Comprehensive mass spectrometric mapping of the hydroxylated amino acid residues of the α1(V) collagen chain

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40598-40610

  Yang, Chenxi ^a,b   Park, Arick C ^b   Davis, Nicholas A ^b   Russell, Jason D ^a,b   Kim, Byoungjae ^b   Brand, David D ^c   Lawrence, Matthew J ^a,b   Ge, Ying ^a,b   Westphall, Michael S ^a   Coon, Joshua J ^a,b   Greenspan, Daniel S ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID ANALYSIS; AMINO ACID RESIDUES; BIOLOGICAL PROPERTIES; CHROMATOGRAPHIC SEPARATIONS; CONNECTIVE TISSUES; EHLERS-DANLOS SYNDROMES; FIBRILLAR COLLAGENS; GLYCOSYLATED; HIGH RESOLUTION MASS SPECTROMETRY; IMMUNE RESPONSE; LUNG TRANSPLANT; MASS SPECTROMETRIC MAPPING; NANOFLOWS; POST-TRANSLATIONAL MODIFICATIONS; PROCOLLAGEN; SENSITIVITY AND SPECIFICITY; TANDEM MASS SPECTROMETRY;

AMINO ACIDS; HYDROXYLATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MUSCULOSKELETAL SYSTEM; TISSUE;

COLLAGEN;

AMINO ACID; COLLAGEN TYPE 5; COLLAGEN TYPE 5 ALPHA1; GLYCINE; HYDROXYPROLINE; PROCOLLAGEN; PROCOLLAGEN TYPE 5 ALPHA1; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; CHROMATOGRAPHY; CONTROLLED STUDY; HUMAN; HUMAN CELL; NANOFLOW CHROMATOGRAPHY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RESIDUE ANALYSIS; SENSITIVITY AND SPECIFICITY; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CATTLE; COLLAGEN TYPE V; HUMANS; HYDROXYPROLINE; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING;

BOVINAE;

EID: 84870014480     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.406850     Document Type: Article

References (81)

1. Fichard, A., Kleman, J. P., and Ruggiero, F. (1995) Another look at collagen V and XI molecules. Matrix Biol 14, 515-531
2. Imamura, Y., Scott, I. C., and Greenspan, D. S. (2000) The pro-α3(V) collagen chain. Complete primary structure, expression domains in adult and developing tissues, and comparison to the structures and expression domains of the other types V and XI procollagen chains. J. Biol. Chem. 275, 8749-8759 (Pubitemid 30180228)
3. Morris, N. P., and Bächinger, H. P. (1987) Type XI collagen is a heterotrimer with the composition (1α, 2α, 3α) retaining non-triple-helical domains. J. Biol. Chem. 262, 11345-11350
4. Wu, J. J., Weis, M. A., Kim, L. S., Carter, B. G., and Eyre, D. R. (2009) Differences in chain usage and cross-linking specificities of cartilage type V/XI collagen isoforms with age and tissue. J. Biol. Chem. 284, 5539-5545
5. Birk, D. E., Fitch, J. M., Babiarz, J. P., and Linsenmayer, T. F. (1988) Collagen type I and type V are present in the same fibril in the avian corneal stroma. J. Cell Biol. 106, 999-1008 (Pubitemid 18090000)
6. Birk, D. E., Fitch, J. M., Babiarz, J. P., Doane, K. J., and Linsenmayer, T. F. (1990) Collagen fibrillogenesis in vitro. Interaction of types I and V collagen regulates fibril diameter. J. Cell Sci. 95, 649-657 (Pubitemid 20141358)
7. Toriello, H. V., Glover, T. W., Takahara, K., Byers, P. H., Miller, D. E., Higgins, J. V., and Greenspan, D. S. (1996) A translocation interrupts the COL5A1 gene in a patient with Ehlers-Danlos syndrome and hypomelanosis of Ito. Nat. Genet. 13, 361-365 (Pubitemid 26230506)
8. Richards, A. J., Martin, S., Nicholls, A. C., Harrison, J. B., Pope, F. M., and Burrows, N. P. (1998) A single base mutation in COL5A2 causes Ehlers-Danlos syndrome type II. J. Med. Genet. 35, 846-848 (Pubitemid 28431706)
