Gap junctional communication in osteocytes is amplified by low intensity vibrations in vitro

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Uzer, Gunes ^a,b   Pongkitwitoon, Suphannee ^a   Ian, Cheng ^a   Thompson, William R ^b   Rubin, Janet ^b   Chan, Meilin E ^a   Judex, Stefan ^a  

^a St Francis Hospital The Heart Center   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; MESSENGER RNA; PROTEIN KINASE B; CALCEIN; FLUORESCEIN DERIVATIVE;

ARTICLE; CELL COMMUNICATION; CELL NUCLEUS; CONTROLLED STUDY; FINITE ELEMENT ANALYSIS; GAP JUNCTION; OSTEOCYTE; SHEAR STRESS; SIGNAL TRANSDUCTION; VIBRATION; ANIMAL; CELL ADHESION; CELL LINE; CYTOLOGY; METABOLISM; MOUSE; SHEAR STRENGTH;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL LINE; CELL NUCLEUS; FINITE ELEMENT ANALYSIS; FLUORESCEINS; GAP JUNCTIONS; MICE; OSTEOCYTES; PROTO-ONCOGENE PROTEINS C-AKT; SHEAR STRENGTH; SIGNAL TRANSDUCTION; VIBRATION;

EID: 84897566494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090840     Document Type: Article

References (74)

1. Bergoffen J, Scherer S, Wang S, Scott M, Bone L, et al. (1993) Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science 262: 2039-2042. (Pubitemid 24041884)
2. Simon AM, Goodenough DA, Li E, Paul DL (1997) Female infertility in mice lacking connexin 37. Nature 385: 525-529. (Pubitemid 27074669)
3. Kelsell DP, Dunlop J, Stevens HP, Lench NJ, Liang JN, et al. (1997) Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature 387: 80-83. (Pubitemid 27202653)
4. Ilvesaro J, Vaananen K, Tuukkanen J (2000) Bone-resorbing osteoclasts contain gap-junctional connexin-43. Journal of Bone and Mineral Research 15: 919-926. (Pubitemid 30233416)
5. Schirrmacher K, Schmitz I, Winterhager E, Traub O, Brummer F, et al. (1992) Characterization of gap junctions between osteoblast-like cells in culture. Calcified Tissue International 51: 285-290.
6. Civitelli R, Beyer EC, Warlow PM, Robertson AJ, Geist ST, et al. (1993) Connexin43 mediates direct intercellular communication in human osteoblastic cell networks. The Journal of Clinical Investigation 91: 1888-1896. (Pubitemid 23141456)
7. Jones SJ, Gray C, Sakamaki H, Arora M, Boyde A, et al. (1993) The incidence and size of gap junctions between the bone cells in rat calvaria. Anatomy and Embryology 187: 343-352. (Pubitemid 23183694)
8. Kamioka H, Ishihara Y, Ris H, Murshid SA, Sugawara Y, et al. (2007) Primary Cultures of Chick Osteocytes Retain Functional Gap Junctions between Osteocytes and between Osteocytes and Osteoblasts. Microscopy and Microanalysis 13: 108-117. (Pubitemid 46642772)
9. Nomura S, Takano-Yamamoto T (2000) Molecular events caused by mechanical stress in bone. Matrix Biology 19: 91-96. (Pubitemid 30332432)
10. Bacabac RG, Smit TH, Mullender MG, Dijcks SJ, Van Loon JJWA, et al. (2004) Nitric oxide production by bone cells is fluid shear stress rate dependent. Biochemical and Biophysical Research Communications 315: 823-829. (Pubitemid 38249377)
11. Genetos DC, Kephart CJ, Zhang Y, Yellowley CE, Donahue HJ (2007) Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. Journal of Cellular Physiology 212: 207-214. (Pubitemid 46867603)
12. Cherian PP, Siller-Jackson AJ, Gu S, Wang X, Bonewald LF, et al. (2005) Mechanical Strain Opens Connexin 43 Hemichannels in Osteocytes: A Novel Mechanism for the Release of Prostaglandin. Molecular Biology of the Cell 16: 3100-3106. (Pubitemid 40962583)
13. Ajubi NE, Klein-Nulend J, Alblas MJ, Burger EH, Nijweide PJ (1999) Signal transduction pathways involved in fluid flow-induced PGE(2) production by cultured osteocytes. American Journal of Physiology-Endocrinology and Metabolism 276: E171-E178. (Pubitemid 29065607)
14. Li Z, Zhou Z, Yellowley CE, Donahue HJ (1999) Inhibiting gap junctional intercellular communication alters expression of differentiation markers in osteoblastic cells. Bone 25: 661-666. (Pubitemid 29525431)
15. Schiller PC, D'Ippolito G, Balkan W, Roos BA, Howard GA (2001) Gap-junctional communication is required for the maturation process of osteoblastic cells in culture. Bone 28: 362-369. (Pubitemid 32385407)
16. Lloyd SA, Loiselle AE, Zhang Y, Donahue HJ (2013) Shifting Paradigms on the Role of Connexin43 in the Skeletal Response to Mechanical Load. Journal of Bone and Mineral Research: n/a-n/a.
