NMR investigation of the role of osteocalcin and osteopontin at the organic-inorganic interface in bone

Langmuir

Volumn 29, Issue 45, 2013, Pages 13873-13882

  Nikel, Ondřej ^a,b   Laurencin, Danielle ^b   McCallum, Scott A ^a   Gundberg, Caren M ^c   Vashishth, Deepak ^a  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPERIMENTAL EVIDENCE; GENETICALLY MODIFIED; ISOTOPIC ENRICHMENT; MOLECULAR LEVELS; ORGANIC-INORGANIC INTERFACE; POST-TRANSLATIONAL MODIFICATIONS; SOLID-STATE NUCLEAR MAGNETIC RESONANCE; STRUCTURAL INFORMATION;

AMINO ACIDS; FRACTURE TOUGHNESS; MAMMALS; MATRIX ALGEBRA; MINERALS; TISSUE;

BONE;

MINERAL; ORGANIC COMPOUND; OSTEOCALCIN; OSTEOPONTIN;

ANIMAL; ARTICLE; FEMUR; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY;

ANIMALS; FEMUR; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MINERALS; ORGANIC CHEMICALS; OSTEOCALCIN; OSTEOPONTIN;

EID: 84887600965     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la403203w     Document Type: Article

References (61)

1. Martin, B. Aging and strength of bone as a structural material Calcif. Tissue Int. 1993, 53, S34-9
2. Burge, R.; Dawson-Hughes, B.; Solomon, D. H.; Wong, J. B.; King, A.; Tosteson, A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025 J. Bone Miner. Res. 2007, 22, 465-75
3. Dempster, D. W. Osteoporosis and the burden of osteoporosis-related fractures Am. J. Managed Care 2011, 17, S164-69
4. Kanis, J. A.; Oden, A.; Johansson, H.; Borgstrom, F.; Strom, O.; McCloskey, E. FRAX and its applications to clinical practice Bone 2009, 44, 734-43
5. Launey, M. E.; Buehler, M. J.; Ritchie, R. O. On the mechanistic origins of toughness in bone Annu. Rev. Mater. Res. 2010, 40, 25-53
6. Gupta, H. S.; Seto, J.; Wagermaier, W.; Zaslansky, P.; Boesecke, P.; Fratzl, P. Cooperative deformation of mineral and collagen in bone at the nanoscale Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 17741-6
7. Fantner, G. E.; Hassenkam, T.; Kindt, J. H.; Weaver, J. C.; Birkedal, H.; Pechenik, L.; Cutroni, J. A.; Cidade, G. A. G.; Stucky, G. D.; Morse, D. E.; Hansma, P. K. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture Nat. Mater. 2005, 4, 612-6
8. Gupta, H. S.; Fratzl, P.; Kerschnitzki, M.; Benecke, G.; Wagermaier, W.; Kirchner, H. O. K. Evidence for an elementary process in bone plasticity with an activation enthalpy of 1 eV J. R. Soc. Interface 2007, 4, 277-82
9. Fantner, G. E.; Adams, J.; Turner, P.; Thurner, P. J.; Fisher, L. W.; Hansma, P. K. Nanoscale ion mediated networks in bone: Osteopontin can repeatedly dissipate large amounts of energy Nano Lett. 2007, 7, 2491-8
10. Buehler, M. J. Molecular nanomechanics of nascent bone: Fibrillar toughening by mineralization Nanotechnology 2007, 18, 295102/1-295102/9
11. Poundarik, A. A.; Diab, T.; Sroga, G. E.; Ural, A.; Boskey, A. L.; Gundberg, C. M.; Vashishth, D. Dilatational band formation in bone Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 19178-83
12. Romberg, R. W.; Werness, P. G.; Riggs, B. L.; Mann, K. G. Inhibition of hydroxyapatite-crystal growth by bone-specific and other calcium-binding proteins Biochemistry 1986, 25, 1176-80
13. Hunter, G. K.; Kyle, C. L.; Goldberg, H. A. Modulation of crystal formation by bone phosphoproteins: Structural specificity of the osteopontin-mediated inhibition of hydroxyapatite formation Biochem. J. 1994, 300, 723-8
14. Hunter, G. K.; Haushka, P. V.; Poole, A. R.; Rosenberg, L. C.; Goldberg, H. A. Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins Biochem. J. 1996, 317, 59-64
15. Martinek, N.; Shahab, J.; Sodek, J.; Ringuette, M. Is SPARC an evolutionarily conserved collagen chaperone? J. Dent. Res. 2007, 86, 296-305
16. Vejlens, L. Glycosaminoglycans of human bone tissue. I. Pattern of compact bone in relation to age Calcif. Tissue Res. 1971, 7, 175-90
17. Dickens, F. The citric acid content of animal tissues, with reference to its occurrence in bone and tumour Biochem. J. 1941, 35, 1011-23