9. Burlingham, W. J., Love, R. B., Jankowska-Gan, E., Haynes, L. D., Xu, Q., Bobadilla, J. L., Meyer, K. C., Hayney, M. S., Braun, R. K., Greenspan, D. S., Gopalakrishnan, B., Cai, J., Brand, D. D., Yoshida, S., Cummings, O. W., and Wilkes, D. S. (2007) IL-17-dependent cellular immunity to collagen type V predisposes to obliterative bronchiolitis in human lung transplants. J. Clin. Invest. 117, 3498-3506 (Pubitemid 350097005)
10. Sumpter, T. L., and Wilkes, D. S. (2004) Role of autoimmunity in organ allograft rejection. A focus on immunity to type V collagen in the pathogenesis of lung transplant rejection. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L1129-L1139 (Pubitemid 38656647)
11. Iwata, T., Philipovskiy, A., Fisher, A. J., Presson, R. G., Jr., Chiyo, M., Lee, J., Mickler, E., Smith, G. N., Petrache, I., Brand, D. B., Burlingham, W. J., Gopalakrishnan, B., Greenspan, D. S., Christie, J. D., and Wilkes, D. S. (2008) Anti-type V collagen humoral immunity in lung transplant primary graft dysfunction. J. Immunol. 181, 5738-5747
12. Bobadilla, J. L., Love, R. B., Jankowska-Gan, E., Xu, Q., Haynes, L. D., Braun, R. K., Hayney, M. S., Munoz del Rio, A., Meyer, K., Greenspan, D. S., Torrealba, J., Heidler, K. M., Cummings, O. W., Iwata, T., Brand, D., Presson, R., Burlingham, W. J., and Wilkes, D. S. (2008) Th-17, monokines, collagen type V, and primary graft dysfunction in lung transplantation. Am. J. Respir. Crit. Care Med. 177, 660-668 (Pubitemid 351442174)
13. Dart, M. L., Jankowska-Gan, E., Huang, G., Roenneburg, D. A., Keller, M. R., Torrealba, J. R., Rhoads, A., Kim, B., Bobadilla, J. L., Haynes, L. D., Wilkes, D. S., Burlingham, W. J., and Greenspan, D. S. (2010) Interleukin-17-dependent autoimmunity to collagen type V in atherosclerosis. Circ. Res. 107, 1106-1116
14. Henkel, W., and Dreisewerd, K. (2007) Cyanogen bromide peptides of the fibrillar collagens I, III, and V and their mass spectrometric characterization. Detection of linear peptides, peptide glycosylation, and cross-linking peptides involved in formation of homo- and heterotypic fibrils. J. Proteome Res. 6, 4269-4289 (Pubitemid 350158504)
15. Chung, E., Rhodes, K., and Miller, E. J. (1976) Isolation of three collagenous components of probable basement membrane origin from several tissues. Biochem. Biophys. Res. Commun. 71, 1167-1174
16. Shoulders, M. D., and Raines, R. T. (2009) Collagen structure and stability. Annu. Rev. Biochem. 78, 929-958
17. Kivirikko, K. I. (1993) Collagens and their abnormalities in a wide spectrum of diseases. Ann. Med. 25, 113-126
18. Sipilä, L., Ruotsalainen, H., Sormunen, R., Baker, N. L., Lamandé, S. R., Vapola, M., Wang, C., Sado, Y., Aszodi, A., and Myllylä, R. (2007) Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines. J. Biol. Chem. 282, 33381-33388
19. Mizuno, K., Peyton, D. H., Hayashi, T., Engel, J., and Bächinger, H. P. (2008) Effect of the -Gly-3(S)-hydroxyprolyl-4(R)-hydroxyprolyl-tripeptide unit on the stability of collagen model peptides. FEBS J. 275, 5830-5840
20. Jenkins, C. L., Bretscher, L. E., Guzei, I. A., and Raines, R. T. (2003) Effect of 3-hydroxyproline residues on collagen stability. J Am Chem Soc 125, 6422-6427 (Pubitemid 36605410)