17. Batra N, Kar R, Jiang JX (2012) Gap junctions and hemichannels in signal transmission, function and development of bone. Biochimica et Biophysica Acta (BBA) - Biomembranes 1818: 1909-1918.
18. Jiang JX, Siller-Jackson AJ, Burra S (2007) Roles of gap junctions and hemichannels in bone cell functions and in signal transmission of mechanical stress. Frontiers in Bioscience 12: 1450-1462. (Pubitemid 46850642)
19. Sugawara Y, Ando R, Kamioka H, Ishihara Y, Honjo T, et al. (2011) The Three-Dimensional Morphometry and Cell-Cell Communication of the Osteocyte Network in Chick and Mouse Embryonic Calvaria. Calcified Tissue International 88: 416-424.
20. Saunders MM, You J, Trosko JE, Yamasaki H, Li Z, et al. (2001) Gap junctions and fluid flow response in MC3T3-E1 cells. American Journal of Physiology - Cell Physiology 281: C1917-C1925.
21. Chan M, Lu X, Huo B, Baik A, Chiang V, et al. (2009) A Trabecular Bone Explant Model of Osteocyte-Osteoblast Co-Culture for Bone Mechanobiology. Cellular and Molecular Bioengineering 2: 405-415.
22. Grimston SK, Screen J, Haskell JH, Chung DJ, Brodt MD, et al. (2006) Role of connexin43 in osteoblast response to physical load. In: Zaidi M, editor. Skeletal Development and Remodeling in Health, Disease, and Aging. Oxford: Blackwell Publishing. 214-224. (Pubitemid 43824152)
23. Alford AI, Jacobs CR, Donahue HJ (2003) Oscillating fluid flow regulates gap junction communication in osteocytic MLO-Y4 cells by an ERK1/2 MAP kinase-dependent mechanism. Bone 33: 64-70. (Pubitemid 36952688)
24. Turner CH, Robling AG, Duncan RL, Burr DB (2002) Do Bone Cells Behave Like a Neuronal Network? Calcified Tissue International 70: 435-442. (Pubitemid 36929579)
25. Klein-Nulend J, Nijweide PJ, Burger EH (2003) Osteocyte and bone structure. Curr Osteoporos Rep 1: 5-10.
26. Riddle RC, Donahue HJ (2009) From Streaming Potentials to Shear Stress: 25 Years of Bone Cell Mechanotransduction. Journal of Orthopaedic Research 27: 143-149.
27. Taylor AF, Saunders MM, Shingle DL, Cimbala JM, Zhou Z, et al. (2007) Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. American Journal of Physiology - Cell Physiology 292: C545-C552. (Pubitemid 46115163)
28. Yellowley CE, Li Z, Zhou Z, Jacobs CR, Donahue HJ (2000) Functional Gap Junctions Between Osteocytic and Osteoblastic Cells. Journal of Bone and Mineral Research 15: 209-217. (Pubitemid 30095707)
29. Batra N, Burra S, Siller-Jackson AJ, Gu SM, Xia XC, et al. (2012) Mechanical stress-activated integrin alpha 5 beta 1 induces opening of connexin 43 hemichannels. Proceedings of the National Academy of Sciences of the United States of America 109: 3359-3364.
30. Cheng B, Zhao S, Luo J, Sprague E, Bonewald LF, et al. (2001) Expression of Functional Gap Junctions and Regulation by Fluid Flow in Osteocyte-Like MLO-Y4 Cells. Journal of Bone and Mineral Research 16: 249-259. (Pubitemid 32105406)
31. Ziambaras K, Lecanda F, Steinberg TH, Civitelli R (1998) Cyclic Stretch Enhances Gap Junctional Communication Between Osteoblastic Cells. Journal of Bone and Mineral Research 13: 218-228. (Pubitemid 28082377)
32. Cherian PP, Cheng B, Gu S, Sprague E, Bonewald LF, et al. (2003) Effects of Mechanical Strain on the Function of Gap Junctions in Osteocytes Are Mediated through the Prostaglandin EP2 Receptor. Journal of Biological Chemistry 278: 43146-43156. (Pubitemid 37345933)
33. Xia XC, Batra N, Shi Q, Bonewald LF, Sprague E, et al. (2010) Prostaglandin Promotion of Osteocyte Gap Junction Function through Transcriptional Regulation of Connexin 43 by Glycogen Synthase Kinase 3/beta-Catenin Signaling. Molecular and Cellular Biology 30: 206-219.
