The effect of osteocyte apoptosis on signalling in the osteocyte and bone lining cell network: A computer simulation

Journal of Biomechanics

Volumn 45, Issue 16, 2012, Pages 2876-2883

  Jahani, Masoumeh ^a   Genever, Paul G ^b   Patton, Ronald J ^a   Ahwal, Fadi ^a   Fagan, Michael J ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Apoptosis; Bone lining cells; Mechanotransduction; Osteocytes; Signalling

Indexed keywords

APOPTOTIC; BI-DIRECTIONAL; BIOCHEMICAL SIGNAL; BONE LOSS; BONE MATRIX; BONE REMODELLING; BONE SURFACE; CELL NETWORK; CELL-CELL COMMUNICATIONS; INTERCELLULAR COMMUNICATIONS; MECHANICAL LOADING; MECHANOTRANSDUCTION; OSTEOCYTES; STRAIN LEVELS;

BONE; COMMUNICATION; COMPUTER SIMULATION; LININGS; LOADING; SIGNALING;

CELL DEATH;

CALCIUM;

APOPTOSIS; ARTICLE; BONE CELL; BONE LINING CELL; BONE MATRIX; BONE REMODELING; CALCIUM SIGNALING; CELL ACTIVITY; CELL COMMUNICATION; CELL DENSITY; COMPUTER SIMULATION; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; OSTEOCYTE; OSTEOLYSIS; OSTEOPOROSIS; PRIORITY JOURNAL;

APOPTOSIS; BONE AND BONES; COMPUTER SIMULATION; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; OSTEOCYTES; STRESS, MECHANICAL;

EID: 84868368707     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2012.08.005     Document Type: Article

References (68)