21. Morello, R., Bertin, T. K., Chen, Y., Hicks, J., Tonachini, L., Monticone, M., Castagnola, P., Rauch, F., Glorieux, F. H., Vranka, J., Bächinger, H. P., Pace, J. M., Schwarze, U., Byers, P. H., Weis, M., Fernandes, R. J., Eyre, D. R., Yao, Z., Boyce, B. F., and Lee, B. (2006) CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127, 291-304 (Pubitemid 44604299)
22. Arbogast, B. W., Gunson, D. E., and Kefalides, N. A. (1976) The role of hydroxylation of proline in the antigenicity of basement membrane collagen. J. Immunol. 117, 2181-2184 (Pubitemid 8009013)
23. Brand, D. D., Myers, L. K., Terato, K., Whittington, K. B., Stuart, J. M., Kang, A. H., and Rosloniec, E. F. (1994) Characterization of the T cell determinants in the induction of autoimmune arthritis by bovine α 1(II)-CB11 in H-2q mice. J. Immunol. 152, 3088-3097
24. Corthay, A., Bäcklund, J., Broddefalk, J., Michaëlsson, E., Goldschmidt, T. J., Kihlberg, J., and Holmdahl, R. (1998) Epitope glycosylation plays a critical role for T cell recognition of type II collagen in collagen-induced arthritis. Eur. J. Immunol. 28, 2580-2590 (Pubitemid 28362732)
25. Myers, L. K., Miyahara, H., Terato, K., Seyer, J. M., Stuart, J. M., and Kang, A. H. (1995) Collagen-induced arthritis in B10.RIII mice (H-2r). Identification of an arthritogenic T-cell determinant. Immunology 84, 509-513
26. Myers, L. K., Myllyharju, J., Nokelainen, M., Brand, D. D., Cremer, M. A., Stuart, J. M., Bodo, M., Kivirikko, K. I., and Kang, A. H. (2004) Relevance of posttranslational modifications for the arthritogenicity of type II collagen. J. Immunol. 172, 2970-2975 (Pubitemid 38263684)
27. Van den Steen, P. E., Proost, P., Brand, D. D., Kang, A. H., Van Damme, J., and Opdenakker, G. (2004) Generation of glycosylated remnant epitopes from human collagen type II by gelatinase B. Biochemistry 43, 10809-10816 (Pubitemid 39096723)
28. Van den Steen, P. E., Proost, P., Grillet, B., Brand, D. D., Kang, A. H., Van Damme, J., and Opdenakker, G. (2002) Cleavage of denatured natural collagen type II by neutrophil gelatinase B reveals enzyme specificity, post-translational modifications in the substrate, and the formation of remnant epitopes in rheumatoid arthritis. FASEB J. 16, 379-389 (Pubitemid 34195299)
29. Michaëlsson, E., Malmström, V., Reis, S., Engström, A., Burkhardt, H., and Holmdahl, R. (1994) T cell recognition of carbohydrates on type II collagen. J. Exp. Med. 180, 745-749
30. Eyre, D. R., Weis, M., Hudson, D. M., Wu, J. J., and Kim, L. (2011) A novel 3-hydroxyproline (3Hyp)-rich motif marks the triple-helical C terminus of tendon type I collagen. J. Biol. Chem. 286, 7732-7736
31. Fernandes, R. J., Farnand, A. W., Traeger, G. R., Weis, M. A., and Eyre, D. R. (2011) A role for prolyl 3-hydroxylase 2 in post-translational modification of fibril-forming collagens. J. Biol. Chem. 286, 30662-30669
32. Weis, M. A., Hudson, D. M., Kim, L., Scott, M., Wu, J. J., and Eyre, D. R. (2010) 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, 2580-2590
33. Vaisar, T., and Urban, J. (1996) Probing the proline effect in CID of protonated peptides. J Mass Spectrom 31, 1185-1187 (Pubitemid 26360255)
34. Huang, Y., Triscari, J. M., Pasa-Tolic, L., Anderson, G. A., Lipton, M. S., Smith, R. D., and Wysocki, V. H. (2004) Dissociation behavior of doubly-charged tryptic peptides: correlation of gas-phase cleavage abundance with ramachandran plots. J. Am. Chem. Soc. 126, 3034-3035 (Pubitemid 38380694)