34. Watabe H, Furuhama T, Tani-Ishii N, Mikuni-Takagaki Y (2011) Mechanotransduction activates alpha(5)beta(1) integrin and PI3K/Akt signaling pathways in mandibular osteoblasts. Experimental Cell Research 317: 2642-2649.
35. Rangaswami H, Schwappacher R, Tran T, Chan GC, Zhuang S, et al. (2012) Protein Kinase G and Focal Adhesion Kinase Converge on Src/Akt/β-Catenin Signaling Module in Osteoblast Mechanotransduction. Journal of Biological Chemistry 287: 21509-21519.
36. Thompson WR, Guilluy C, Xie Z, Sen B, Brobst KE, et al. (2013) Mechanically Activated Fyn Utilizes mTORC2 to Regulate RhoA and Adipogenesis in Mesenchymal Stem Cells. STEM CELLS 31: 2528-2537.
37. Sen B, Xie Z, Case N, Thompson WR, Uzer G, et al. (2013) mTORC2 regulates mechanically induced cytoskeletal reorganization and lineage selection in marrow derived mesenchymal stem cells. Journal of Bone and Mineral Research: n/a-n/a.
38. Garman R, Gaudette G, Donahue LR, Rubin C, Judex S (2007) Low-level Accelerations applied in the absence of weight bearing can enhance trabecular bone formation. Journal of Orthopaedic Research 25: 732-740. (Pubitemid 46838522)
39. Judex S, Lei X, Han D, Rubin C (2007) Low-magnitude mechanical signals that stimulate bone formation in the ovariectomized rat are dependent on the applied frequency but not on the strain magnitude. Journal of Biomechanics 40: 1333-1339. (Pubitemid 46483448)
40. Ozcivici E, Luu YK, Rubin CT, Judex S (2010) Low-level vibrations retain bone marrow's osteogenic potential and augment recovery of trabecular bone during reambulation. PLoS One 5: e11178.
41. Lau E, Al-Dujaili S, Guenther A, Liu D, Wang L, et al. (2010) Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts. Bone 46: 1508-1515.
42. Sen B, Xie Z, Case N, Styner M, Rubin CT, et al. (2011) Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. Journal of Biomechanics 44: 593-599.
43. Coughlin TR, Niebur GL (2012) Fluid shear stress in trabecular bone marrow due to low-magnitude high-frequency vibration. Journal of Biomechanics 45: 2222-2229.
44. Dickerson DA, Sander EA, Nauman EA (2008) Modeling the mechanical consequences of vibratory loading in the vertebral body: microscale effects. Biomechanics and Modeling in Mechanobiology 7: 191-202. (Pubitemid 351768571)
45. Ozcivici E, Garman R, Judex S (2007) High-frequency oscillatory motions enhance the simulated mechanical properties of non-weight bearing trabecular bone. Journal of Biomechanics 40: 3404-3411. (Pubitemid 47632598)
46. Uzer G, Manske S, Chan M, Chiang F-P, Rubin C, et al. (2012) Separating Fluid Shear Stress from Acceleration during Vibrations In Vitro: Identification of Mechanical Signals Modulating the Cellular Response. Cellular and Molecular Bioengineering 5: 266-276.
47. Bacabac RG, Smit TH, Van Loon JJWA, Doulabi BZ, Helder M, et al. (2006) Bone cell responses to high-frequency vibration stress: does the nucleus oscillate within the cytoplasm? FASEB J 20: 858-864. (Pubitemid 44943944)
48. Uzer G, Pongkitwitoon S, Ete Chan M, Judex S (2013) Vibration induced osteogenic commitment of mesenchymal stem cells is enhanced by cytoskeletal remodeling but not fluid shear. Journal of Biomechanics 46: 2296-2302.
49. Kato Y, Windle JJ, Koop BA,Mundy GR, Bonewald LF (1997) Establishment of an Osteocyte-like Cell Line, MLO-Y4. Journal of Bone and Mineral Research 12: 2014-2023. (Pubitemid 27524478)
50. McGarry JG, Klein-Nulend J, Mullender MG, Prendergast PJ (2004) A comparison of strain and fluid shear stress in stimulating bone cell responses - a computational and experimental study. Faseb Journal 18: 4822+.
51. McGarry JG, Prendergast PJ (2004) A three-dimensional finite element model of an adherent eukaryotic cell. European cells & materials 7: 27-33; discussion 33-24.
52. Verbruggen SW, Vaughan TJ, McNamara LM (2012) Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. Journal of the Royal Society Interface 9: 2735-2744.
