) in the α1-chain of type I collagen is almost completely 3-hydroxylated in every tissue of the wild type mice. In contrast, no 3-hydroxylation of this proline residue was found in P3H1 null mice. Partial 3-hydroxylation of the A3 site (Pro-707) was present in tendon and bone, but absent in skin in both α-chains of the wild type animals. Type I collagen extracted from bone of P3H1 null mice shows a large reduction in 3-hydroxylation of the A3 site in bothα-chains, whereas type I collagen extracted from tendon of P3H1 null mice shows little difference as compared with wild type. These results demonstrate that the A1 site in type I collagen is exclusively 3-hydroxylated by P3H1, and presumably, this enzyme is required for the 3-hydroxylation of the A3 site of both α-chains in bone but not in tendon. The increase in glycosylation of hydroxylysine in P3H1 null mice in bone was found to be due to an increased occupancy of normally glycosylated sites. Despite the severe disorganization of collagen fibrils in adult tissues, the D-period of the fibrils is unchanged. Tendon fibrils of newborn P3H1 null mice are well organized with only a slight increase in diameter. The absence of 3-hydroxyproline and/or the increased glycosylation of hydroxylysine in type I collagen disturbs the lateral growth of the fibrils.

AB - Background: 3-Hydroxylation of proline residues in type I collagen is rare but important. Results: 3-Hyp sites have been identified in both chains of mouse type I collagen in wild type and P3H1 null mice. Conclusion: The absence of 3-Hyp does not alter the D-period of collagen fibrils, but alters the lateral growth of the fibrils. Significance: Type I collagen prolyl 3-hydroxylation is tissue-specific. Type I collagen extracted from tendon, skin, and bone of wild type and prolyl 3-hydroxylase 1 (P3H1) null mice shows distinct patterns of 3-hydroxylation and glycosylation of hydroxylysine residues. The A1 site (Pro-986) in the α1-chain of type I collagen is almost completely 3-hydroxylated in every tissue of the wild type mice. In contrast, no 3-hydroxylation of this proline residue was found in P3H1 null mice. Partial 3-hydroxylation of the A3 site (Pro-707) was present in tendon and bone, but absent in skin in both α-chains of the wild type animals. Type I collagen extracted from bone of P3H1 null mice shows a large reduction in 3-hydroxylation of the A3 site in bothα-chains, whereas type I collagen extracted from tendon of P3H1 null mice shows little difference as compared with wild type. These results demonstrate that the A1 site in type I collagen is exclusively 3-hydroxylated by P3H1, and presumably, this enzyme is required for the 3-hydroxylation of the A3 site of both α-chains in bone but not in tendon. The increase in glycosylation of hydroxylysine in P3H1 null mice in bone was found to be due to an increased occupancy of normally glycosylated sites. Despite the severe disorganization of collagen fibrils in adult tissues, the D-period of the fibrils is unchanged. Tendon fibrils of newborn P3H1 null mice are well organized with only a slight increase in diameter. The absence of 3-hydroxyproline and/or the increased glycosylation of hydroxylysine in type I collagen disturbs the lateral growth of the fibrils.

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