Dynamic footprint of sequestration in the molecular fluctuations of osteopontin

Journal of the Royal Society Interface

Volumn 12, Issue 110, 2015, Pages

  Lenton, S ^a,b   Seydel, T ^a   Nylander, T ^c   Holt, C ^d   Hartlein M ^a   Teixeira, S ^a,b   Zaccai, G ^a,e  

^a INSTITUT LAUE LANGEVIN   (France)

^b KEELE UNIVERSITY   (United Kingdom)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Biomineralization; Calcium phosphate nanoclusters; Elastic incoherent neutron scattering; Intrinsically disordered proteins; Osteopontin; Small angle scattering

Indexed keywords

BIOMINERALIZATION; CALCIUM; CALCIUM PHOSPHATE; ENZYME ACTIVITY; NANOCLUSTERS; NEUTRON SCATTERING; PEPTIDES; PROTEINS;

CONFORMATIONAL FLEXIBILITY; ELASTIC INCOHERENT NEUTRON SCATTERING; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR FLUCTUATION; NEUTRON SPECTROSCOPY; OSTEOPONTIN; SMALL ANGLE SCATTERING; SMALL ANGLE X-RAYS;

INCOHERENT SCATTERING;

GLOBULAR PROTEIN; OSTEOPONTIN; PHOSPHOPEPTIDE; CALCIUM PHOSPHATE; MILK PROTEIN; PEPTIDE;

ANIMAL EXPERIMENT; ARTICLE; BIOMINERALIZATION; BOVINE; CIRCULAR DICHROISM; CONTROLLED STUDY; ELASTICITY; MILK; MOLECULAR DYNAMICS; NEUTRON SCATTERING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPECTROSCOPY; X RAY CRYSTALLOGRAPHY; ANIMAL; CHEMISTRY; PROTEIN UNFOLDING;

ANIMALS; CALCIUM PHOSPHATES; CATTLE; MILK PROTEINS; MOLECULAR DYNAMICS SIMULATION; OSTEOPONTIN; PEPTIDES; PROTEIN UNFOLDING;

EID: 84942046000     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.0506     Document Type: Article

References (77)

