DOI: 10.1091/mbc.9.8.2249. Gap Junctional Communication Modulates Gene Expression in Osteoblastic Cells

Gap Junctional Communication Modulates Gene Expression in Osteoblastic Cells

10.1091/mbc.9.8.2249

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Bone-forming cells are organized in a multicellular network interconnected by gap junctions. In these cells, gap junctions are formed by connexin43 (Cx43) and connexin45 (Cx45). Cx43 gap junctions form pores that are more permeable to negatively charged dyes such as Lucifer yellow and calcein than are Cx45 pores. We studied whether altering gap junctional communication by manipulating the relative expression of Cx43 and Cx45 affects the osteoblast phenotype. Transfection of Cx45 in cells that express primarily Cx43 (ROS 17/2.8 and MC3T3-E1) decreased both dye transfer and expression of osteocalcin (OC) and bone sialoprotein (BSP), genes pivotal to bone matrix formation and calcification. Conversely, transfection of Cx43 into cells that express predominantly Cx45 (UMR 106–01) increased both cell coupling and expression of OC and BSP. Transient cotransfection of promoter–luciferase constructs and connexin expression vectors demonstrated that OC and BSP gene transcription was down-regulated by Cx45 cotransfection in ROS 17/2.8 and MC3T3-E1 cells, in association with a decrease in dye coupling. Conversely, cotransfection of Cx43 in UMR 106–01 cells up-regulated OC and BSP gene transcription. Activity of other less specific osteoblast promoters, such as osteopontin and osteonectin, was less sensitive to changes in gap junctional communication. Thus, altering gap junctional permeability by manipulating the expression of Cx43 and Cx45 in osteoblastic cells alters transcriptional activity of osteoblast-specific promoters, presumably via modulation of signals that can diffuse from cell to cell. A communicating intercellular network is required for the full elaboration of a differentiated osteoblastic phenotype.

Bibliography

Lecanda, F., Towler, D. A., Ziambaras, K., Cheng, S.-L., Koval, M., Steinberg, T. H., & Civitelli, R. (1998). Gap Junctional Communication Modulates Gene Expression in Osteoblastic Cells. Molecular Biology of the Cell, 9(8), 2249â2258.

Authors 7

Fernando Lecanda (first)
Dwight A. Towler (additional)
Konstantinos Ziambaras (additional)
Su-Li Cheng (additional)
Michael Koval (additional)
Thomas H. Steinberg (additional)
Roberto Civitelli (additional)

