In situ imaging of the autonomous intracellular Ca 2+ oscillations of osteoblasts and osteocytes in bone

Bone

Volumn 50, Issue 4, 2012, Pages 842-852

  Ishihara, Yoshihito ^a   Sugawara, Yasuyo ^a   Kamioka, Hiroshi ^a   Kawanabe, Noriaki ^a   Kurosaka, Hiroshi ^a   Naruse, Keiji ^a   Yamashiro, Takashi ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Gap junction; In situ calcium imaging; Intracellular calcium stores; Osteoblast; Osteocyte

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; CALCIUM ION; OCTANOL; OLEAMIDE; THAPSIGARGIN;

ANIMAL CELL; ARTICLE; BONE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CALVARIA; CELL COMMUNICATION; CHICK; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EX VIVO STUDY; GAP JUNCTION; IMAGING SYSTEM; IN SITU CALCIUM IMAGING; NONHUMAN; OSTEOBLAST; OSTEOCYTE; SCANNING ELECTRON MICROSCOPY;

ANIMALS; BONE AND BONES; CALCIUM SIGNALING; CHICKENS; COLLAGENASES; ENDOPLASMIC RETICULUM; FLUORESCENT DYES; GAP JUNCTIONS; IMAGING, THREE-DIMENSIONAL; INTRACELLULAR SPACE; MICROSCOPY, CONFOCAL; OSTEOBLASTS; OSTEOCYTES; SKULL; TIME-LAPSE IMAGING;

EID: 84857229741     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.01.021     Document Type: Article

References (50)