1. Habchi J, Tompa P, Longhi S, Uversky VN. 2014 Introducing protein intrinsic disorder. Chem. Rev. 114, 6561-6588. (doi:10.1021/cr400514h).
2. Oldfield CJ, Dunker AK. 2014 Intrinsically disordered proteins and intrinsically disordered protein regions. Annu. Rev. Biochem. 83, 553-584. (doi:10.1146/annurev-biochem-072711-164947).
3. Smith JC. 2009 Protein dynamics: comparison of simulations with inelastic neutron scattering experiments. Q. Rev. Biophys. 24, 227-291. (doi:10.1017/S0033583500003723).
4. Liu Z, Huang Y. 2014 Advantages of proteins being disordered. Protein Sci. 23, 539-550. (doi:10.1002/pro.2443).
5. Holt C, Sawyer L. 1988 Primary and predicted secondary structures of the caseins in relation to their biological functions. Protein Eng. Des. Select. 2, 251-259. (doi:10.1093/protein/2.4.251).
6. Thorn DC, Ecroyd H, Carver JA, Holt C. 2014 Casein structures in the context of unfolded proteins. Int. Dairy J. 46, 2-11. (doi:10.1016/j.idairyj.2014.07.008).
7. Lenton S, Nylander T, Teixeira SCM, Holt C. 2015 A review of the biology of calcium phosphate sequestration with special reference to milk. Dairy Sci. Technol. 95, 3-14. (doi:10.1007/s13594-014-0177-2).
8. Holt C. 2013 Unfolded phosphopolypeptides enable soft and hard tissues to coexist in the same organism with relative ease. Curr. Opin. Struct. Biol. 23, 420-425. (doi:10.1016/j.sbi.2013.02.010).
9. Kalmar L, Homola D, Varga G, Tompa P. 2012 Structural disorder in proteins brings order to crystal growth in biomineralization. Bone 51, 528-534. (doi:10.1016/j.bone.2012.05.009).
10. Fisher LW, Torchia DA, Fohr B, Young MF, Fedarko NS. 2001 Flexible structures of SIBLING proteins, bone sialoprotein, and osteopontin. Biochem. Biophy. Res. Comm. 280, 460-465. (doi:10.1006/bbrc.2000.4146).
11. Kurzbach D, Schwarz TC, Platzer G, Höfler S, Hinderberger D, Konrat R. 2014 Compensatory adaptations of structural dynamics in an intrinsically disordered protein complex. Angew. Chemie 53, 3840-3843. (doi:10.1002/anie.201308389).
12. Christensen B, Sørensen E. 2014 Osteopontin is highly susceptible to cleavage in bovine milk and the proteolytic fragments bind the aVb3-integrin receptor. J. Dairy Sci. 97, 136-146. (doi:10.3168/jds.2013-7223).
13. Holt C, Sørensen ES, Clegg RA. 2009 Role of calcium phosphate nanoclusters in the control of calcification. FEBS J. 276, 2308-2323. (doi:10.1111/j.1742-4658.2009.06958.x).
14. Holt C, Lenton S, Nylander T, Sørensen ES, Teixeira SCM. 2014 Mineralisation of soft and hard tissues and the stability of biofluids. J. Struct. Biol. 185, 383-396. (doi:10.1016/j.jsb.2013.11.009).
15. Clegg RA, Holt C. 2009 An E. coli over-expression system for multiply-phosphorylated proteins and its use in a study of calcium phosphate sequestration by novel recombinant phosphopeptides. Protein Express. Purif. 67, 23-34. (doi:10.1016/j.pep.2009.04.004).
16. Holt C, Wahlgren N, Drakenberg T. 1996 Ability of a b-casein phosphopeptide to modulate the precipitation of calcium phosphate by forming amorphous dicalcium phosphate nanoclusters. Biochem. J. 314, 1035-1039. (doi:10.1042/bj3141035).
17. Holt C, Timmins P, Errington N, Leaver J. 1998 A core-shell model of calcium phosphate nanoclusters stabilized by b-casein phosphopeptides, derived from sedimentation equilibrium and small-angle X-ray and neutron-scattering measurements. Eur. J. Biochem. 252, 73-78. (doi:10.1046/j.1432-1327.1998.2520073.x).
18. Holt C, de-Kruif C, Tuinier R, Timmins P. 2003 Substructure of bovine casein micelles by smallangle X-ray and neutron scattering. Colloids Surf. A 213, 275-284. (doi:10.1016/S0927-7757(02)00520-4).
