Osteogenesis imperfecta missense mutations in collagen: Structural consequences of a glycine to alanine replacement at a highly charged site

Biochemistry

Volumn 50, Issue 50, 2011, Pages 10771-10780

  Xiao, Jianxi ^a   Cheng, Haiming ^b,d   Silva, Teresita ^b   Baum, Jean ^a   Brodsky, Barbara ^b,c  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c Tufts University   (United States)

^d SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN BINDING; COLLAGEN TRIPLE HELIX; LOCAL SEQUENCES; MUTATION SITES; OSTEOGENESIS IMPERFECTA; PATHOLOGICAL CONDITIONS; STRUCTURAL DEFECT; STRUCTURAL PERTURBATION;

AMINO ACIDS; BINDING SITES; DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; HYDROGEN BONDS; PATHOLOGY;

COLLAGEN;

ALANINE; COLLAGEN; GLYCINE; HYDROGEN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CIRCULAR DICHROISM; COLLAGEN DISEASE; DIFFERENTIAL SCANNING CALORIMETRY; HYDROGEN BOND; MISSENSE MUTATION; MOLECULAR STABILITY; MUTATION RATE; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOGENESIS IMPERFECTA; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TRIPLE HELIX;

ALANINE; AMINO ACID SUBSTITUTION; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; COLLAGEN TYPE I; GLYCINE; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; MUTANT PROTEINS; MUTATION, MISSENSE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OSTEOGENESIS IMPERFECTA; PEPTIDE FRAGMENTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; TRANSITION TEMPERATURE;

EID: 83455221652     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201476a     Document Type: Article

References (45)