18. Sroga, G., E.; Vashishth, D. Effects of bone matrix proteins on fracture and fragility in osteoporosis Curr. Osteoporos. Rep. 2012, 10, 141-50
19. 31P HetCor experiments on bone, bone mineral, and model calcium phosphate phases J. Magn. Reson., Ser. B 1994, 105, 183-7
20. Wu, Y.; Ackerman, J. L.; Kim, H.-M.; Rey, C.; Barroug, A.; Glimcher, M. J. Nuclear magnetic resonance spin-spin relaxation of the crystals of bone, dental enamel, and synthetic hydroxyapatites J. Bone Miner. Res. 2002, 17, 472-80
21. 31P solid-state NMR spectroscopy at early stages of mineralization Calcif. Tissue Int. 2003, 72, 610-26
22. Pourpoint, F.; Coelho Diogo, C.; Gervais, C.; Bonhomme, C.; Fayon, F.; Dalicieux, S. L.; Gennero, I.; Salles, J.-P.; Howes, A. P.; Dupree, R.; Hanna, J. V.; Smith, M. E.; Mauri, F.; Guerrero, G.; Mutin, P. H.; Laurencin, D. High-resolution solid state NMR experiments for the characterization of calcium phosphate biomaterials and biominerals J. Mater. Res. 2011, 26, 2355-68
23. 31P CP/MAS NMR study of human bone mineral Calcif. Tissue Int. 2003, 73, 476-86
24. Cho, G.; Wu, Y.; Ackerman, J. L. Spectroscopy detection of hydroxyl ions in bone mineral by solid-state NMR Science 2003, 300, 1123-7
25. Maltsev, S.; Duer, M. J.; Murray, R. C.; Jaeger, C. A solid-state NMR comparison of the mineral structure in bone from diseased joints in the horse J. Mater. Sci. 2007, 42, 8804-10
26. Kolodziejski, W. Solid-state NMR studies of bone Top. Curr. Chem. 2005, 246, 235-70
27. Singh, C.; Rai, R. K.; Sinha, N. Experimental aspect of solid-state nuclear magnetic resonance studies of biomaterials such as bones Solid State Nucl. Magn. Reson. 2013, 54, 18-25
28. Zhu, P.; Xu, J.; Sahar, N.; Morris, M. D.; Kohn, D. H.; Ramamoorthy, A. Time-resolved dehydration-induced structural changes in an intact bovine cortical bone revealed by solid-state NMR spectroscopy J. Am. Chem. Soc. 2009, 131, 17064-5
29. 13C solid-state NMR spectroscopy to study collagen synthesis and biomineralization in polymer-based bone implants NMR Biomed. 2012, 25, 464-75
30. Gullion, T.; Schaefer, J. Rotational-echo double-resonance NMR J. Magn. Reson. 1989, 81, 196-200
31. 31P} REDOR NMR investigation of the role of glutamic acid residues in statherin-hydroxyapatite recognition Langmuir 2009, 25, 12136-43
32. Ndao, M.; Ash, J. T.; Stayton, P. S.; Drobny, G. P. The role of basic amino acids in the molecular recognition of hydroxyapatite by statherin using solid state NMR Surf. Sci. 2010, 604, L39-42
33. Reid, D. G.; Duer, M. J.; Murray, R. C.; Wise, E. R. The organic-mineral interface in teeth is like that in bone and dominated by polysaccharides: Universal mediators of normal calcium phosphate biomineralization in vertebrates? Chem. Mater. 2008, 20, 3549-50
34. Reid, D. G.; Jackson, G. J.; Duer, M. J.; Rodgers, A. L. Apatite in kidney stones is a molecular composite with glycosaminoglycans and proteins: Evidence from nuclear magnetic resonance spectroscopy, and relevance to Randall's plaque, pathogenesis and prophylaxis J. Urol. 2011, 185, 725-30
35. Duer, M. J.; Friscic, T.; Murray, R. C.; Reid, D. G.; Wise, E. R. The mineral phase of calcified cartilage: Its molecular structure and interface with the organic matrix Biophys. J. 2009, 96, 3372-8
36. Duer, M. J.; Friscic, T.; Proudfoot, D.; Reid, D. G.; Schoppet, M.; Shanahan, C. M.; Skepper, J. N.; Wise, E. R. Mineral surface in calcified plaque is like that of bone: Further evidence for regulated mineralization Arterioscler., Thromb., Vasc. Biol. 2008, 28, 2030-4
37. 3 biomineral in crayfish gastroliths Proc. Nat. Acad. Sci. U.S.A. 2011, 108, 14763-8
38. Jaeger, C.; Groom, N. S.; Bowe, E. A.; Horner, A.; Davies, M. E.; Murray, R. C.; Duer, M. J. Investigation of the nature of the protein-mineral interface in bone by solid-state NMR Chem. Mater. 2005, 17, 3059-61
39. Wise, E. R.; Maltsev, S.; Davies, M. E.; Duer, M. J.; Jaeger, C.; Loveridge, N.; Murray, R. C.; Reid, D. G. The organic-mineral interface in bone is predominantly polysaccharide Chem. Mater. 2007, 19, 5055-7
