Rescuing loading induced bone formation at senescence

PLoS Computational Biology

Volumn 6, Issue 9, 2010, Pages

  Srinivasan, Sundar ^a   Ausk, Brandon J ^a   Prasad, Jitendra ^a   Threet, Dewayne ^a   Bain, Steven D ^a   Richardson, Thomas S ^a   Gross, Ted S ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTONOMOUS AGENTS; BONE; COMPUTATIONAL METHODS; DISEASES; LOADING;

AGE-RELATED; BONE FORMATION; CELL RESPONSE; CELLULAR SIGNALLING; HEALTHCARE SYSTEMS; HIGH-FIDELITY CONTROLS; MECHANICAL STIMULUS; MECHANOTRANSDUCTION; REAL- TIME; TISSUE ADAPTATION;

CELL SIGNALING;

CALCIUM ION; CYCLOSPORIN A; TRANSCRIPTION FACTOR NFAT;

AGE DISTRIBUTION; AGED; ANIMAL EXPERIMENT; ARTICLE; BONE AGE; BONE CELL; BONE MASS; BONE MINERAL; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; LOW DRUG DOSE; MECHANICAL STIMULATION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PREDICTION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SENESCENCE;

ANIMALIA;

EID: 78049448192     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000924     Document Type: Article

References (69)

