Total water, phosphorus relaxation and inter-atomic organic to inorganic interface are new determinants of trabecular bone integrity

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Rai, Ratan Kumar ^a   Barbhuyan, Tarun ^b   Singh, Chandan ^a   Mittal, Monika ^b   Khan, Mohd Parvez ^b   Sinha, Neeraj ^a   Chattopadhyay, Naibedya ^b  

^a SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

^b CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BONE AND BONES; BONE DENSITY; BONE DISEASES, METABOLIC; EPIPHYSES; FEMALE; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OVARIECTOMY; PHOSPHORUS; RATS; WATER;

EID: 84893625027     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083478     Document Type: Article

References (48)

1. Meier DE, Orwoll ES, Jones JM (1984) Marked disparity between trabecular and cortical bone loss with age in healthy men. Measurement by vertebral computed tomography and radial photon absorptiometry. Ann Intern Med 101: 605-612. (Pubitemid 15223296)
2. Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3 Suppl 3: S131-139.
3. Compston J (2011) Age-Related Changes in Bone Remodelling and Structure in Men: Histomorphometric Studies. Journal of Osteoporosis 2011: 4.
4. Kovacs CS, Kronenberg HM (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 18: 832-872. (Pubitemid 28009569)
5. Kalkwarf HJ (1999) Hormonal and dietary regulation of changes in bone density during lactation and after weaning in women. J Mammary Gland Biol Neoplasia 4: 319-329.
6. Ardeshirpour L, Dann P, Adams DJ, Nelson T, VanHouten J, et al. (2007) Weaning triggers a decrease in receptor activator of nuclear factor-kappaB ligand expression, widespread osteoclast apoptosis, and rapid recovery of bone mass after lactation in mice. Endocrinology 148: 3875-3886. (Pubitemid 47105861)
7. Raggatt LJ, Partridge NC (2010) Cellular and Molecular Mechanisms of Bone Remodeling. Journal of Biological Chemistry 285: 25103-25108.
8. Weiner S WH (1998) The material bone: Structure mechanical function relations. Annu ReV Mater Sci 28: 271-298
9. R K Rai NS (2011) Dehydration-Induced Structural Changes in the Collagen-Hydroxyapatite Interface in Bone by High-Resolution Solid-State NMR Spectroscopy. The Journal of Physical Chemistry C 115 (29): 14219-14227.
10. Cho G, Wu Y, Ackerman JL (2003) Detection of hydroxyl ions in bone mineral by solid-state NMR spectroscopy. Science 300: 1123-1127. (Pubitemid 36583091)
11. Wehrli FW, Fernandez-Seara MA (2005) Nuclear magnetic resonance studies of bone water. Ann Biomed Eng 33: 79-86. (Pubitemid 40496062)
12. Wilson EE, Awonusi A, Morris MD, Kohn DH, Tecklenburg MM, et al. (2005) Highly ordered interstitial water observed in bone by nuclear magnetic resonance. J Bone Miner Res 20: 625-634. (Pubitemid 40393071)
13. Fernandez-Seara MA, Wehrli SL, Takahashi M, Wehrli FW (2004) Water content measured by proton-deuteron exchange NMR predicts bone mineral density and mechanical properties. J Bone Miner Res 19: 289-296. (Pubitemid 38116743)
14. Robinson RA (1975) Physiocochemical structure of bone. Clin Orthop Relat Res: 263-315.
15. Nyman JS, Ni Q, Nicolella DP, Wang X (2008) Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone 42: 193-199. (Pubitemid 350297186)
16. Reichert D, Pascui O, deAzevedo ER, Bonagamba TJ, Arnold K, et al. (2004) A solid-state NMR study of the fast and slow dynamics of collagen fibrils at varying hydration levels. Magnetic Resonance in Chemistry 42: 276-284. (Pubitemid 38178097)