40. Hu, Y. Y.; Rawal, A.; Schmidt-Rohr, K. Strongly bound citrate stabilizes the apatite nanocrystals in bone Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 22425-9
41. Rai, R. K.; Sinha, N. Dehydration-induced structural changes in the collagenhydroxyapatite interface in bone by high-resolution solid-state NMR spectroscopy J. Phys. Chem. C 2011, 115, 14219-27
42. Nikel, O.; Laurencin, D.; Bonhomme, C.; Sroga, G. E.; Besdo, S.; Lorenz, A.; Vashishth, D. Solid state NMR investigation of intact human bone quality: Balancing issues and insight into the structure at the organic-mineral interface J. Phys. Chem. C 2012, 116, 6320-31
43. Ducy, P.; Desbois, C.; Boyce, B.; Pinero, G.; Story, B.; Dunstan, C.; Smith, E.; Bonadio, J.; Goldstein, S.; Gundberg, C. M.; Bradley, A.; Karsenty, G. Increased bone formation in osteocalcin-deficient mice Nature 1996, 382, 448-52
44. Rittling, S. R.; Matsumoto, H. N.; McKee, M. D.; Nanci, A.; An, X.-R.; Novick, K. E.; Kowalski, A. J.; Noda, M.; Denhardt, D. T. Mice lacking osteopontin show normal development and bone structure but display altered osteoclast formation in vitro J. Bone Miner. Res. 1998, 13, 1101-11
45. Aliev, A. E. Solid-state NMR studies of collagen-based parchments and gelatin Biopolymers 2005, 77, 230-45
46. Massiot, D.; Fayon, F.; Capron, M.; King, I.; Le Calve, S.; Alonso, B.; Durand, J.-O.; Bujoli, B.; Gan, Z.; Hoatson, G. Modelling one- and two-dimensional solid-state NMR spectra Magn. Reson. Chem. 2002, 40, 70-6
47. Mason, H. E.; Kozlowski, A.; Phillips, B. L. Solid-state NMR study of the role of H and Na in AB-type carbonate hydroxylapatite Chem. Mater. 2008, 20, 294-302
48. Reid, D. G.; Duer, M. J.; Jackson, G. E.; Murray, R. C.; Rodgers, A. L.; Shanahan, C. M. Citrate occurs widely in healthy and pathological apatitic biomineral: Mineralized articular cartilage, and intimal atherosclerotic plaque and apatitic kidney stones Calcif. Tissue Int. 2013, 93, 253-260
49. Chow, W. Y.; Taylor, A. M.; Reid, D. G.; Gallagher, J. A.; Duer, M. J. Collagen atomic scale molecular disorder in ochronotic cartilage from an alkaptonuria patient, observed by solid state NMR J. Inherited Metab. Dis. 2011, 34, 1137-40
50. Duer, M. J.; Solid State NMR Spectroscopy: Principles and Applications; Blackwell Science: Oxford, U.K., 2002.
51. Alexander, B.; Daulton, T. L.; Genin, G. M.; Lipner, J.; Pasteris, J. D.; Wopenka, B.; Thomopoulos, S. The nanometre-scale physiology of bone: Steric modelling and scanning transmission electron microscopy of collagen-mineral structure J. R. Soc., Interface 2012, 9, 1774-86
52. 1H NMR spectroscopy Biochemistry 2003, 42, 7769-79
53. Knott, L.; Bailey, A. J. Collagen cross-links in mineralizing tissues: A review of their chemistry, function, and clinical relevance Bone 1998, 22, 181-7
54. Yamauchi, M.; Shiiba, M. Lysine hydroxylation and cross-linking of collagen Methods Mol. Biol. 2008, 446, 95-108
55. McDermott, A. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR Annu. Rev. Biophys. 2009, 38, 385-403
56. 13C-labelled proteins J. Biomol. NMR 2009, 44, 245-60
57. Comellas, G.; Rienstra, C. M. Protein structure determination by magic-angle spinning solid-state NMR, and insights into the formation, structure, and stability of amyloid fibrils Annu. Rev. Biophys. 2013, 42, 515-36
58. Rienstra, C. M.; Tucker-Kellogg, L.; Jaroniec, C. P.; Hohwy, M.; Reif, B.; McMahon, M. T.; Tidor, B.; Lozano-Perez, T.; Griffin, R. G. De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 10260-5
59. Zech, S. G.; Wand, A. J.; McDermott, A. E. Protein structure determination by high-resolution solid-state NMR spectroscopy: Application to microcrystalline ubiquitin J. Am. Chem. Soc. 2005, 127, 8618-26
60. 15N-labeled solids J. Am. Chem. Soc. 2002, 124, 10728-42
61. 19F-dephased REDOR shift (FRESH) spectroscopy Magn. Reson. Chem. 2007, 45, S129-34