19. Little EM, Holt C. 2004 An equilibrium thermodynamic model of the sequestration of calcium phosphate by casein phosphopeptides. Eur. Biophys. J. 33, 435-447. (doi:10.1007/s00249-003-0376-x).
20. Holt C. 2004 An equilibrium thermodynamic model of the sequestration of calcium phosphate by casein micelles and its application to the calculation of the partition of salts in milk. Eur. Biophys. J. 33, 421-434. (doi:10.1007/s00249-003-0377-9).
21. Konrat R. 2014 NMR contributions to structural dynamics studies of intrinsically disordered proteins. J. Magnetic Resonance 241, 74-85. (doi:10.1016/j.jmr.2013.11.011).
22. Zaccai G. 2011 Neutron scattering perspectives for protein dynamics. J. Non-Crystalline Solids 357, 615-621. (doi:10.1016/j.jnoncrysol.2010.06.060).
23. Platzer G et al. 2011 The metastasis-associated extracellular matrix protein osteopontin forms transient structure in ligand interaction sites. Biochemistry 50, 6113-6124. (doi:10.1021/bi200291e).
24. Bernado P, Mylonas E, Petoukhov MV, Blackledge M, Svergun DI. 2007 Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc. 129, 5656-5664. (doi:10.1021/ja069124n).
25. Ozenne V, Bauer F, Salmon L, Huang J-R, Jensen MR, Segard S, Bernado P, Charavay C, Blackledge M. 2012 Flexible-meccano: A tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 28, 1463-1470. (doi:10.1093/bioinformatics/bts172).
26. Dunker AK et al. 2013 What's in a name? Why these proteins are intrinsically disordered. Intrinsically Disordered Proteins 1, e24157. (doi:10.4161/idp.24157).
27. Fisher CK, Stultz CM. 2011 Constructing ensembles for intrinsically disordered proteins. Curr. Opin. Struct. Biol. 21, 426-431. (doi:10.1016/j.sbi.2011.04.001).
28. Dedmon MM, Patel CN, Young GB, Pielak GJ. 2002 FlgM gains structure in living cells. Proc. Natl Acad. Sci. USA 99, 12681-12684. (doi:10.1073/pnas.202331299).
29. Ellis RJ. 2001 Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26, 597-604. (doi:10.1016/S0968-0004(01)01938-7).
30. Soranno A, Koenig I, Borgia MB, Hofmann H, Zosel F, Nettels D, Schuler B. 2014 Single-molecule spectroscopy reveals polymer effects of disordered proteins in crowded environments. Proc. Natl Acad. Sci. USA 111, 4874-4879. (doi:10.1073/pnas.1322611111).
31. Theillet F-X et al. 2014 Physicochemical properties of cells and their effects on intrinsically disordered proteins (IDPs). Chem. Rev. 114, 6661-6714. (doi:10.1021/cr400695p).
32. Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, Dunker AK. 2008 Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9(Suppl. 1), S1-S0. (doi:10.1186/1471-2164-9-S1-S1).
33. Demarest SJ, Martinez-Yamout M, Chung J, Chen H, Xu W, Dyson HJ, Evans RM, Wright PE. 2002 Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415, 549-553. (doi:10.1038/415549a).
34. Lopes JLS, Orcia D, Araujo APU, DeMarco R, Wallace BA. 2013 Folding factors and partners for the intrinsically disordered protein micro-exon gene 14 (MEG-14). Biophys. J. 104, 2512-2520. (doi:10.1016/j.bpj.2013.03.063).
35. Fuxreiter M, Tompa P. 2012 Advances in experimental medicine and biology. Adv. Exp. Med. Biol. 725, 1-14. (doi:10.1007/978-1-4614-0659-4-1).
36. Kurzbach D, Platzer G, Schwarz TC, Henen MA, Konrat R, Hinderberger D. 2013 Cooperative unfolding of compact conformations of the intrinsically disordered protein osteopontin. Biochemistry 52, 5167-5175. (doi:10.1021/bi400502c).
37. Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, Hughes J. 2002 Osteopontin-a molecule for all seasons. Q. J. Med. 95, 3-13. (doi:10.1093/qjmed/95.1.3).
38. Fedarko NS, Jain A, Karadag A, Fisher LW. 2004 FASEB J. 18, 734-736.