17. Zhu P, Xu J, Sahar N, Morris MD, Kohn DH, et al. (2009) Time-Resolved Dehydration-Induced Structural Changes in an Intact Bovine Cortical Bone Revealed by Solid-State NMR Spectroscopy. J Am Chem Soc 131: 17064-17065.
18. Nikel O, Laurencin D, Bonhomme C, Sroga GE, Besdo S, et al. (2012) 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 Nanomater Interfaces 116: 6320-6331.
19. Xu J, Zhu P, Morris MD, Ramamoorthy A (2011) Solid-State NMR Spectroscopy Provides Atomic-Level Insights Into the Dehydration of Cartilage. J Phys Chem B 115: 9948-9954.
20. Singh C, Rai RK, Sinha N (2013) Experimental aspect of solid-state nuclear magnetic resonance studies of biomaterials such as bones. Solid State Nucl Magn Reson 54: 18-25.
21. Wilson EE, Awonusi A, Morris MD, Kohn DH, Tecklenburg MM, et al. (2006) Three structural roles for water in bone observed by solid-state NMR. Biophys J 90: 3722-3731.
22. Zhang Q, Hu JZ, Rommereim DN, Murphy MK, Phipps RP, et al. (2009) Application of High-Resolution 1H MAS NMR Spectroscopy to the Analysis of Intact Bones from Mice Exposed to Gamma Radiation. Radiation Research 172: 607-616.
23. Takata S, Shibata A, Yonezu H, Yamada T, Takahashi M, et al. (2004) Biophysic evaluation of bone quality-application of Fourier transform infrared spectroscopy and phosphorus-31 solid-state nuclear magnetic resonance spectroscopy& mdash. The Journal of Medical Investigation 51: 133-138. (Pubitemid 39610906)
24. Kaflak A, Kolodziejski W (2007) Phosphorus-31 spin-lattice NMR relaxation in bone apatite and its mineral standards. Solid State Nucl Magn Reson: 174-183. (Pubitemid 47021348)
25. Saito H, Tabeta R, Shoji A, Ozaki T, Ando I, et al. (1984) A high-resolution 13C-NMR study of collagenlike polypeptides and collagen fibrils in solid state studied by the cross-polarization-magic angle-spinning method. Manifestation of conformation-dependent 13C chemical shifts and application to conformational characterization. Biopolymers 23: 2279-2297. (Pubitemid 15217124)
26. Saito H, Yokoi M (1992) A 13C NMR study on collagens in the solid state: hydration/dehydration-induced conformational change of collagen and detection of internal motions. J Biochem 111: 376-382.
27. Portal-Nunez S, Lozano D, Esbrit P (2012) Role of angiogenesis on bone formation. Histol Histopathol 27: 559-566.
28. Maes C, Carmeliet P, Moermans K, Stockmans I, Smets N, et al. (2002) Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111: 61-73. (Pubitemid 34136979)
29. Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, et al. (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27: 1018-1029.
30. Belanger LF (1969) Osteocytic osteolysis. Calcif Tissue Res 4: 1-12.
31. Baud CA, Boivin G (1978) Effects of hormones on osteocyte function and perilacunar wall structure. Clin Orthop Relat Res: 270-281.
32. Recker RR, Bare SP, Smith SY, Varela A, Miller MA, et al. (2009) Cancellous and cortical bone architecture and turnover at the iliac crest of postmenopausal osteoporotic women treated with parathyroid hormone 1-84. Bone 44: 113-119.
33. Miller MA, Bare SP, Recker RR, Smith SY, Fox J (2008) Intratrabecular tunneling increases trabecular number throughout the skeleton of ovariectomized rhesus monkeys treated with parathyroid hormone 1-84. Bone 42: 1175-1183.
