Stable isotope-labeled collagen: A novel and versatile tool for quantitative collagen analyses using mass spectrometry

Journal of Proteome Research

Volumn 13, Issue 8, 2014, Pages 3671-3678

  Taga, Yuki ^a   Kusubata, Masashi ^a   Ogawa Goto, Kiyoko ^a   Hattori, Shunji ^a  

^a NIPPI RESEARCH INSTITUTE OF BIOMATRIX   (Japan)

Author keywords

collagen; mass spectrometry; post translational modification; quantification; stable isotope labeling

Indexed keywords

ARGININE; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 3; LYSINE; PROLINE; STABLE ISOTOPE; STABLE ISOTOPE LABELED COLLAGEN; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; HYDROLYSIS; HYDROPHILIC INTERACTION CHROMATOGRAPHY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; PROTEIN PROCESSING; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; RAT; ANIMAL; CHEMICAL ANALYSIS; FIBROBLAST; METABOLISM; PROCEDURES;

ANIMALS; ARGININE; CHEMISTRY TECHNIQUES, ANALYTICAL; CHROMATOGRAPHY, LIQUID; COLLAGEN; FIBROBLASTS; ISOTOPE LABELING; LYSINE; MASS SPECTROMETRY; PROLINE; RATS;

EID: 84905387556     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500213a     Document Type: Article

References (42)