53. Darling EM, Topel M, Zauscher S, Vail TP, Guilak F (2008) Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. Journal of Biomechanics 41: 454-464.
54. Dick DAT, Fry DJ, John PN, Rogers AW (1970) Autoradiographic demonstration of inhomogeneous distribution of sodium in single oocytes of Bufo bufo. Journal of Physiology-London 210: 305-&.
55. Gouw TH, Vlugter JC (1966) Physical Properties of Triglycerides. I. Density and Refractive Index. Fette, Seifen, Anstrichmittel 68: 544-549.
56. Heinrich V, Waugh RE (1996) A piconewton force transducer and its application to measurement of the bending stiffness of phospholipid membranes. Annals of Biomedical Engineering 24: 595-605. (Pubitemid 26304923)
57. Guilak F, Tedrow JR, Burgkart R (2000) Viscoelastic Properties of the Cell Nucleus. Biochemical and Biophysical Research Communications 269: 781-786. (Pubitemid 30440377)
58. Sugawara Y, Ando R, Kamioka H, Ishihara Y, Murshid SA, et al. (2008) The alteration of a mechanical property of bone cells during the process of changing from osteoblasts to osteocytes. Bone 43: 19-24.
59. Kato Y, Windle JJ, Koop BA,Mundy GR, Bonewald LF (1997) Establishment of an Osteocyte-like Cell Line, MLO-Y4. Journal of bone and mineral research 12: 2014-2023. (Pubitemid 27524478)
60. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-[Delta][Delta]CT Method. Methods 25: 402-408. (Pubitemid 34164012)
61. You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, et al. (2000) Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. Journal of Biomechanical Engineering-Transactions of the Asme 122: 387-393.
62. Bancroft GN, Sikavitsast VI, van den Dolder J, Sheffield TL, Ambrose CG, et al. (2002) Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteloblasts in a dose-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 99: 12600-12605.
63. Hu SH, Chen JX, Butler JP, Wang N (2005) Prestress mediates force propagation into the nucleus. Biochemical and Biophysical Research Communications 329: 423-428. (Pubitemid 40311763)
64. Klein-Nulend J, van der Plas A, Semeins CM, Ajubi NE, Frangos JA, et al. (1995) Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9: 441-445.
65. Shafrir Y, Forgacs G (2002) Mechanotransduction through the cytoskeleton. American Journal of Physiology-Cell Physiology 282: C479-C486. (Pubitemid 34663163)
66. Ishihara Y, Kamioka H, Honjo T, Ueda H, Takano-Yamamoto T, et al. (2008) Hormonal, pH, and Calcium Regulation of Connexin 43-Mediated Dye Transfer in Osteocytes in Chick Calvaria. Journal of Bone and Mineral Research 23: 350-360. (Pubitemid 351304665)
67. Loiselle AE, Paul EM, Lewis GS, Donahue HJ (2013) Osteoblast and osteocyte-specific loss of Connexin43 results in delayed bone formation and healing during murine fracture healing. Journal of Orthopaedic Research 31: 147-154.
68. Case N, Ma M, Sen B, Xie Z, Gross TS, et al. (2008) β-Catenin Levels Influence Rapid Mechanical Responses in Osteoblasts. Journal of Biological Chemistry 283: 29196-29205.
69. Sen B, Guilluy C, Xie Z, Case N, Styner M, et al. (2011) Mechanically induced focal adhesion assembly amplifies anti-adipogenic pathways in mesenchymal stem cells. Stem Cells 29: 1829-1836.
70. Batra N, Burra S, Siller-Jackson AJ, Gu S, Xia X, et al. (2012) Mechanical stress-activated integrin α5β1 induces opening of connexin 43 hemichannels. Proceedings of the National Academy of Sciences 109: 3359-3364.
71. Ai Z, Fischer A, Spray DC, Brown AMC, Fishman GI (2000) Wnt-1 regulation of connexin43 in cardiac myocytes. The Journal of Clinical Investigation 105: 161-171. (Pubitemid 30054355)
72. Tirkkonen L, Halonen H, Hyttinen J, Kuokkanen H, Sievanen H, et al. (2011) The effects of vibration loading on adipose stem cell number, viability and differentiation towards bone-forming cells. Journal of the Royal Society Interface 8: 1736-1747.
73. Tanaka SM, Li J, Duncan RL, Yokota H, Burr DB, et al. (2003) Effects of broad frequency vibration on cultured osteoblasts. Journal of Biomechanics 36: 73-80. (Pubitemid 35448095)
74. Patel MJ, Chang KH, Sykes MC, Talish R, Rubin C, et al. (2009) Low Magnitude and High Frequency Mechanical Loading Prevents Decreased Bone Formation Responses of 2T3 Preosteoblasts. Journal of Cellular Biochemistry 106: 306-316.