1. Bella, J., Eaton, M., Brodsky, B., and Berman, H. M. (1994) Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution Science 266, 75-81
2. Kielty, C. M. and Grant, M. E. (2002) The collagen family: Strucutre, assembly, and organization in the extracellular matrix. In Connective tissue and its heritable disorders, molecular, genetic and medical aspects (Royes, P. M. and Steinmann, B. U., Eds.) pp 159-222, Wiley-Liss, New York.
3. Ramachandran, G. N. (1967) Structure of Collagen at the Molecular Level. In Treatise on Collagen (Ramachandran, G. N., Ed.) pp 103-184, Academic Press, New York.
4. Rich, A. and Crick, F. H. (1961) The molecular structure of collagen J. Mol. Biol. 3, 483-506
5. Byers, P. H. and Cole, W. G. (2002) Osteogenesis Imperfecta. In Connective tissue and its hereditable disorders (Royce, P. M. and Steinmann, B., Eds.) pp 385-430, Wiley-Liss, New York.
6. Dalgleish, R. (1997) The human type I collagen mutation database Nucleic Acids Res. 25, 181-187 (Pubitemid 27307006)
7. Dalgleish, R. (1998) The Human Collagen Mutation Database 1998 Nucleic Acids Res. 26, 253-255 (Pubitemid 28295282)
8. Marini, J. C., Forlino, A., Cabral, W. A., Barnes, A. M., San Antonio, J. D., Milgrom, S., Hyland, J. C., Korkko, J., Prockop, D. J., and De Paepe, A. 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
9. Bodian, D. L., Madhan, B., Brodsky, B., and Klein, T. E. (2008) Predicting the clinical lethality of osteogenesis imperfecta from collagen glycine mutations Biochemistry 47, 5424-5432 (Pubitemid 351656986)
10. Xiao, J., Madhan, B., Li, Y., Brodsky, B., and Baum, J. (2011) Osteogenesis imperfecta model peptides: Incorporation of residues replacing Gly within a triple helix achieved by renucleation and local flexibility Biophys. J. 101, 449-458
11. Beck, K., Chan, V. C., Shenoy, N., Kirkpatrick, A., Ramshaw, J. A., and Brodsky, B. (2000) Destabilization of osteogenesis imperfecta collagen-like model peptides correlates with the identity of the residue replacing glycine Proc. Natl. Acad. Sci. U.S.A. 97, 4273-4278 (Pubitemid 30226123)
12. Bryan, M. A., Cheng, H., and Brodsky, B. (2011) Sequence environment of mutation affects stability and folding in collagen model peptides of osteogenesis imperfecta Biopolymers 96, 4-13
13. Makareeva, E., Mertz, E. L., Kuznetsova, N. V., Sutter, M. B., Deridder, A. M., Cabral, W. A., Barnes, A. M., Mcbride, D. J., Marini, J. C., and Leikin, S. (2008) Structural heterogeneity of type I collagen triple helix and its role in osteogenesis imperfecta J. Biol. Chem. 283, 4787-4798
14. Persikov, A. V., Pillitteri, R. J., Amin, P., Schwarze, U., Byers, P. H., and Brodsky, B. (2004) Stability related bias in residues replacing glycines within the collagen triple helix (Gly-Xaa-Yaa) in inherited connective tissue disorders Hum. Mutat. 24, 330-337 (Pubitemid 39336639)
15. Dalgleish, R. Osteogenesis imperfecta and Ehlers-Danlos syndrome variant databases. http://www.le.ac.uk/genetics/collagen/, Leiden University Medical Center, Leiden, The Netherlands.
16. Long, C. G., Braswell, E., Zhu, D., Apigo, J., Baum, J., and Brodsky, B. (1993) Characterization of collagen-like peptides containing interruptions in the repeating Gly-X-Y sequence Biochemistry 32, 11688-11695 (Pubitemid 23341448)
17. Bella, J., Brodsky, B., and Berman, H. M. (1995) Hydration structure of a collagen peptide Structure 3, 893-906
18. Li, Y., Brodsky, B., and Baum, J. (2009) NMR conformational and dynamic consequences of a Gly to Ser substitution in an osteogenesis imperfecta collagen model peptide J. Biol. Chem. 284, 20660-20667
19. Persikov, A. V., Ramshaw, J. A., Kirkpatrick, A., and Brodsky, B. (2005) Electrostatic interactions involving lysine make major contributions to collagen triple-helix stability Biochemistry 44, 1414-1422 (Pubitemid 40204385)
20. Persikov, A. V., Xu, Y., and Brodsky, B. (2004) Equilibrium thermal transitions of collagen model peptides Protein Sci. 13, 893-902 (Pubitemid 38429213)
21. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10665
22. 15N-enriched proteins J. Am. Chem. Soc. 115, 7772-7777
23. n repeat J. Biol. Chem. 282, 22699-22706 (Pubitemid 47267324)
24. 15N NMR relaxation and hydrogen-exchange measurements Biochemistry 32, 13299-13309 (Pubitemid 24005940)
