Lysyl Hydroxylase 3-mediated Glucosylation in Type I Collagen

Sricholpech, Marnisa; Perdivara, Irina; Yokoyama, Megumi; Nagaoka, Hideaki; Terajima, Masahiko; Tomer, Kenneth B.; Yamauchi, Mitsuo

doi:10.1074/jbc.m112.343954

Cited by 81 publications

(129 citation statements)

References 79 publications

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“…Both of the aforementioned O-linked glycosylations are unique to fibrillar collagens (63) and have been previously reported in other proteomics datasets (60,62,71,72). Although their biological function still remains somewhat unclear (73), they are believed to play a role in modulating the structural stability of collagen (74,75).…”

Section: Table I Proteins Identified In Ice Age Bison Skull (Identifimentioning

confidence: 69%

“…Similarities in glycosylation patterns between our dataset and modern datasets suggest that these modifications are bona fide PTMs and not post mortem artifacts. For example, the hydroxylysine glycosylation of COL1A2 site K175 has recently been identified in collagen isolated from mouse osteoblast cells at 80% stoichiometry (62) and from a modern bovine femur at ϳ60% stoichiometry (60). In our B. latifrons dataset, nearly all tryptic peptides containing K175 from COL1A2 are glycosylated, hinting at the possible correlation between glycosylation and protection from diagensis.…”

Section: Table I Proteins Identified In Ice Age Bison Skull (Identifimentioning

confidence: 82%

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Preserved Proteins from Extinct Bison latifrons Identified by Tandem Mass Spectrometry; Hydroxylysine Glycosides are a Common Feature of Ancient Collagen

Hill

Wither

Nemkov

et al. 2015

Molecular & Cellular Proteomics

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Bone samples from several vertebrates were collected from the Ziegler Reservoir fossil site, in Snowmass Village, Colorado, and processed for proteomics analysis. The specimens come from Pleistocene megafauna Bison latifrons, dating back ϳ120,000 years. Proteomics analysis using a simplified sample preparation procedure and tandem mass spectrometry (MS/MS) was applied to obtain protein identifications. Several bioinformatics resources were used to obtain peptide identifications based on sequence homology to extant species with annotated genomes. With the exception of soil sample controls, all samples resulted in confident peptide identifications that mapped to type I collagen. In addition, we analyzed a specimen from the extinct B. latifrons that yielded peptide identifications mapping to over 33 bovine proteins. Our analysis resulted in extensive fibrillar collagen sequence coverage, including the identification of posttranslational modifications. Hydroxylysine glucosylgalactosylation, a modification thought to be involved in collagen fiber formation and bone mineralization, was identified for the first time in an ancient protein dataset. Meta-analysis of data from other studies indicates that this modification may be common in well-preserved prehistoric samples. Additional peptide sequences from extracellular matrix (ECM) and non-ECM proteins have also been identified for the first time in ancient tissue samples. These data provide a framework for analyzing ancient protein signatures in wellpreserved fossil specimens, while also contributing novel insights into the molecular basis of organic matter preservation. As such, this analysis has unearthed common posttranslational modifications of collagen that may assist in its preservation over time. During the last decade, paleontology and taphonomy (the study of decaying organisms over time and the fossilization processes) have begun to overlap with the field of proteomics to shed new light on preserved organic matter in fossilized bones (1-4). These bones represent a time capsule of ancient biomolecules, owing to their natural resistance to post mortem decay arising from a unique combination of mechanical, structural, and chemical properties (4 -7).Although bones can be cursorily described as a composite of collagen (protein) and hydroxyapatite (mineral), fossilized bones undergo three distinct diagenesis pathways: (i) chemical deterioration of the organic phase; (ii) chemical deterioration of the mineral phase; and (iii) (micro)biological attack of the composite (6). In addition, the rate of these degradation pathways are affected by temperature, as higher burial temperatures have been shown to accelerate these processes (6,8). Though relatively unusual, the first of these three pathways results in a slower deterioration process, which is more generally mitigated under (6) specific environmental constraints, such as geochemical stability (stable temperature and acidity) that promote bone mineral preservation. Importantly, slower deterioration results in more pre...

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Section: Table I Proteins Identified In Ice Age Bison Skull (Identifimentioning

confidence: 69%

Section: Table I Proteins Identified In Ice Age Bison Skull (Identifimentioning

confidence: 82%

Preserved Proteins from Extinct Bison latifrons Identified by Tandem Mass Spectrometry; Hydroxylysine Glycosides are a Common Feature of Ancient Collagen

Hill

Wither

Nemkov

et al. 2015

Molecular & Cellular Proteomics

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“…Hydroxylation of specific Lys residues catalyzed by LHs is an important modification because it determines the fate of the cross-linking pathway and provides the glycosylation sites in type I collagen (2,17,18). Mutations in the LH-encoding genes lead to various connective diseases, but it has also become clear that defects in specific ER chaperones/foldases result in aberrant LH functions, suggesting that these ER proteins also control the functionality of LHs.…”