34. Jerome CP, Burr DB, Van Bibber T, Hock JM, Brommage R (2001) Treatment with human parathyroid hormone (1-34) for 18 months increases cancellous bone volume and improves trabecular architecture in ovariectomized cynomolgus monkeys (Macaca fascicularis). Bone 28: 150-159. (Pubitemid 32140971)
35. Iida-Klein A, Lu SS, Cosman F, Lindsay R, Dempster DW (2007) Effects of cyclic vs. daily treatment with human parathyroid hormone (1-34) on murine bone structure and cellular activity. Bone 40: 391-398. (Pubitemid 46054555)
36. Mroue KH, MacKinnon N, Xu J, Zhu P, McNerny E, et al. (2012) High-Resolution Structural Insights into Bone: A Solid-State NMR Relaxation Study Utilizing Paramagnetic Doping. J Phys Chem B 116: 11656-11661.
37. Trivedi R, Kumar A, Gupta V, Kumar S, Nagar GK, et al. (2009) Effects of Egb 761 on bone mineral density, bone microstructure, and osteoblast function: Possible roles of quercetin and kaempferol. Mol Cell Endocrinol 302: 86-91.
38. Tyagi AM, Srivastava K, Singh AK, Kumar A, Changkija B, et al. (2012) Formononetin reverses established osteopenia in adult ovariectomized rats. Menopause 19: 856-863.
39. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, et al. (2010) Guidelines for assessment of bone microstructure in rodents using microcomputed tomography. J Bone Miner Res 25: 1468-1486.
40. Sharan K, Swarnkar G, Siddiqui JA, Kumar A, Rawat P, et al. (2010) A novel flavonoid, 6-C-beta-d-glucopyranosyl-(2S,3S)-(+) - 3′, 4′,5,7-tetrahydroxyflavanone, isolated from Ulmus wallichiana Planchon mitigates ovariectomy-induced osteoporosis in rats. Menopause 17: 577-586.
41. Siddiqui JA, Sharan K, Swarnkar G, Rawat P, Kumar M, et al. (2011) Quercetin-6-C-beta-D-glucopyranoside isolated from Ulmus wallichiana planchon is more potent than quercetin in inhibiting osteoclastogenesis and mitigating ovariectomy-induced bone loss in rats. Menopause 18: 198-207.
42. Khan K, Sharan K, Swarnkar G, Chakravarti B, Mittal M, et al. (2013) Positive skeletal effects of cladrin, a naturally occurring dimethoxydaidzein, in osteopenic rats that were maintained after treatment discontinuation. Osteoporos Int 24: 1455-1470.
43. Sharan K, Mishra JS, Swarnkar G, Siddiqui JA, Khan K, et al. (2011) A novel quercetin analogue from a medicinal plant promotes peak bone mass achievement and bone healing after injury and exerts an anabolic effect on osteoporotic bone: the role of aryl hydrocarbon receptor as a mediator of osteogenic action. J Bone Miner Res 26: 2096-2111.
44. Odgaard A, Gundersen HJG (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14: 173-182. (Pubitemid 23098966)
45. Srivastava K, Khan K, Tyagi AM, Khan MP, Yadav DK, et al. (2013) Greater Skeletal Gains in Ovary Intact Rats at Maturity Are Achieved by Supplementing a Standardized Extract of Butea monosperma Stem Bark that Confers Better Bone Conserving Effect following Ovariectomy and Concurrent Treatment Withdrawal. Evidence-Based Complementary and Alternative Medicine 2013: 12.
46. Zhang G, Qin L, Shi Y, Leung K (2005) A comparative study between axial compression and lateral fall configuration tested in a rat proximal femur model. Clinical biomechanics (Bristol, Avon) 20: 729-735. (Pubitemid 40917243)
47. Vinogradov E, Madhu PK, Vega S (1999) High-resolution proton solid-state NMR spectroscopy by phase-modulated Lee-Goldburg experiment. Chem Phys Lett 314: 443-450. (Pubitemid 129594703)
48. Gullion T, Schaefer J (1989) Rotational-echo double-resonance NMR. Journal of Magnetic Resonance (1969) 81: 196-200.