25. 15N NMR relaxation Biochemistry 33, 5984-6003 (Pubitemid 24184605)
26. Palmer, A. G., III (1993) Dynamic properties of proteins from NMR spectroscopy Curr. Opin. Biotechnol. 4, 385-391
27. 15N relaxation data for an anisotropic collagen peptide J. Am. Chem. Soc. 131, 18194-18195
28. Glasoe, P. K. and Long, F. A. (1960) Use of glass electrodes to measure acidities in deuterium oxide J. Phys. Chem. 64, 188-189
29. Xiao, J., Addabbo, R. M., Lauer, J. L., Fields, G. B., and Baum, J. (2010) Local conformation and dynamics of isoleucine in the collagenase cleavage site provides recognition signal for matrix metalloproteinases J. Biol. Chem. 285, 34181-34190
30. Bai, Y., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen exchange Proteins 17, 75-86 (Pubitemid 23261059)
31. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
32. Goddard, T. D. and Kneller, D. G. (2008) Sparky: NMR Assignment and Integration Software. University of California, San Francisco.
33. Persikov, A. V., Ramshaw, J. A., and Brodsky, B. (2005) Prediction of collagen stability from amino acid sequence J. Biol. Chem. 280, 19343-19349 (Pubitemid 41379641)
34. Buevich, A. V., Dai, Q. H., Liu, X., Brodsky, B., and Baum, J. (2000) Site-specific NMR monitoring of cis-trans isomerization in the folding of the proline-rich collagen triple helix Biochemistry 39, 4299-4308 (Pubitemid 30212645)
35. Mann, K., Gaill, F., and Timpl, R. (1992) Amino-acid sequence and cell-adhesion activity of a fibril-forming collagen from the tube worm Riftia pachyptila living at deep sea hydrothermal vents Eur. J. Biochem. 210, 839-847 (Pubitemid 23015784)
36. Sicot, F. X., Mesnage, M., Masselot, M., Exposito, J. Y., Garrone, R., Deutsch, J., and Gaill, F. (2000) Molecular adaptation to an extreme environment: Origin of the thermal stability of the pompeii worm collagen J. Mol. Biol. 302, 811-820
37. Yoneda, C., Hirayama, Y., Nakaya, M., Matsubara, Y., Irie, S., Hatae, K., and Watabe, S. (1999) The occurrence of two types of collagen pro-α-chain in the abalone Haliotis discus muscle Eur. J. Biochem. 261, 714-721 (Pubitemid 29226069)
38. Xu, K., Nowak, I., Kirchner, M., and Xu, Y. (2008) Recombinant collagen studies link the severe conformational changes induced by osteogenesis imperfecta mutations to the disruption of a set of interchain salt bridges J. Biol. Chem. 283, 34337-34344
39. Sweeney, S. M., Orgel, J. P., Fertala, A., Mcauliffe, J. D., Turner, K. R., Di Lullo, G. A., Chen, S., Antipova, O., Perumal, S., and Ala-Kokko, L. 2008, Candidate cell and matrix interaction domains on the collagen fibril, the predominant protein of vertebrates J. Biol. Chem. 283, 21187-21197
40. Farndale, R. W., Lisman, T., Bihan, D., Hamaia, S., Smerling, C. S., Pugh, N., Konitsiotis, A., Leitinger, B., De Groot, P. G., and Jarvis, G. E. 2008, Cell-collagen interactions: The use of peptide Toolkits to investigate collagen-receptor interactions Biochem. Soc. Trans. 36, 241-250 (Pubitemid 351570596)
41. Konitsiotis, A. D., Raynal, N., Bihan, D., Hohenester, E., Farndale, R. W., and Leitinger, B. (2008) Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen J. Biol. Chem. 283, 6861-6868
42. Di Lullo, G. A., Sweeney, S. M., Korkko, J., Ala-Kokko, L., and San Antonio, J. D. (2002) Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen J. Biol. Chem. 277, 4223-4231 (Pubitemid 34968685)
43. Giudici, C., Raynal, N., Wiedemann, H., Cabral, W. A., Marini, J. C., Timpl, R., Bachinger, H. P., Farndale, R. W., Sasaki, T., and Tenni, R. (2008) Mapping of SPARC/BM-40/osteonectin-binding sites on fibrillar collagens J. Biol. Chem. 283, 19551-19560
44. Raynal, N., Hamaia, S. W., Siljander, P. R., Maddox, B., Peachey, A. R., Fernandez, R., Foley, L. J., Slatter, D. A., Jarvis, G. E., and Farndale, R. W. (2006) Use of synthetic peptides to locate novel integrin α2β1- binding motifs in human collagen III J. Biol. Chem. 281, 3821-3831 (Pubitemid 43847806)
45. Lebbink, R. J., Raynal, N., De Ruiter, T., Bihan, D. G., Farndale, R. W., and Meyaard, L. (2009) Identification of multiple potent binding sites for human leukocyte associated Ig-like receptor LAIR on collagens II and III Matrix Biol. 28, 202-210