1. Berridge M.J., Bootman M.D., Lipp P. Calcium-a life and death signal. Nature 1998, 395:645-648.
2. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signaling: dynamics, homeostasis and remodeling. Nat Rev Mol Cell Biol 2003, 4:517-529.
3. Dolmetsch R.E., Xu K., Lewis R.S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998, 392:933-936.
4. 2+ spike frequency can optimize gene expression. Nature 1998, 392:936-941.
5. 2+ oscillations. Science 1998, 279:227-230.
6. Bootman M.D., Collins T.J., Peppiatt C.M., Prothero L.S., MacKenzie L., De Smet P., et al. Calcium signaling - an overview. Cell Dev Biol 2001, 12:3-10.
7. 2+ oscillations in non-excitable cells. Annu Rev Physiol 1993, 55:427-454.
8. Tsai J.A., Larsson O., Kindmark H. Spontaneous and stimulated transients in cytoplasmic free Ca(2+) in normal human osteoblast-like cells: aspects of their regulation. Biochem Biophys Res Commun 1999, 263:206-212.
9. Sun S., Liu Y., Lipsky S., Cho M. Physical manipulation of calcium oscillations facilitates osteodifferentiation of human mesenchymal stem cells. FASEB J 2007, 21:1472-1480.
10. Jorgensen N.R., Geist S.T., Civitelli R., Steinberg T.H. ATP- and gap junction-dependent intercellular calcium signaling in osteoblastic cells. J Cell Biol 1997, 139:497-506.
11. 2+ regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am J Physiol Cell Physiol 2000, 278:C989-C997.
12. Kamioka H., Sugawara Y., Murshid S.A., Ishihara Y., Honjo T., Takano-Yamamoto T. Fluid shear stress induces less calcium response in a single primary osteocyte than in a single osteoblast: implication of different focal adhesion formation. J Bone Miner Res 2006, 21:1012-1021.
13. 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. Am J Physiol Cell Physiol 2007, 292:C545-C552.
14. Kamioka H., Honjo T., Takano-Yamamoto T. The 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.
15. Abbott A. Cell culture: biology's new dimension. Nature 2003, 424:870-872.
16. Wang L., Wang Y., Han Y., Henderson S.C., Majeska R.J., Weinbaum S., et al. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc Natl Acad Sci U S A 2005, 102:11911-11916.
17. Chan M.E., Lu X.L., Huo B., Baik A.D., Chiang V., Guldberg R.E., et al. A trabecular bone explant model of osteocyte-osteoblast co-culture for bone mechanobiology. Cell Mol Bioeng 2009, 2:405-415.
18. Thomas A.P., Bird G.S., Hajnóczky G., Robb-Gaspers L.D., Jr Putney J.W. Spatial and temporal aspects of cellular calcium signaling. FASEB J 1996, 10:1505-1517.
19. Doty S.B. Morphological evidence of gap junctions between bone cells. Calcif Tissue Int 1981, 33:509-512.
20. Cotrina M.L., Lin J.H., Alves-Rodrigues A., Liu S., Li J., Azmi-Ghadimi H., et al. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 1998, 95:15735-15740.
21. Sanderson M.J., Charles A.C., Boitano S., Dirksen E.R. Mechanisms and function of intercellular calcium signaling. Mol Cell Endocrinol 1994, 98:173-187.
22. Goodenough D.A., Goliger J.A., Paul D.L. Connexins, connexons, and intercellular communication. Annu Rev Biochem 1996, 65:475-502.
23. Civitelli R., Beyer E.C., Warlow P.M., Robertson A.J., Geist S.T., Steinberg T.H. Connexin43 mediates direct intercellular communication in human osteoblastic cell networks. J Clin Invest 1993, 91:1888-1896.
24. Donahue H.J., McLeod K.J., Rubin C.T., Andersen J., Grine E.A., Hertzberg E.L., et al. Cell-to-cell communication in osteoblastic networks: cell line-dependent hormonal regulation of gap junction function. J Bone Miner Res 1995, 10:881-889.
25. Yellowley C.E., Li Z., Zhou Z., Jacobs C.R., Donahue H.J. Functional gap junctions between osteocytic and osteoblastic cells. J Bone Miner Res 2000, 15:209-217.
26. Kamioka H., Ishihara Y., Ris H., Murshid S.A., Sugawara Y., Takano-Yamamoto T., et al. Primary cultures of chick osteocytes retain functional gap junctions between osteocytes and between osteocytes and osteoblasts. Microsc Microanal 2007, 13:108-117.
27. 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. J Bone Miner Res 2008, 23:350-360.
28. Schiller P.C., D'Ippolito G., Brambilla R., Roos B.A., Howard G.A. Inhibition of gap-junctional communication induces the trans-differentiation of osteoblasts to an adipocytic phenotype in vitro. J Biol Chem 2001, 276:14133-14138.
29. Li Z., Zhou Z., Saunders M.M., Donahue H.J. Modulation of connexin43 alters expression of osteoblastic differentiation markers. Am J Physiol Cell Physiol 2006, 290:C1248-C1255.
30. Civitelli R. Cell-cell communication in the osteoblast/osteocyte lineage. Arch Biochem Biophys 2008, 473:188-192.
31. Lecanda F., Warlow P.M., Sheikh S., Furlan F., Steinberg T.H., Civitelli R. Connexin43 deficiency causes delayed ossification, craniofacial abnormalities, and osteoblast dysfunction. J Cell Biol 2000, 151:931-943.
32. Sugawara Y., Ando R., Kamioka H., Ishihara Y., Honjo T., Kawanabe N., et al. The three-dimensional morphometry and cell-cell communication of the osteocyte network in chick and mouse embryonic calvaria. Calcif Tissue Int 2011, 88:416-424.
33. Tanaka K., Matsuo T., Ohta M., Sato T., Tezuka K., Nijweide P.J., et al. Time-lapse microcinematography of osteocytes. Miner Electrolyte Metab 1995, 21:189-192.
34. Thastrup O., Cullen P.J., Drøbak B.K., Hanley M.R., Dawson A.P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A 1990, 87:2466-2470.
35. Davidson J.S., Baumgarten I.M. Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharmacol Exp Ther 1988, 246:1104-1107.
36. Ciovacco W.A., Goldberg C.G., Taylor A.F., Lemieux J.M., Horowitz M.C., Donahue H.J., et al. The role of gap junctions in megakaryocyte-mediated osteoblast proliferation and differentiation. Bone 2009, 44:80-86.
37. Boitano S., Evans W.H. Connexin mimetic peptides reversibly inhibit Ca(2+) signaling through gap junctions in airway cells. Am J Physiol Lung Cell Mol Physiol 2000, 279:L623-L630.
38. Jørgensen N.R., Henriksen Z., Brot C., Eriksen E.F., Sørensen O.H., Civitelli R., et al. Human osteoblastic cells propagate intercellular calcium signals by two different mechanisms. J Bone Miner Res 2000, 15:1024-1032.
39. Cravatt B.F., Prospero-Garcia O., Siuzdak G., Gilula N.B., Henriksen S.J., Boger D.L., et al. Chemical characterization of a family of brain lipids that induce sleep. Science 1995, 268:1506-1509.
40. Guan X., Cravatt B.F., Ehring G.R., Hall J.E., Boger D.L., Lerner R.A., et al. The sleep-inducing lipid oleamide deconvolutes gap junction communication and calcium wave transmission in glial cells. J Cell Biol 1997, 139:1785-1792.
41. Finkbeiner S. Calcium waves in astrocytes-filling in the gaps. Neuron 1992, 8:1101-1108.
42. You J., Reilly GC G.C., Zhen X., Yellowley C.E., Chen Q., Donahue H.J., et al. 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 2001, 276:13365-13371.
43. Xia S.L., Ferrier J. Propagation of a calcium pulse between osteoblastic cells. Biochem Biophys Res Commun 1992, 186:1212-1219.
44. Ishii K., Hirose K., Iino M. Ca2+ shuttling between endoplasmic reticulum and mitochondria underlying Ca2+ oscillations. EMBO Rep 2006, 7:390-396.
45. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 2002, 32:235-249.
46. Jørgensen N.R., Teilmann S.C., Henriksen Z., Civitelli R., Sørensen O.H., Steinberg T.H. Activation of L-type calcium channels is required for gap junction-mediated intercellular calcium signaling in osteoblastic cells. J Biol Chem 2003, 278:4082-4086.
47. Rosselló R.A., Wang Z., Kizana E., Krebsbach P.H., Kohn D.H. Connexin 43 as a signaling platform for increasing the volume and spatial distribution of regenerated tissue. Proc Natl Acad Sci U S A 2009, 106:13219-13224.
48. Saunder M.M., You J., Trosko J.E., Yamasaki H., Li Z., Donahue H.J., et al. Gap junctions and fluid flow response in MC3T3-E1 cells. Am J Physiol Cell Physiol 2001, 281:C1917-C1925.
49. Huo B., Lu X.L., Costa K.D., Xu Q., Guo X.E. An ATP-dependent mechanism mediates intercellular calcium signaling in bone cell network under single cell nanoindentation. Cell Calcium 2010, 47:234-241.
50. Henriksen Z., Hiken J.F., Steinberg T.H., Jørgensen N.R. The predominant mechanism of intercellular calcium wave propagation changes during long-term culture of human osteoblast-like cells. Cell Calcium 2006, 39:435-444.