Aged male rats regenerate cortical bone with reduced osteocyte density and reduced secretion of nitric oxide after mechanical stimulation

Calcified Tissue International

Volumn 94, Issue 5, 2014, Pages 484-494

  Joiner, Danese M ^a   Tayim, Riyad J ^a   McElderry, John David ^a   Morris, Michael D ^a   Goldstein, Steven A ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Aging; Bone regeneration; Fragility; Mechanotransduction; Osteocyte

Indexed keywords

CONNEXIN 43; NITRIC OXIDE; PROSTAGLANDIN E2;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MATRIX; BONE MINERALIZATION; BONE REGENERATION; BONE TISSUE; CELL DENSITY; CELLULAR SECRETION; CONTROLLED STUDY; CORTICAL BONE; DIAPHYSIS; EXPLANT; GAP JUNCTION; GEOMETRY; MALE; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; NONHUMAN; OSSIFICATION; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; AGING; ANIMAL; BONE; CYTOLOGY; MECHANICAL STRESS; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; PHYSIOLOGY; RAMAN SPECTROMETRY; SECRETION (PROCESS); SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STIMULATION; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; BONE AND BONES; BONE REGENERATION; CALCIFICATION, PHYSIOLOGIC; MALE; MECHANOTRANSDUCTION, CELLULAR; NITRIC OXIDE; OSTEOCYTES; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPECTRUM ANALYSIS, RAMAN; STRESS, MECHANICAL; X-RAY MICROTOMOGRAPHY;

EID: 84898856014     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-013-9832-5     Document Type: Article

References (46)