1. Rodan GA, Bourret LA, Harvey A, Mensi T (1975) Cyclic AMP and cyclic GMP: mediators of the mechanical effects on bone remodeling. Science 189: 467-469.
2. Rubin C, Turner AS, Bain S, Mallinckrodt C, McLeod K (2001) Anabolism. Low mechanical signals strengthen long bones. Nature 412: 603-604.
3. (2003) Prevention and management of osteoporosis. World Health Organ Tech Rep Ser 921: 1-164.
4. Prince RL, Smith M, Dick IM, Price RI, Webb PG, et al. (1991) Prevention of postmenopausal osteoporosis. A comparative study of exercise, calcium supplementation, and hormone-replacement therapy. N Engl J Med 325: 1189-1195.
5. Pruitt LA, Taaffe DR, Marcus R (1995) Effects of a one-year high-intensity versus low-intensity resistance training program on bone mineral density in older women. J Bone Miner Res 10: 1788-1795.
6. Klein-Nulend J, Sterck JG, Semeins CM, Lips P, Joldersma M, et al. (2002) Donor age and mechanosensitivity of human bone cells. Osteoporos Int 13: 137-146.
7. 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: C1635-1641.
8. Leppanen OV, Sievanen H, Jokihaara J, Pajamaki I, Kannus P, et al. (2008) Pathogenesis of age-related osteoporosis: impaired mechano-responsiveness of bone is not the culprit. PLoS One 3: e2540.
9. Buhl KM, Jacobs CR, Turner RT, Evans GL, Farrell PA, et al. (2001) Aged bone displays an increased responsiveness to low-intensity resistance exercise. J Appl Physiol 90: 1359-1364.
10. Rubin CT, Bain SD, McLeod KJ (1992) Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50: 306-313.
11. Turner CH, Takano Y, Owan I (1995) Aging changes mechanical loading thresholds for bone formation in rats. J Bone Miner Res 10: 1544-1549.
12. Srinivasan S, Agans SC, King KA, Moy NY, Poliachik SL, et al. (2003) Enabling bone formation in the aged skeleton via rest-inserted mechanical loading. Bone 33: 946-955.
13. Pead MJ, Skerry TM, Lanyon LE (1988) Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res 3: 647-656.
14. Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S (1997) Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res 12: 1480-1485.
15. Batra NN, Li YJ, Yellowley CE, You L, Malone AM, et al. (2005) Effects of short-term recovery periods on fluid-induced signaling in osteoblastic cells. J Biomech 38: 1909-1917.
16. Donahue SW, Donahue HJ, Jacobs CR (2003) Osteoblastic cells have refractory periods for fluid-flow-induced intracellular calcium oscillations for short bouts of flow and display multiple low-magnitude oscillations during long-term flow. J Biomech 36: 35-43.
17. Hung CT, Pollack SR, Reilly TM, Brighton CT (1995) Real-time calcium response of cultured bone cells to fluid flow. Clin Orthop. pp 256-269.
18. Chen NX, Ryder KD, Pavalko FM, Turner CH, Burr DB, et al. (2000) Ca(2+) regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am J Physiol Cell Physiol 278: C989-997.
19. You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, et al. (2001) Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J Biol Chem 276: 13365-13371.
20. Huo B, Lu XL, Hung CT, Costa KD, Xu Q, et al. (2008) Fluid flow induced calcium response in bone cell network. Cellular and Molecular Bioengineering 1: 58-66.
21. Taylor AF, Saunders MM, Shingle DL, Cimbala JM, Zhou Z, et al. (2007) Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am J Physiol Cell Physiol 292: C545-552.
22. Schiller PC, D'Ippolito G, Balkan W, Roos BA, Howard GA (2001) Gapjunctional communication is required for the maturation process of osteoblastic cells in culture. Bone 28: 362-369.
23. Tomida T, Hirose K, Takizawa A, Shibasaki F, Iino M (2003) NFAT functions as a working memory of Ca2+ signals in decoding Ca2+ oscillation. Embo J 22: 3825-3832.
24. Timmerman LA, Clipstone NA, Ho SN, Northrop JP, Crabtree GR (1996) Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383: 837-840.
25. Aydemir ABC, Minematsu H, Gardner TR, Kim KO, Ahn JM, et al. (2010) Nuclear factor of activated T cells mediates fluid shear stress- and tensile straininduced Cox2 in human and murine bone cells. Bone 46: 167-175.
26. Riddle RC, Taylor AF, Rogers JR, Donahue HJ (2007) ATP release mediates fluid flow-induced proliferation of human bone marrow stromal cells. J Bone Miner Res 22: 589-600.
27. Ausk BJ, Gross TS, Srinivasan S (2006) An agent based model for real-time signaling induced in osteocytic networks by mechanical stimuli. J Biomech 39: 2638-2646.
28. Gonzalez PP, Cardenas M, Camacho D, Franyuti A, Rosas O, et al. (2003) Cellulat: an agent-based intracellular signalling model. Biosystems 68: 171-185.
29. Peacor SD, Allesina S, Riolo RL, Pascual M (2006) Phenotypic plasticity opposes species invasions by altering fitness surface. PLoS Biol 4: e372.
30. Srinivasan S, Ausk BJ, Poliachik SL, Warner SE, Richardson TS, et al. (2007) Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. J Appl Physiol 102: 1945-1952.
31. Pahlavani MA, Vargas DM (1999) Age-related decline in activation of calcium/ calmodulin-dependent phosphatase calcineurin and kinase CaMK-IV in rat T cells. Mech Ageing Dev 112: 59-74.
32. Pahlavani MA, Harris MD, Richardson A (1995) The age-related decline in the induction of IL-2 transcription is correlated to changes in the transcription factor NFAT. Cell Immunol 165: 84-91.
33. Murphy LL, Hughes CC (2002) Endothelial cells stimulate T cell NFAT nuclear translocation in the presence of cyclosporin A: involvement of the wnt/glycogen synthase kinase-3 beta pathway. J Immunol 169: 3717-3725.