39. Kawasaki K, Suzuki T, Weiss KM. 2004 Genetic basis for the evolution of vertebrate mineralized tissue. Proc. Natl Acad. Sci. USA 101, 11356-11361. (doi:10.1073/pnas.0404279101).
40. Kawasaki K, Weiss KM. 2003 Mineralized tissue and vertebrate evolution: The secretory calcium-binding phosphoprotein gene cluster. Proc. Natl Acad. Sci. USA 100, 4060-4065. (doi:10.1073/pnas.0638023100).
41. Christensen B, Kazanecki CC, Petersen TE, Rittling SR, Denhardt DT, Sørensen ES. 2007 Cell typespecific post-translational modifications of mouse osteopontin are associated with different adhesive properties. J. Biol. Che. 282, 19463-19472. (doi:10.1074/jbc.M703055200).
42. Christensen B, Schack L, Kläning E, Sørensen ES. 2010 Osteopontin is cleaved at multiple sites close to its integrin-binding motifs in milk and is a novel substrate for plasmin and cathepsin D. J. Biol. Chem. 285, 7929-7937. (doi:10.1074/jbc.M109.075010).
43. Yamaguchi Y et al. 2010 NMR characterization of intramolecular interaction of osteopontin, an intrinsically disordered protein with cryptic integrinbinding motifs. Biochem. Biophy. Res. Comm. 393, 487-491. (doi:10.1016/j.bbrc.2010.02.030).
44. Gabel F, Bicout D, Lehnert U, Tehei M, Weik M, Zaccai G. 2002 Protein dynamics studied by neutron scattering. Q. Rev. Biophys. 35, 327-367. (doi:10.1017/S0033583502003840).
45. Zaccai G. 2000 How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science 288, 1604-1607. (doi:10.1126/science.288.5471.1604).
46. Bicout D, Zaccai G. 2001 Protein flexibility from the dynamical transition:a force constant analysis. Biophys. J. 80, 1115-1123. (doi:10.1016/S0006-3495(01)76089-4).
47. Gallat F-X et al. 2012 Dynamical coupling of intrinsically disordered proteins and their hydration water: comparison with folded soluble and membrane proteins. Biophys. J. 103, 129-136. (doi:10.1016/j.bpj.2012.05.027).
48. Réat V, Patzelt H, Ferrand M, Pfister C, Oesterhelt D, Zaccai G. 1998 Dynamics of different functional parts of bacteriorhodopsin: H-2H labeling and neutron scattering. Proc. Natl Acad. Sci. USA 95, 4970-4975. (doi:10.1073/pnas.95.9.4970).
49. Sørensen ES, Højrup P, Petersen TE. 1995 Posttranslational modifications of bovine osteopontin: identification of twenty-eight phosphorylation and three O-glycosylation sites. Protein Sci. 4, 2040-2049. (doi:10.1002/pro.5560041009).
50. Uversky VN. 1993 Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry 32, 13288-13298. (doi:10.1021/bi00211a042).
51. Labrador A, Cerenius Y, Svensson C, Theodor K, Plivelic T. 2013 The yellow mini-hutch for SAXS experiments at MAX IV Laboratory. J. Phys. Conf. Series 425, 072019. (doi:10.1088/1742-6596/425/7/072019).
52. Semenyuk AV, Svergun DI. 1991 GNOM-a program package for small-angle scattering data processing. J. App. Crystallogr. 24, 537-540. (doi:10.1107/S002188989100081X).
53. Bernado P, Svergun DI. 2012 Structural analysis of intrinsically disordered proteins by small-angle X-ray scattering. Mol. Biosyst. 8, 151-167. (doi:10.1039/C1MB05275F).
54. Kohn JE et al. 2004 Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl Acad. Sci. USA 101, 12491-12496. (doi:10.1073/pnas.0403643101).
55. Dewey TG. 1993 Protein structure and polymer collapse. J. Chem. Phys. 98, 2250. (doi:10.1063/1.464205).
56. Franke D, Svergun DI. 2009 DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. App. Crystallogr. 42, 342-346. (doi:10.1107/S0021889809000338).
57. Svergun DI, Petoukhov MV, Koch MH. 2001 Determination of domain structure of proteins from X-Ray solution scattering. Biophys. J. 80, 2946-2953. (doi:10.1016/S0006-3495(01)76260-1).