Section: Discussionmentioning

confidence: 99%

“…By applying the hydrolysates to the HPLC system, the glycosylated (GG-and G-) and non-glycosylated cross-links were separated. These forms of cross-links were quantified as moles/mole of collagen, as reported previously (18). As for the mature non-reducible cross-link, Pyr, its glycosylated forms were not quantified because it is labile with base hydrolysis (37).…”

Section: Methodsmentioning

confidence: 99%

Cyclophilin-B Modulates Collagen Cross-linking by Differentially Affecting Lysine Hydroxylation in the Helical and Telopeptidyl Domains of Tendon Type I Collagen

Terajima

Taga

Chen

et al. 2016

Journal of Biological Chemistry

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Covalent intermolecular cross-linking provides collagen fibrils with stability. The cross-linking chemistry is tissue-specific and determined primarily by the state of lysine hydroxylation at specific sites. A recent study on cyclophilin B (CypB) null mice, a model of recessive osteogenesis imperfecta, demonstrated that lysine hydroxylation at the helical cross-linking site of bone type I collagen was diminished in these animals (Cabral, W. A., Perdivara, I., Weis, M., Terajima, M., Blissett, A. R., Chang, W., Perosky, J. E., Makareeva, E. N., Mertz, E. L., Leikin, S., Tomer, K. B., Kozloff, K. M., Eyre, D. R., Yamauchi, M., and Marini, J. C. (2014) PLoS Genet. 10, e1004465). However, the extent of decrease appears to be tissue-and molecular site-specific, the mechanism of which is unknown. Here we report that although CypB deficiency resulted in lower lysine hydroxylation in the helical cross-linking sites, it was increased in the telopeptide cross-linking sites in tendon type I collagen. This resulted in a decrease in the lysine aldehyde-derived cross-links but generation of hydroxylysine aldehyde-derived cross-links. The latter were absent from the wild type and heterozygous mice. Glycosylation of hydroxylysine residues was moderately increased in the CypB null tendon. We found that CypB interacted with all lysyl hydroxylase isoforms (isoforms 1-3) and a putative lysyl hydroxylase-2 chaperone, 65-kDa FK506-binding protein. Tendon collagen in CypB null mice showed severe size and organizational abnormalities. The data indicate that CypB modulates collagen cross-linking by differentially affecting lysine hydroxylation in a site-specific manner, possibly via its interaction with lysyl hydroxylases and associated molecules. This study underscores the critical importance of collagen post-translational modifications in connective tissue formation.Collagens comprise a large family of structurally related extracellular matrix proteins (1). Among all of the genetic types of collagen identified, fibrillar type I collagen is the most abundant, providing tissues and organs with form and stability. It is a heterotrimeric molecule composed of two ␣1 chains and one ␣2 chain forming a long uninterrupted triple helix with short non-helical domains (telopeptide) at both N and C termini. One of the functionally important characteristics of collagen is its unique, sequential post-translational modifications of Lys residues. The modifications include hydroxylation and monoand diglycosylation of hydroxylysine (Hyl), 3 and oxidative deamination of Lys and Hyl in the N-and C-telopeptides followed by extensive covalent intermolecular cross-linking (2). It is now clear that defective Lys modifications of collagen cause and/or are associated with a broad range of connective tissue disorders, including Ehlers-Danlos syndrome type VIA (3), bronchopulmonary dysplasia (4), Kuskokwim syndrome (5), Bruck syndrome (6, 7), fibrosis (8), disuse osteoporosis (9), and cancer progression (10, 11). Our recent finding showed that a switch of collage...

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“…This is well reflected in the next three papers, where the authors describe part of their work that reflects their expertise in glycomics and its applications in biomedicine (Flangea et al), [26][27][28][29] in glycomic-based biomarker discovery (Shetty and Philip), [30][31][32][33][34][35] or in glycomic signature (Perdivara et al). [36][37][38] Quantitative proteomics is also elegantly revealed by Shetty and Philip. [35] The same mass spectrometry principles are then applied in designing and using cross-linkers for study of proteins and protein-protein interactions (Calabrese and Pukala), [39] already demonstrated in previous studies.…”

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confidence: 98%

Mass Spectrometry and its Applications in Life Sciences

Darie

2013

Aust. J. Chem.

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Deciphering the biological and clinical significance of the proteins is investigated by mass spectrometry in a relatively new field, named proteomics. Mass spectrometry is, however, also used in chemistry for many years. In this Research Front we try to show the potential use of mass spectrometry in chemical, environmental and biomedical research and also to illustrate the applications of mass spectrometry in proteomics.

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Lysyl Hydroxylase 3-mediated Glucosylation in Type I Collagen

Cited by 81 publications

References 79 publications

Preserved Proteins from Extinct Bison latifrons Identified by Tandem Mass Spectrometry; Hydroxylysine Glycosides are a Common Feature of Ancient Collagen

Preserved Proteins from Extinct Bison latifrons Identified by Tandem Mass Spectrometry; Hydroxylysine Glycosides are a Common Feature of Ancient Collagen

Cyclophilin-B Modulates Collagen Cross-linking by Differentially Affecting Lysine Hydroxylation in the Helical and Telopeptidyl Domains of Tendon Type I Collagen

Mass Spectrometry and its Applications in Life Sciences

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