1. Seyer, J. M.; Hutcheson, E. T.; Kang, A. H. Collagen polymorphism in idiopathic chronic pulmonary fibrosis J. Clin. Invest. 1976, 57 (6) 1498-1507
2. Seyer, J. M.; Hutcheson, E. T.; Kang, A. H. Collagen polymorphism in normal and cirrhotic human liver J. Clin. Invest. 1977, 59 (2) 241-248
3. McKleroy, W.; Lee, T. H.; Atabai, K. Always cleave up your mess: targeting collagen degradation to treat tissue fibrosis Am. J. Physiol.: Lung Cell. Mol. Physiol. 2013, 304 (11) L709-L721
4. Forlino, A.; Cabral, W. A.; Barnes, A. M.; Marini, J. C. New perspectives on osteogenesis imperfecta Nat. Rev. Endocrinol 2011, 7 (9) 540-557
5. Haralson, M. A.; Hassell, J. R. Extracellular Matrix: A Practical Approach; Oxford University Press: New York, 1995.
6. Butler, W. T. Hydroxylysine glycosides Methods Enzymol. 1982, 82, 339-346
7. Berg, R. A. Determination of 3- and 4-hydroxyproline Methods Enzymol. 1982, 82, 372-398
8. von der Mark, K. Localization of collagen types in tissues Int. Rev. Connect. Tissue Res. 1981, 9, 265-324
9. Langrock, T.; Czihal, P.; Hoffmann, R. Amino acid analysis by hydrophilic interaction chromatography coupled on-line to electrospray ionization mass spectrometry Amino Acids 2006, 30 (3) 291-297
10. Pataridis, S.; Eckhardt, A.; Mikulikova, K.; Sedlakova, P.; Miksik, I. Identification of collagen types in tissues using HPLC-MS/MS J. Sep Sci. 2008, 31 (20) 3483-3488
11. Weis, M. A.; Hudson, D. M.; Kim, L.; Scott, M.; Wu, J. J.; Eyre, D. R. Location of 3-hydroxyproline residues in collagen types I, II, III, and V/XI implies a role in fibril supramolecular assembly J. Biol. Chem. 2010, 285 (4) 2580-2590
12. Ishikawa, Y.; Vranka, J. A.; Boudko, S. P.; Pokidysheva, E.; Mizuno, K.; Zientek, K.; Keene, D. R.; Rashmir-Raven, A. M.; Nagata, K.; Winand, N. J.; Bachinger, H. P. 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. 2012, 287 (26) 22253-22265
13. Sricholpech, M.; Perdivara, I.; Yokoyama, M.; Nagaoka, H.; Terajima, M.; Tomer, K. B.; Yamauchi, M. Lysyl hydroxylase 3-mediated glucosylation in type I collagen: molecular loci and biological significance J. Biol. Chem. 2012, 287 (27) 22998-3009
14. Yang, C.; Park, A. C.; Davis, N. A.; Russell, J. D.; Kim, B.; Brand, D. D.; Lawrence, M. J.; Ge, Y.; Westphall, M. S.; Coon, J. J.; Greenspan, D. S. Comprehensive mass spectrometric mapping of the hydroxylated amino acid residues of the alpha1(V) collagen chain J. Biol. Chem. 2012, 287 (48) 40598-40610
15. Ong, S. E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-486
16. Ishihama, Y.; Sato, T.; Tabata, T.; Miyamoto, N.; Sagane, K.; Nagasu, T.; Oda, Y. Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards Nat. Biotechnol. 2005, 23 (5) 617-621
17. Geiger, T.; Cox, J.; Ostasiewicz, P.; Wisniewski, J. R.; Mann, M. Super-SILAC mix for quantitative proteomics of human tumor tissue Nat. Methods 2010, 7 (5) 383-385
18. Hanke, S.; Besir, H.; Oesterhelt, D.; Mann, M. Absolute SILAC for accurate quantitation of proteins in complex mixtures down to the attomole level J. Proteome Res. 2008, 7 (3) 1118-1130
19. Engvall, E.; Ruoslahti, E.; Miller, E. J. Affinity of fibronectin to collagens of different genetic types and to fibrinogen J. Exp. Med. 1978, 147 (6) 1584-1595
20. Barnes, M. J.; Constable, B. J.; Morton, L. F.; Kodicek, E. The influence of dietary calcium deficiency and parathyroidectomy on bone collagen structure Biochim. Biophys. Acta 1973, 328 (2) 373-382
21. Isemura, M.; Takahashi, K.; Ikenaka, T. Comparative study of carbohydrate-protein complexes. II. Determination of hydroxylysine and its glycosides in human skin and scar collagens by an improved method J. Biochem. 1976, 80 (4) 653-658
22. Ueno, T.; Tanaka, K.; Kaneko, K.; Taga, Y.; Sata, T.; Irie, S.; Hattori, S.; Ogawa-Goto, K. Enhancement of procollagen biosynthesis by p180 through augmented ribosome association on the endoplasmic reticulum in response to stimulated secretion J. Biol. Chem. 2010, 285 (39) 29941-29950
23. Adams, E.; Frank, L. Metabolism of proline and the hydroxyprolines Annu. Rev. Biochem. 1980, 49, 1005-1061
24. Bendall, S. C.; Hughes, C.; Stewart, M. H.; Doble, B.; Bhatia, M.; Lajoie, G. A. Prevention of amino acid conversion in SILAC experiments with embryonic stem cells Mol. Cell. Proteomics 2008, 7 (9) 1587-1597
25. Lossner, C.; Warnken, U.; Pscherer, A.; Schnolzer, M. Preventing arginine-to-proline conversion in a cell-line-independent manner during cell cultivation under stable isotope labeling by amino acids in cell culture (SILAC) conditions Anal. Biochem. 2011, 412 (1) 123-125
26. Eagle, H.; Washington, C. L.; Levy, M. End product control of amino acid synthesis by cultured human cells J. Biol. Chem. 1965, 240 (10) 3944-3950
27. Miller, E. J.; Gay, S. Collagen: an overview Methods Enzymol. 1982, 82 (Pt A) 3-32
28. Spiro, R. G. The structure of the disaccharide unit of the renal glomerular basement membrane J. Biol. Chem. 1967, 242 (20) 4813-4823
29. Mukhopadhyay, K.; Lefebvre, V.; Zhou, G.; Garofalo, S.; Kimura, J. H.; de Crombrugghe, B. Use of a new rat chondrosarcoma cell line to delineate a 119-base pair chondrocyte-specific enhancer element and to define active promoter segments in the mouse pro-alpha 1(II) collagen gene J. Biol. Chem. 1995, 270 (46) 27711-27719
30. Keene, D. R.; Sakai, L. Y.; Burgeson, R. E. Human bone contains type III collagen, type VI collagen, and fibrillin: type III collagen is present on specific fibers that may mediate attachment of tendons, ligaments, and periosteum to calcified bone cortex J. Histochem. Cytochem. 1991, 39 (1) 59-69
31. Eyre, D. R.; Weis, M.; Hudson, D. M.; Wu, J. J.; Kim, L. A novel 3-hydroxyproline (3Hyp)-rich motif marks the triple-helical C terminus of tendon type I collagen J. Biol. Chem. 2011, 286 (10) 7732-7736
32. Spiro, R. G. Characterization and quantitative determination of the hydroxylysine-linked carbohydrate units of several collagens J. Biol. Chem. 1969, 244 (4) 602-612
33. Stoltz, M.; Furthmayr, H.; Timpl, R. Increased lysine hydroxylation in rat bone and tendon collagen and localization of the additional residues Biochim. Biophys. Acta 1973, 310 (2) 461-468
34. Shapiro, F. D.; Eyre, D. R. Collagen polymorphism in extracellular matrix of human osteosarcoma J. Natl. Cancer Inst. 1982, 69 (5) 1009-1016
35. Lehmann, H. W.; Wolf, E.; Roser, K.; Bodo, M.; Delling, G.; Muller, P. K. Composition and posttranslational modification of individual collagen chains from osteosarcomas and osteofibrous dysplasias J. Cancer Res. Clin. Oncol. 1995, 121 (7) 413-418
36. Kern, P.; Sebert, B.; Robert, L. Increased type-III/type-I collagen ratios in diabetic human conjunctival biopsies Clin. Physiol. Biochem. 1986, 4 (2) 113-119
37. Abrass, C. K.; Peterson, C. V.; Raugi, G. J. Phenotypic expression of collagen types in mesangial matrix of diabetic and nondiabetic rats Diabetes 1988, 37 (12) 1695-1702
38. Bailey, A. J.; Wotton, S. F.; Sims, T. J.; Thompson, P. W. Biochemical changes in the collagen of human osteoporotic bone matrix Connect Tissue Res. 1993, 29 (2) 119-132
39. Taga, Y.; Kusubata, M.; Ogawa-Goto, K.; Hattori, S. Development of a novel method for analyzing collagen O-glycosylations by hydrazide chemistry Mol. Cell. Proteomics 2012, 11 (6) M111.010397
40. Taga, Y.; Kusubata, M.; Ogawa-Goto, K.; Hattori, S. Site-specific Quantitative Analysis of Overglycosylation of Collagen in Osteogenesis Imperfecta Using Hydrazide Chemistry and SILAC J. Proteome Res. 2013, 12 (5) 2225-2232
41. Marcilla, M.; Alpizar, A.; Paradela, A.; Albar, J. P. A systematic approach to assess amino acid conversions in SILAC experiments Talanta 2011, 84 (2) 430-436
42. Madsen, D. H.; Engelholm, L. H.; Ingvarsen, S.; Hillig, T.; Wagenaar-Miller, R. A.; Kjoller, L.; Gardsvoll, H.; Hoyer-Hansen, G.; Holmbeck, K.; Bugge, T. H.; Behrendt, N. Extracellular collagenases and the endocytic receptor, urokinase plasminogen activator receptor-associated protein/Endo180, cooperate in fibroblast-mediated collagen degradation J. Biol. Chem. 2007, 282 (37) 27037-27045