35. Loo, J. A., Edmonds, C. G., and Smith, R. D. (1993) Tandem mass spectrometry of very large molecules. 2. Dissociation of multiply charged proline-containing proteins from electrospray ionization. Anal. Chem. 65, 425-438 (Pubitemid 23087026)
36. Tang, X. J., Thibault, P., and Boyd, R. K. (1993) Fragmentation reactions of multiply protonated peptides and implications for sequencing by tandem mass spectrometry with low-energy collision-induced dissociation. Anal. Chem. 65, 2824-2834
37. Breci, L. A., Tabb, D. L., Yates, J. R., 3rd, and Wysocki, V. H. (2003) Cleavage N-terminal to proline. Analysis of a database of peptide tandem mass spectra. Anal. Chem. 75, 1963-1971 (Pubitemid 36542332)
38. McAlister, G. C., Phanstiel, D., Wenger, C. D., Lee, M. V., and Coon, J. J. (2010) Analysis of tandem mass spectra by FTMS for improved large-scale proteomics with superior protein quantification. Anal. Chem. 82, 316-322
39. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., and Hunt, D. F. (2004) Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 101, 9528-9533 (Pubitemid 38869270)
40. 2-terminal propeptide, and a furin-like proprotein convertase processes the COOH-terminal propeptide of pro-α1(V) collagen. J. Biol. Chem. 273, 27511-27517
41. Mares, D. C., Heidler, K. M., Smith, G. N., Cummings, O. W., Harris, E. R., Foresman, B., and Wilkes, D. S. (2000) Type V collagen modulates alloantigen-induced pathology and immunology in the lung. Am. J. Respir. Cell Mol. Biol. 23, 62-70 (Pubitemid 30597096)
42. Seyer, J. M., and Kang, A. H. (1989) Covalent structure of collagen, Amino acid sequence of three cyanogen bromide-derived peptides from human α1(V) collagen chain. Arch. Biochem. Biophys. 271, 120-129 (Pubitemid 19119824)
43. Shah, R., Smith, P., Purdie, C., Quinlan, P., Baker, L., Aman, P., Thompson, A. M., and Crook, T. (2009) The prolyl 3-hydroxylases P3H2 and P3H3 are novel targets for epigenetic silencing in breast cancer. Br. J. Cancer 100, 1687-1696
44. Greenspan, D. S., Cheng, W., and Hoffman, G. G. (1991) The pro-α 1(V) collagen chain. Complete primary structure, distribution of expression, and comparison with the pro-α 1(XI) collagen chain. J. Biol. Chem. 266, 24727-24733 (Pubitemid 21909002)
45. Swaney, D. L., Wenger, C. D., and Coon, J. J. (2010) Value of using multiple proteases for large-scale mass spectrometry-based proteomics. J. Proteome Res. 9, 1323-1329
46. Ficarro, S. B., Zhang, Y., Lu, Y., Moghimi, A. R., Askenazi, M., Hyatt, E., Smith, E. D., Boyer, L., Schlaeger, T. M., Luckey, C. J., and Marto, J. A. (2009) Improved electrospray ionization efficiency compensates for diminished chromatographic resolution and enables proteomics analysis of tyrosine signaling in embryonic stem cells. Anal. Chem. 81, 3440-3447
47. Olsen, J. V., Schwartz, J. C., Griep-Raming, J., Nielsen, M. L., Damoc, E., Denisov, E., Lange, O., Remes, P., Taylor, D., Splendore, M., Wouters, E. R., Senko, M., Makarov, A., Mann, M., and Horning, S. (2009) A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol. Cell. Proteomics 8, 2759-2769
48. Good, D. M., Wirtala, M., McAlister, G. C., and Coon, J. J. (2007) Performance characteristics of electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 6, 1942-1951 (Pubitemid 350213868)