1. Aarden E.M., Burger E.H., Nijweide P.J. Function of osteocytes in bone. Journal of Cellular Biochemistry 1994, 55:287-299.
2. Adachi T., Aonuma Y., Taira K., Hojo M., Kamioka H. Asymmetric intercellular communication between bone cells: propagation of the calcium signalling. Biochemical and Biophysical Research Communications 2009, 389:495-500.
3. Adachi T., Aonuma Y., Tanaka M., Hojo M., Takano-Yamamoto T., Kamioka H. Calcium response in single osteocytes to locally applied mechanical stimulus: differences in cell process and cell body. Journal of Biomechanics 2009, 42:1989-1995.
4. Alford A.I., Jacobs C.R., Donahue H.J. Oscillating fluid flow regulates gap junction communication in osteocytic MLO-Y4 cells by an ERK1/2 MAP kinase-dependent mechanism. Bone 2003, 33:64-70.
5. Almeida M., Han L., Martin-Millan M., Plotkin L.I., Stewart S.A., Roberson P.K., Kousteni S., O'Brien C.A., Bellido T., Parfitt A.M., Weinstein R.S., Jilka R.L., Manolagas S.C. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. Journal of Biological Chemistry 2007, 282:27285-27297.
6. Ausk B.J., Gross T.S., Srinivasan S. An agent based model for real-time signaling induced in osteocytic networks by mechanical stimuli. Journal of Biomechanics 2006, 39:2638-2646.
7. Batra N., Kar R., Jiang J.X. Gap junctions and hemichannels in signal transmission, function and development of bone. Biochimica et Biophysica Acta (BBA) - Biomembranes 2012, 1818:1909-1918.
8. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 1993, 361:315-325.
9. Bonewald L.F. Mechanosensation and Transduction in Osteocytes. BoneKEy Osteovision 2006, 3:7-15.
10. Bonewald L.F. The amazing osteocyte. Journal of Bone and Mineral Research 2011, 26:229-238.
11. Burger E.H., Klein-Nulend J. Mechanotransduction in bone-role of the lacuno-canalicular network. The FASEB Journal 1999, 13:101-112.
12. Burger E.H., Klein-Nulend J. Mechanotransduction in bone-role of the lacuno-canalicular network. The FASEB Journal 1999, 13:S101-112. (Suppl.).
13. Charras G.T., Horton M.A. Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation. Biophysical Journal 2002, 82:2970-2981.
14. Clapham D.E. Replenishing the stores. Nature 1995, 375:634-635.
15. Cowin S.C. Bone poroelasticity. Journal of Biomechanics 1999, 32:217-238.
16. Cowin S.C. Mechanosensation and fluid transport in living bone. Journal of Musculoskeletal and Neuronal Interactions 2002, 2:256-260.
17. Cowin S.C., Moss-Salentijn L., Moss M.L. Candidates for the mechanosensory system in bone. Journal of Biomechanical Engineering 1991, 113:191-197.
18. Cowin S.C., Weinbaum S., Zeng Y. A case for bone canaliculi as the anatomical site of strain generated potentials. Journal of Biomechanics 1995, 28:1281-1297.
19. Damien E., Price J.S., Lanyon L.E. Mechanical strain stimulates osteoblast proliferation through the estrogen receptor in males as well as females. Journal of Bone and Mineral research 2000, 15:2169-2177.
20. Di Palma F., Guignandon A., Chamson A., Lafage-Proust M.-H., Laroche N., Peyroche S., Vico L., Rattner A. Modulation of the responses of human osteoblast-like cells to physiologic mechanical strains by biomaterial surfaces. Biomaterials 2005, 26:4249-4257.
21. Dodd J.S., Raleigh J.A., Gross T.S. Osteocyte hypoxia: a novel mechanotransduction pathway. American Journal of Physiology - Cell Physiology 1999, 277:C598-C602.
22. Donahue H.J. Gap junctions and biophysical regulation of bone cell differentiation. Bone 2000, 26:417-422.
23. Duncan R.L., Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcified Tissue International 1995, 57:344-358.
24. Fermor B., Gundle R., Evans M., Emerton M., Pocock A., Murray D. Primary human osteoblast proliferation and prostaglandin E2 release in response to mechanical strain in vitro. Bone 1998, 22:637-643.
25. Franz-Odendaal T.A., Hall B.K., Witten P.E. Buried alive: how osteoblasts become osteocytes. Developmental Dynamics 2006, 235:176-190.
26. Frost H.M. Bone dynamics in metabolic bone disease. Journal of Bone & Joint Surgery 1966, 48:1203.
27. Gu G., Kurata K., Chen Z., Väänänen K.H. Osteocyte: a cellular basis for mechanotransduction in bone. Journal of Biomechanical Science and Engineering 2007, 2:150-165.
28. Guo X.E., Takai E., Jiang X., Xu Q., Whitesides G.M., Yardley J.T., Hung C.T., Chow E.M., Hantschel T., Costa K.D. Intracellular calcium waves in bone cell networks under single cell nanoindentation. MCB Molecular and Cellular Biomechanics 2006, 3:95-107.
29. Han Y., Cowin S.C., Schaffler M.B., Weinbaum S. Mechanotransduction and strain amplification in osteocyte cell processes. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16689-16694.
30. Harrigan T.P., Hamilton J.J. Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications. Journal of Biomechanics 1993, 26:183-200.
31. Harter L.V., Hruska K.A., Duncan R.L. Human osteoblast-like cells respond to mechanical strain with increased bone matrix protein production independent of hormonal regulation. Endocrinology 1995, 136:528-535.
32. Hedgecock N.L., Hadi T., Chen A.A., Curtiss S.B., Martin R.B., Hazelwood S.J. Quantitative regional associations between remodeling, modeling, and osteocyte apoptosis and density in rabbit tibial midshafts. Bone 2007, 40:627-637.
33. 2+ response of bone cells experiencing fluid flow. Journal of Biomechanics 1996, 29:1411-1417.
34. Huo B.B., Lu X.L., Guo X.E. Intercellular calcium wave propagation in linear and circuit-like bone cell networks. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 2010, 368:617-633.