1. Rubin CT, Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am 66(3):397-402
2. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285(33):25103-25108
3. Robling AG, Castillo AB, Turner CH (2006) Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 8:455-498
4. Szulc P, Garnero P, Munoz F, Marchand F, Delmas PD (2001) Cross-sectional evaluation of bone metabolism in men. J Bone Miner Res 16(9):1642-1650
5. Loiselle AE, Jiang JX, Donahue HJ (2013) Gap junction and hemichannel functions in osteocytes. Bone 54:205-212
6. Stains JP, Civitelli R (2005) Gap junctions in skeletal development and function. Biochim Biophys Acta 1719(1-2):69-81
7. Blackwell KA, Raisz LG, Pilbeam CC (2010) Prostaglandins in bone: bad cop, good cop? Trends Endocrinol Metab 21(5):294-301
8. 2 induces early-response genes in rat bones. Bone 20(4):347-353
9. 2 on bone in mice in vivo. Prostaglandins Other Lipid Mediat 89(1-2):20-25
10. Dekel S, Lenthall G, Francis MJ (1981) Release of prostaglandins from bone and muscle after tibial fracture: an experimental study in rabbits. J Bone Joint Surg Br 63-B(2):185-189
11. Naik AA, Xie C, Zuscik MJ, Kingsley P, Schwarz EM, Awad H et al (2009) Reduced COX-2 expression in aged mice is associated with impaired fracture healing. J Bone Miner Res 24(2):251-264
12. Chow JW, Fox SW, Lean JM, Chambers TJ (1998) Role of nitric oxide and prostaglandins in mechanically induced bone formation. J Bone Miner Res 13(6):1039-1044
13. van't Hof RJ, Ralston SH (2001) Nitric oxide and bone. Immunology 103(3):255-261
14. Damoulis PD, Hauschka PV (1997) Nitric oxide acts in conjunction with proinflammatory cytokines to promote cell death in osteoblasts. J Bone Miner Res 12(3):412-422
15. Zhu W, Diwan AD, Lin JH, Murrell GA (2001) Nitric oxide synthase isoforms during fracture healing. J Bone Miner Res 16(3):535-540
16. Diwan AD, Wang MX, Jang D, Zhu W, Murrell GA (2000) Nitric oxide modulates fracture healing. J Bone Miner Res 15(2):342-351
17. Baldik Y, Diwan AD, Appleyard RC, Fang ZM, Wang Y, Murrell GA (2005) Deletion of iNOS gene impairs mouse fracture healing. Bone 37(1):32-36
18. Cau SB, Carneiro FS, Tostes RC (2012) Differential modulation of nitric oxide synthases in aging: therapeutic opportunities. Front Physiol 3:218
19. Waldorff EI, Christenson KB, Cooney LA, Goldstein SA (2010) Microdamage repair and remodeling requires mechanical loading. J Bone Miner Res 25(4):734-745
20. Turner CH, Takano Y, Owan I (1995) Aging changes mechanical loading thresholds for bone formation in rats. J Bone Miner Res 10(10):1544-1549
21. Donahue SW, Jacobs CR, Donahue HJ (2001) Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. Am J Physiol Cell Physiol 281(5):C1635-C1641
22. Rubin CT, Bain SD, McLeod KJ (1992) Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50(4):306-313
23. Silbermann M, Bar-Shira-Maymon B, Coleman R, Reznick A, Weisman Y, Steinhagen-Thiessen E et al (1990) Long-term physical exercise retards trabecular bone loss in lumbar vertebrae of aging female mice. Calcif Tissue Int 46(2):80-93
24. Buhl KM, Jacobs CR, Turner RT, Evans GL, Farrell PA, Donahue HJ (2001) Aged bone displays an increased responsiveness to low-intensity resistance exercise. J Appl Physiol 90(4):1359-1364
25. Srinivasan S, Agans SC, King KA, Moy NY, Poliachik SL, Gross TS (2003) Enabling bone formation in the aged skeleton via rest-inserted mechanical loading. Bone 33(6):946-955
26. Pruitt LA, Taaffe DR, Marcus R (1995) Effects of a 1 year high-intensity versus low-intensity resistance training program on bone mineral density in older women. J Bone Miner Res 10(11):1788-1795
27. Allison SJ, Folland JP, Rennie WJ, Summers GD, Brooke-Wavell K (2013) High impact exercise increased femoral neck bone mineral density in older men: a randomised unilateral intervention. Bone 53:321-328
28. Hoffler CE, Hankenson KD, Miller JD, Bilkhu SK, Goldstein SA (2006) Novel explant model to study mechanotransduction and cell-cell communication. J Orthop Res 24(8):1687-1698
29. Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA (2009) Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 45(6):1104-1116
30. Volkman SK, Galecki AT, Burke DT, Paczas MR, Moalli MR, Miller RA et al (2003) Quantitative trait loci for femoral size and shape in a genetically heterogeneous mouse population. J Bone Miner Res 18(8):1497-1505
31. Draper ER, Morris MD, Camacho NP, Matousek P, Towrie M, Parker AW et al (2005) Novel assessment of bone using time-resolved transcutaneous Raman spectroscopy. J Bone Miner Res 20(11):1968-1972
32. Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, Hughes J (2002) Osteopontin - a molecule for all seasons. QJM 95(1):3-13
33. Cheng MZ, Zaman G, Rawlinson SC, Pitsillides AA, Suswillo RF, Lanyon LE (1997) Enhancement by sex hormones of the osteoregulatory effects of mechanical loading and prostaglandins in explants of rat ulnae. J Bone Miner Res 12(9):1424-1430
34. Waldorff EI, Goldstein SA, McCreadie BR (2007) Age-dependent microdamage removal following mechanically induced microdamage in trabecular bone in vivo. Bone 40(2):425-432
35. Bonar LC, Roufosse AH, Sabine WK, Grynpas MD, Glimcher MJ (1983) X-ray diffraction studies of the crystallinity of bone mineral in newly synthesized and density fractionated bone. Calcif Tissue Int 35(2):202-209
36. Currey JD (1984) Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci 304(1121):509-518
37. Donnelly E, Chen DX, Boskey AL, Baker SP, van der Meulen MC (2010) Contribution of mineral to bone structural behavior and tissue mechanical properties. Calcif Tissue Int 87(5):450-460
38. Burr DB (2002) The contribution of the organic matrix to bone's material properties. Bone 31(1):8-11
39. Raghavan M, Sahar ND, Kohn DH, Morris MD (2012) Age-specific profiles of tissue-level composition and mechanical properties in murine cortical bone. Bone 50(4):942-953
40. Yerramshetty JS, Akkus O (2008) The associations between mineral crystallinity and the mechanical properties of human cortical bone. Bone 42(3):476-482
41. Mehta M, Strube P, Peters A, Perka C, Hutmacher D, Fratzl P et al (2010) Influences of age and mechanical stability on volume, microstructure, and mineralization of the fracture callus during bone healing: is osteoclast activity the key to age-related impaired healing? Bone 47(2):219-228
42. Joiner DM, Tayim RJ, Kadado A, Goldstein SA (2012) Bone marrow stromal cells from aged male rats have delayed mineralization and reduced response to mechanical stimulation through nitric oxide and ERK1/2 signaling during osteogenic differentiation. Biogerontology 13(5):467-478
43. Justesen J, Stenderup K, Eriksen EF, Kassem M (2002) Maintenance of osteoblastic and adipocytic differentiation potential with age and osteoporosis in human marrow stromal cell cultures. Calcif Tissue Int 1:36-44
44. Busse B, Djonic D, Milovanovic P, Hahn M, Puschel K, Ritchie RO et al (2010) Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9(6):1065-1075
45. Vashishth D, Verborgt O, Divine G, Schaffler MB, Fyhrie DP (2000) Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 26(4):375-380
46. Xia X, Batra N, Shi Q, Bonewald LF, Sprague E, Jiang JX (2010) Prostaglandin promotion of osteocyte gap junction function through transcriptional regulation of connexin 43 by glycogen synthase kinase 3/beta-catenin signaling. Mol Cell Biol 30(1):206-219