34. Matsuda S, Shibasaki F, Takehana K, Mori H, Nishida E, et al. (2000) Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T-cell activation. EMBO Rep 1: 428-434.
35. Yeo H, Beck LH, McDonald JM, Zayzafoon M (2007) Cyclosporin A elicits dose-dependent biphasic effects on osteoblast differentiation and bone formation. Bone 40: 1502-1516.
36. Pitsillides AA, Rawlinson SC, Suswillo RF, Bourrin S, Zaman G, et al. (1995) Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modeling? Faseb J 9: 1614-1622.
37. Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936.
38. Charras GT, Horton MA (2002) Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophys J 82: 2970-2981.
39. Xia SL, Ferrier J (1992) Propagation of a calcium pulse between osteoblastic cells. Biochem Biophys Res Commun 186: 1212-1219.
40. Hung CT, Allen FD, Pollack SR, Brighton CT (1996) Intracellular Ca2+ stores and extracellular Ca2+ are required in the real-time Ca2+ response of bone cells experiencing fluid flow. J Biomech 29: 1411-1417.
41. Li YX, Keizer J, Stojilkovic SS, Rinzel J (1995) Ca2+ excitability of the ER membrane: an explanation for IP3-induced Ca2+ oscillations. Am J Physiol 269: C1079-1092.
42. Burdakov D, Verkhratsky A (2006) Biophysical re-equilibration of Ca2+ fluxes as a simple biologically plausible explanation for complex intracellular Ca2+ release patterns. FEBS Lett 580: 463-468.
43. Berridge MJ, Bootman MD, Lipp P (1998) Calcium-a life and death signal. Nature 395: 645-648.
44. Veitia RA (2003) A sigmoidal transcriptional response: cooperativity, synergy and dosage effects. Biol Rev Camb Philos Soc 78: 149-170.
45. Kim HD, O'Shea EK (2008) A quantitative model of transcription factoractivated gene expression. Nat Struct Mol Biol 15: 1192-1198.
46. O'Connor JA, Lanyon LE, MacFie H (1982) The influence of strain rate on adaptive bone remodelling. J Biomech 15: 767-781.
47. Hankenson KD, Ausk BJ, Bain SD, Bornstein P, Gross TS, et al. (2006) Mice lacking thrombospondin 2 show an atypical pattern of endocortical and periosteal bone formation in response to mechanical loading. Bone 38: 310-316.
48. Qin YX, Kaplan T, Saldanha A, Rubin C (2003) Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity. J Biomech 36: 1427-1437.
49. Raab-Cullen DM, Akhter MP, Kimmel DB, Recker RR (1994) Bone response to alternate-day mechanical loading of the rat tibia. J Bone Miner Res 9: 203-211.
50. Gomez del Arco P, Martinez-Martinez S, Maldonado JL, Ortega-Perez I, Redondo JM (2000) A role for the p38 MAP kinase pathway in the nuclear shuttling of NFATp. J Biol Chem 275: 13872-13878.
51. Green KN, Demuro A, Akbari Y, Hitt BD, Smith IF, et al. (2008) SERCA pump activity is physiologically regulated by presenilin and regulates amyloid beta production. J Cell Biol 181: 1107-1116.
52. Belmont PJ, Tadimalla A, Chen WJ, Martindale JJ, Thuerauf DJ, et al. (2008) Coordination of growth and endoplasmic reticulum stress signaling by regulator of calcineurin 1 (RCAN1), a novel ATF6-inducible gene. J Biol Chem 283: 14012-14021.
53. Murchison D, Griffith WH (1999) Age-related alterations in caffeine-sensitive calcium stores and mitochondrial buffering in rat basal forebrain. Cell Calcium 25: 439-452.
54. Bergman RJ, Gazit D, Kahn AJ, Gruber H, McDougall S, et al. (1996) Agerelated changes in osteogenic stem cells in mice. J Bone Miner Res 11: 568-577.
55. Vanterpool CK, Pearce WJ, Buchholz JN (2005) Advancing age alters rapid and spontaneous refilling of caffeine-sensitive calcium stores in sympathetic superior cervical ganglion cells. J Appl Physiol 99: 963-971.
56. Dunstan CR, Somers NM, Evans RA (1993) Osteocyte death and hip fracture. Calcif Tissue Int 53: S113-116; discussion S116-117.
57. Movsowitz C, Epstein S, Fallon M, Ismail F, Thomas S (1988) Cyclosporin-A in vivo produces severe osteopenia in the rat: effect of dose and duration of administration. Endocrinology 123: 2571-2577.
58. Orcel P, Bielakoff J, Modrowski D, Miravet L, de Vernejoul MC (1989) Cyclosporin A induces in vivo inhibition of resorption and stimulation of formation in rat bone. J Bone Miner Res 4: 387-391.
59. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. Faseb J 22: 659-661.
60. Bain SD, Impeduglia TM, Rubin CT (1990) Cement line staining in undecalcified thin sections of cortical bone. Stain Technol 65: 159-163.
61. Silbermann M, Weiss A, Reznick AZ, Eilam Y, Szydel N, et al. (1987) Agerelated trend for osteopenia in femurs of female C57BL/6 mice. Compr Gerontol [A] 1: 45-51.
62. Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T (2005) Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 36: 877-883.
63. Marotti G, Ferretti M, Remaggi F, Palumbo C (1995) Quantitative evaluation on osteocyte canalicular density in human secondary osteons. Bone 16: 125-128.
64. 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: 375-380.
65. Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18: 109-113.
66. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610.
67. Zar JH (1996) Biostatistical Analysis. Prentice-Hall, Inc., Upper Saddle River, NJ.
68. Kirkpatrick S, Gelatt CD, Vecchi MP (1983) Optimization by simulated annealing. Science 220: 671-680.
69. Gross TS, Srinivasan S, Liu CC, Clemens TL, Bain SD (2002) Noninvasive loading of the murine tibia: an in vivo model for the study of mechanotransduction. J Bone Miner Res 17: 493-501.