35. Ishihara Y., Kamioka H., Honjo T., Ueda H., Takano-Yamamoto T., Yamashiro T. Hormonal, pH, and calcium regulation of connexin 43-mediated dye transfer in osteocytes in chick calvaria. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research 2008, 23:350-360.
36. Jessop H.L., Rawlinson S.C., Pitsillides A.A., Lanyon L.E. Mechanical strain and fluid movement both activate extracellular regulated kinase (ERK) in osteoblast-like cells but via different signalling pathways. Bone 2002, 31:186-194.
37. Jilka R.L., Weinstein R.S., Parfitt A.M., Manolagas S.C. Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. Journal of Bone and Mineral Research 2007, 22:1492-1501.
38. Kabbara A.A., Allen D.G. The role of calcium stores in fatigue of isolated single muscle fibres from the cane toad. Journal of Physiology 1999, 519:169-176.
39. Kamioka H., Honjo T., Takano-Yamamoto T. A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 2001, 28:145-149.
40. Kamioka H., Ishihara Y., Ris H., Murshid S.A., Sugawara Y., Takano-Yamamoto T., Lim S.S. Primary cultures of chick osteocytes retain functional gap junctions between osteocytes and between osteocytes and osteoblasts. Microscopy and Microanalysis 2007, 13:108-117.
41. Lewandowska-SzumieŁ M., Sikorski K., Szummer A., Lewandowski Z., Marczyński W. Osteoblast response to the elastic strain of metallic support. Journal of Biomechanics 2007, 40:554-560.
42. Manolagas S.C. Choreography from the tomb: an emerging role of dying osteocytes in the purposeful, and perhaps not so purposeful, targeting of bone remodeling. BoneKEy-Osteovision 2006, 3.
43. Manolagas S.C., Parfitt A.M. What old means to bone. Trends in Endocrinology and Metabolism 2010, 21:369-374.
44. Marotti G. The structure of bone tissues and the cellular control of their deposition. Italian Journal of Anatomy and Embryology 1996, 101:25-79.
45. Martin R.B. Toward a unifying theory of bone remodeling. Bone 2000, 26:1-6.
46. Miller S.C., Saint-Georges L.d., Bowman B.M., Jee W.S. Bone lining cells: structure and function. Scanning Microscopy 1989, 3:953-961.
47. Mullender M.G., Huiskes R., Versleyen H., Buma P. Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species. Journal of Orthopaedic Research 1996, 14:972-979.
48. Nguyen V.H., Lemaire T., Naili S. Influence of interstitial bone microcracks on strain-induced fluid flow. Biomechanics and Modeling in Mechanobiology 2011, 10:963-972.
49. Nicolella D.P., Moravits D.E., Gale A.M., Bonewald L.F., Lankford J. Osteocyte lacunae tissue strain in cortical bone. Journal of Biomechanics 2006, 39:1735-1743.
50. Palumbo C., Palazzini S., Zaffe D., Marotti G. Osteocyte differentiation in the tibia of newborn rabbit: an ultrastructural study of the formation of cytoplasmic processes. Cells, tissues, organs 1990, 137:350-358.
51. Parfitt, A.M., 1990. Bone-forming cells in clinical conditions. In: B.K., Hall (Ed.), Bone, The Osteoblast and Osteocyte, Vol. 1, Telford Press and CRC Press. Boca Raton, FL, pp. 351-429.
52. Plotkin L.I., Mathov I., Aguirre J.I., Parfitt A.M., Manolagas S.C., Bellido T. Mechanical stimulation prevents osteocyte apoptosis: requirement of integrins, Src kinases, and ERKs. American Journal of Physiology Cell Physiology 2005, 289:C633-643.
53. Qiu S., Rao D.S., Palnitkar S., Parfitt A.M. Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. Journal of Bone and Mineral Research 2003, 18:1657-1663.
54. Ransjö M., Sahli J., Lie A. Expression of connexin 43 mRNA in microisolated murine osteoclasts and regulation of bone resorption in vitro by gap junction inhibitors. Biochemical and Biophysical Research Communications 2003, 303:1179-1185.
55. Rochefort G., Pallu S., Benhamou C. Osteocyte: the unrecognized side of bone tissue. Osteoporosis International 2010, 21:1457-1469.
56. Rubin C. Skeletal strain and the functional significance of bone architecture. Calcified tissue international 1984, 36:S11-S18.
57. Seeman E. Osteocytes - martyrs for integrity of bone strength. Osteoporosis International 2006, 17:1443-1448.
58. Tatsumi S., Ishii K., Amizuka N., Li M., Kobayashi T., Kohno K., Ito M., Takeshita S., Ikeda K. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metabolism 2007, 5:464-475.
59. Taylor A.F., Saunders M.M., Shingle D.L., Cimbala J.M., Zhou Z., Donahue H.J. Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. American Journal of Physiology - Cell Physiology 2007, 292:C545-C552.
60. Turner C., Forwood M., Otter M. Mechanotransduction in bone: do bone cells act as sensors of fluid flow?. The FASEB Journal 1994, 8:875-878.
61. Vashishth D., Verborgt O., Divine G., Schaffler M.B., Fyhrie D.P. Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 2000, 26:375-380.
62. Wang Y., McNamara L.M., Schaffler M.B., Weinbaum S. A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15941-15946.
63. Wang Y., McNamara Y.L., Schaffler M.B., Weinbaum S. Strain amplification and intergin based signalling in osteocytes. Journal of Musculoskeletal Neuronal Interactions 2008, 8:332-334.
64. Weinbaum S., Cowin S.C., Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. Journal of Biomechanics 1994, 27:339-360.
65. Weinstein R.S., Manolagas S.C. Apoptosis and osteoporosis. American Journal of Medicine 2000, 108:153-164.
66. Yellowley C.E., Li Z., Zhou Z., Jacobs C.R., Donahue H.J. Functional gap junctions between osteocytic and osteoblastic cells. Journal of Bone and Mineral Research 2000, 15:209-217.
67. You L.D., Temiyasathit S., Lee P.L., Kim C.H., Tummala P., Yao W., Kingery W., Malone A.M., Kwon R.Y., Jacobs C.R. Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone 2008, 42:172-179.
68. Zhang P., Su M., Tanaka S., Yokota H. Knee loading stimulates cortical bone formation in murine femurs. BMC Musculoskeletal Disorders 2006, 7:73.