49. Wenger, C. D., Phanstiel, D. H., Lee, M. V., Bailey, D. J., and Coon, J. J. (2011) COMPASS. A suite of pre- and post-search proteomics software tools for OMSSA. Proteomics 11, 1064-1074
50. Good, D. M., Wenger, C. D., McAlister, G. C., Bai, D. L., Hunt, D. F., and Coon, J. J. (2009) Post-acquisition ETD spectral processing for increased peptide identifications. J. Am. Soc. Mass Spectrom. 20, 1435-1440
51. Good, D. M., Wenger, C. D., and Coon, J. J. (2010) The effect of interfering ions on search algorithm performance for electron-transfer dissociation data. Proteomics 10, 164-167
52. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., Yang, X., Shi, W., and Bryant, S. H. (2004) Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964 (Pubitemid 39425651)
53. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214 (Pubitemid 46358868)
54. Gorres, K. L., and Raines, R. T. (2010) Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 45, 106-124
55. Risteli, J., Tryggvason, K., and Kivirikko, K. I. (1977) Prolyl 3-hydroxylase. Partial characterization of the enzyme from rat kidney cortex. Eur. J. Biochem. 73, 485-492 (Pubitemid 8052917)
56. Tiainen, P., Pasanen, A., Sormunen, R., and Myllyharju, J. (2008) Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J. Biol. Chem. 283, 19432-19439
57. Unsöld, C., Pappano, W. N., Imamura, Y., Steiglitz, B. M., and Greenspan, D. S. (2002) Biosynthetic processing of the pro-α 1(V)2pro-α2(V) collagen heterotrimer by bone morphogenetic protein-1 and furin-like proprotein convertases. J. Biol. Chem. 277, 5596-5602 (Pubitemid 34968613)
58. Gopalakrishnan, B., Wang, W. M., and Greenspan, D. S. (2004) Biosynthetic processing of the Pro-α1(V)Pro-α2(V)Pro-α3(V) procollagen heterotrimer. J. Biol. Chem. 279, 30904-30912 (Pubitemid 38938027)
59. Delacoux, F., Fichard, A., Geourjon, C., Garrone, R., and Ruggiero, F. (1998) Molecular features of the collagen V heparin binding site. J. Biol. Chem. 273, 15069-15076 (Pubitemid 28272802)
60. Chanut-Delalande, H., Fichard, A., Bernocco, S., Garrone, R., Hulmes, D. J., and Ruggiero, F. (2001) Control of heterotypic fibril formation by collagen V is determined by chain stoichiometry. J. Biol. Chem. 276, 24352-24359
61. Fichard, A., Tillet, E., Delacoux, F., Garrone, R., and Ruggiero, F. (1997) Human recombinant α1(V) collagen chain. Homotrimeric assembly and subsequent processing. J. Biol. Chem. 272, 30083-30087 (Pubitemid 27512204)
62. Kessler, E., Fichard, A., Chanut-Delalande, H., Brusel, M., and Ruggiero, F. (2001) Bone morphogenetic protein-1 (BMP-1) mediates C-terminal processing of procollagen V homotrimer. J. Biol. Chem. 276, 27051-27057
63. Pyott, S. M., Schwarze, U., Christiansen, H. E., Pepin, M. G., Leistritz, D. F., Dineen, R., Harris, C., Burton, B. K., Angle, B., Kim, K., Sussman, M. D., Weis, M., Eyre, D. R., Russell, D. W., McCarthy, K. J., Steiner, R. D., and Byers, P. H. (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
64. Olsen, J. V., Ong, S. E., and Mann, M. (2004) Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 3, 608-614 (Pubitemid 38878520)
65. Rodriguez, J., Gupta, N., Smith, R. D., and Pevzner, P. A. (2008) Does trypsin cut before proline? J. Proteome Res. 7, 300-305 (Pubitemid 351171143)
66. Licklider, L. J., Thoreen, C. C., Peng, J., and Gygi, S. P. (2002) Automation of nanoscale microcapillary liquid chromatography-tandem mass spectrometry with a vented column. Anal. Chem. 74, 3076-3083 (Pubitemid 34755220)