58. Svergun DI. 1999 Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886. (doi:10.1016/S0006-3495(99)77443-6).
59. Volkov V, Svergun D. 2003 Uniqueness of ab initio shape determination in small-angle scattering. J. App. Crystallogr. 36, 860-864. (doi:10.1107/S0021889803000268).
60. Cilia E, Pancsa R, Tompa P, Lenaerts T, Vranken WF. 2013 From protein sequence to dynamics and disorder with DynaMine. Nat. Comm. 4, 2741. (doi:10.1038/ncomms3741).
61. Jeurnink TJM, De Kruif KG. 1993 Changes in milk on heating: viscosity measurements. J. Dairy Res. 60, 139-150. (doi:10.1017/S0022029900027461).
62. Richard D, Ferrand M, Kearley GJJ. 1996 Analysis and visualisation of neutron-scattering data. Neutron Res. 4, 33-39. (doi:10.1080/10238169608200065).
63. Csizmók V, Szollosi E, Friedrich P, Tompa P. 2006 A novel two-dimensional electrophoresis technique for the identification of intrinsically unstructured proteins. Mol. Cell. Proteomics 5, 265-273. (doi:10.1074/mcp.M500181-MCP200).
64. Lobanov MY, Bogatyreva NS, Galzitskaya OV. 2008 Radius of gyration as an indicator of protein structure compactness. J. Mol. Biol. 42, 623-628. (doi:10.1134/S0026893308040195).
65. Bressan GC, Silva JC, Borges JC, Dos Passos DO, Ramos CHI, Torriani IL, Kobarg J. 2008 Human regulatory protein Ki-1/57 has characteristics of an intrinsically unstructured protein. J. Proteome Res. 7, 4465-4474. (doi:10.1021/pr8005342).
66. Eliezer D. 2009 Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol. 19, 23-30. (doi:10.1016/j.sbi.2008.12.004).
67. Flory PJ. 1969 Statistical mechanics of chain molecules. New York, NY: Wiley Interscience.
68. Receveur-Brechot V, Durand D. 2012 How random are intrinsically disordered proteins? A small angle scattering perspective. Curr. Protein Peptide Sci. 13, 55-75. (doi:10.2174/138920312799277901).
69. Pérez J, Zanotti JM, Durand D. 1999 Evolution of the internal dynamics of two globular proteins from dry powder to solution. Biophys. J. 77, 454-469. (doi:10.1016/S0006-3495(99)76903-1).
70. Perticaroli S, Nickels JD, Ehlers G, Mamontov E, Sokolov AP. 2014 Dynamics and rigidity in an intrinsically disordered protein, b-casein. J. Phys. Chem. B 118, 7317-7326. (doi:10.1021/jp503788r).
71. Gaspar A, Appavou M-S, Busch S, Unruh T, Doster W. 2008 Dynamics of well-folded and natively disordered proteins in solution: A time-of-flight neutron scattering study. Eur. Biophys. J. 37, 573-582. (doi:10.1007/s00249-008-0266-3).
72. Doster W, Cusack S, Petry W. 1989 Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337, 754-756. (doi:10.1038/337754a0).
73. Doster W, Nakagawa H, Appavou MS. 2013 Scaling analysis of bio-molecular dynamics derived from elastic incoherent neutron scattering experiments. J. Chem. Phys. 139, 045105. (doi:10.1063/1.4816513).
74. Ferrand M, Dianoux AJ, Petry W, Zaccai G. 1993 Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering. Proc. Natl Acad. Sci. USA 90, 9668-9672. (doi:10.1073/pnas.90.20.9668).
75. Stadler A, Digel I, Embs J, Unruh T, Tehei M, Zaccai G, Büldt G, Artmann G. 2009 From powder to solution: hydration dependence of human hemoglobin dynamics correlated to body temperature. Biophys. J. 96, 5073-5081. (doi:10.1016/j.bpj.2009.03.043).
76. Qin S, Zhou H-X. 2013 Effects of macromolecular crowding on the conformational ensembles of disordered proteins. J. Phys. Chem. Lett. 4, 3429-3434. (doi:10.1021/jz401817x).
77. Rodriguez DE, Thula-Mata T, Toro EJ, Yeh Y-W, Holt C, Holliday LS, Gower LB. 2014 Multifunctional role of osteopontin in directing intrafibrillar mineralization of collagen and activation of osteoclasts. Acta Biomat. 10, 494-507. (doi:10.1016/j.actbio.2013.10.010).