67. Wiesner, J., Premsler, T., and Sickmann, A. (2008) Application of electron transfer dissociation (ETD) for the analysis of posttranslational modifications. Proteomics 8, 4466-4483
68. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., and Kuster, B. (2011) Confident phosphorylation site localization using the Mascot Delta Score. Mol. Cell. Proteomics M110.003830-1-M110.003830-12
69. Rhodes, R. K., and Miller, E. J. (1979) The isolation and characterization of the cyanogen bromide peptides from the B chain of human collagen. J. Biol. Chem. 254, 12084-12087 (Pubitemid 10143681)
70. Abedin, M. Z., Ayad, S., and Weiss, J. B. (1982) Isolation and native characterization of cysteine-rich collagens from bovine placental tissues and uterus and their relationship to types IV and V collagens. Biosci. Rep. 2, 493-502
71. Butler, W. T., Piez, K. A., and Bornstein, P. (1967) Isolation and characterization of the cyanogen bromide peptides from the α-1 chain of rat skin collagen. Biochemistry 6, 3771-3780
72. Click, E. M., and Bornstein, P. (1970) Isolation and characterization of the cyanogen bromide peptides from the α1 and α2 chains of human skin collagen. Biochemistry 9, 4699-4706
73. Miller, E. J., and Lunde, L. G. (1973) Isolation and characterization of the cyanogen bromide peptides from the α1(II) chain of bovine and human cartilage collagen. Biochemistry 12, 3153-3159
74. Seyer, J. M., and Kang, A. H. (1981) Covalent structure of collagen. Amino acid sequence of α 1(III)-CB9 from type III collagen of human liver. Biochemistry 20, 2621-2627 (Pubitemid 11089789)
75. Kefalides, N. A. (1975) Basement membranes. Structural and biosynthetic considerations. J. Invest. Dermatol. 65, 85-92
76. Gryder, R. M., Lamon, M., and Adams, E. (1975) Sequence position of 3-hydroxyproline in basement membrane collagen. Isolation of glycyl-3-hydroxyprolyl-4-hydroxyproline from swine kidney. J. Biol. Chem. 250, 2470-2474
77. Roulet, M., Välkkilä, M., Chanut-Delalande, H., Hämäläinen, E. R., Kessler, E., Ala-Kokko, L., Männikkö, M., Bonod-Bidaud, C., and Ruggiero, F. (2010) The collagen V homotrimer [α1(V)](3) production is unexpectedly favored over the heterotrimer [α1(V)](2)α2(V) in recombinant expression systems. J. Biomed. Biotechnol. 2010, 376927
78. Zhang, Y., Liu, T., Wang, Q., Chen, L., Lei, J., Luo, J., Ma, G., and Su, Z. (2009) Mass spectrometric detection of marker peptides in tryptic digests of gelatin. A new method to differentiate between bovine and porcine gelatin. Food Hydrocoll. 23, 2001-2007
79. Inouye, K., Kobayashi, Y., Kyogoku, Y., Kishida, Y., Sakakibara, S., and Prockop, D. J. (1982) Synthesis and physical properties of (hydroxyproline- proline-glycine)10. Hydroxyproline in the X-position decreases the melting temperature of the collagen triple helix. Arch. Biochem. Biophys. 219, 198-203
80. Bann, J. G., and Bächinger, H. P. (2000) Glycosylation/ hydroxylation-induced stabilization of the collagen triple helix. 4-Trans-hydroxyproline in the Xaa position can stabilize the triple helix. J. Biol. Chem. 275, 24466-24469 (Pubitemid 30626538)
81. Schumacher, M. A., Mizuno, K., and Bächinger, H. P. (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, 27566-27574 (Pubitemid 44401782)