References 49 Referenced 217

10.1007/BF01868459 / J. Membr. Biol. by Beyer E.C. (1990)
10.1016/S0021-9258(18)92924-8 / J. Biol. Chem. by Beyer E.C. (1991)
10.1074/jbc.271.13.7508 / J. Biol. Chem. by Boudreaux J.M. (1996)
10.1016/0003-2697(76)90527-3 / Anal. Biochem. by Bradford M. (1976)
10.1016/8756-3282(93)90182-A / Bone by Brown M.E.A. (1993)
10.1002/jbmr.5650070816 / J. Bone Miner. Res. by Chen J. (1992)
10.1210/endo.134.1.8275945 / Endocrinology by Cheng S.-L. (1994)
10.1007/BF00299315 / Calcif. Tissue Int. by Cheng S.-L. (1994)
{'key': 'B9', 'first-page': '1054', 'volume': '266', 'author': 'Christ G.J.', 'year': '1996', 'journal-title': 'J. Pharmacol. Exp. Ther.'} / J. Pharmacol. Exp. Ther. by Christ G.J. (1996)
10.1172/JCI116406 / J. Clin. Invest. by Civitelli R. (1993)
10.1002/(SICI)1097-4644(19980101)68:1<8::AID-JCB2>3.0.CO;2-# / J. Cell. Biochem. by Civitelli R. (1998)
10.1038/386855a0 / Nature by Dolmetsh R.E. (1997)
10.1002/jbmr.5650061015 / J. Bone Miner. Res. by Dominguez P. (1991)
10.1007/BF02409482 / Calcif. Tissue Int. by Doty S.B. (1981)
10.1038/sj.onc.1201393 / Oncogene by Duflot-Dancer A. (1997)
10.1007/BF02557679 / Calcif. Tissue Int. by Forrest S.M. (1985)
10.1016/S0021-9258(19)35439-0 / J. Biol. Chem. by Fraser J.D. (1988)
10.1083/jcb.139.2.497 / J. Cell Biol. by Jørgensen N.R. (1997)
10.1161/01.RES.70.2.438 / Circ. Res. by Kanter H.L. (1992)
10.1083/jcb.130.4.987 / J. Cell Biol. by Koval M. (1995)
10.1210/endo-116-1-170 / Endocrinology by Majeska R.J. (1985)
10.1210/endo-107-5-1494 / Endocrinology by Majeska R.J. (1980)
10.1172/JCI117979 / J. Clin. Invest. by Mbalaviele G. (1995)
10.1007/BF00234301 / Anat. Embryol. by Minkoff R. (1994)
10.1172/JCI117813 / J. Clin. Invest. by Munari-Silem Y. (1995)
10.1016/8756-3282(90)90134-K / Bone by Palumbo C. (1990)
10.1172/JCI111096 / J. Clin. Invest. by Parfitt A.M. (1983)
{'key': 'B28', 'first-page': '4308', 'volume': '43', 'author': 'Partridge N.C.', 'year': '1983', 'journal-title': 'Cancer Res.'} / Cancer Res. by Partridge N.C. (1983)
{'key': 'B29', 'first-page': 'E9', 'volume': '255', 'author': 'Reid I.R.', 'year': '1988', 'journal-title': 'Am. J. Physiol.'} / Am. J. Physiol. by Reid I.R. (1988)
10.1016/S0021-9258(19)47201-3 / J. Biol. Chem. by Rodan S.B. (1989)
{'key': 'B31', 'first-page': '163', 'volume': '27', 'author': 'Sáez J.C.', 'year': '1993', 'journal-title': 'Adv. Second Messenger Phosphoprotein Res.'} / Adv. Second Messenger Phosphoprotein Res. by Sáez J.C. (1993)
{'key': 'B32', 'first-page': '1433', 'volume': '6', 'author': 'Schiller P.C.', 'year': '1992', 'journal-title': 'Mol. Endocrinol.'} / Mol. Endocrinol. by Schiller P.C. (1992)
10.1016/S0021-9258(19)81369-8 / J. Biol. Chem. by Shigeno C. (1988)
10.1074/jbc.272.39.24710 / J. Biol. Chem. by Statuto M. (1997)
10.1210/edrv-14-4-424 / Endocr. Rev. by Stein G.S. (1993)
10.1096/fasebj.4.13.2210157 / FASEB J. by Stein G.S. (1990)
10.1002/j.1460-2075.1994.tb06316.x / EMBO J. by Steinberg T.H. (1994)
10.1083/jcb.96.1.191 / J. Cell Biol. by Sudo H. (1983)
10.1002/jbmr.5650101006 / J. Bone Miner. Res. by Tanaka Y. (1995)
10.1210/mend-3-1-36 / Mol. Endocrinol. by Theophan G. (1989)
{'key': 'B41', 'first-page': '614', 'volume': '8', 'author': 'Towler D.A.', 'year': '1994', 'journal-title': 'Mol. Endocrinol.'} / Mol. Endocrinol. by Towler D.A. (1994)
10.1210/endo-125-4-1805 / Endocrinology by Udagawa N. (1989)
10.1074/jbc.271.21.12165 / J. Biol. Chem. by Van der Molen M.A. (1996)
10.1016/8756-3282(88)90111-1 / Bone by Van der Plas A. (1988)
10.1161/01.RES.71.5.1277 / Circ. Res. by Veenstra R.D. (1992)
10.1083/jcb.131.6.1561 / J. Cell Biol. by Vozzi C. (1995)
10.1002/jbmr.5650050806 / J. Bone Miner. Res. by Weinreb M. (1990)
10.1002/jbmr.5650090605 / J. Bone Miner. Res. by Yamaguchi D.T. (1994)
10.1359/jbmr.1998.13.2.218 / J. Bone Miner. Res. by Ziambaras K. (1998)

Dates

Type	When
Created	12 years, 2 months ago (July 2, 2013, 7:14 p.m.)
Deposited	3 years, 6 months ago (Feb. 26, 2022, 9:37 p.m.)
Indexed	1 month ago (July 30, 2025, 8:30 p.m.)
Issued	27 years, 1 month ago (Aug. 1, 1998)
Published	27 years, 1 month ago (Aug. 1, 1998)
Published Print	27 years, 1 month ago (Aug. 1, 1998)

Funders 0

None

BibTeX

@article{Lecanda_1998, title={Gap Junctional Communication Modulates Gene Expression in Osteoblastic Cells}, volume={9}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.9.8.2249}, DOI={10.1091/mbc.9.8.2249}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Lecanda, Fernando and Towler, Dwight A. and Ziambaras, Konstantinos and Cheng, Su-Li and Koval, Michael and Steinberg, Thomas H. and Civitelli, Roberto}, editor={Guidotti, Guido}, year={1998}, month=aug, pages={2249–2258} }

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    {
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      "DOI": "10.1016/S0021-9258(18)92924-8",
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      "author": "Beyer E.C.",
      "year": "1991",
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1074/jbc.271.13.7508",
      "volume": "271",
      "author": "Boudreaux J.M.",
      "year": "1996",
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    {
      "key": "B4",
      "doi-asserted-by": "crossref",
      "first-page": "248",
      "DOI": "10.1016/0003-2697(76)90527-3",
      "volume": "72",
      "author": "Bradford M.",
      "year": "1976",
      "journal-title": "Anal. Biochem."
    },
    {
      "key": "B5",
      "doi-asserted-by": "crossref",
      "first-page": "473",
      "DOI": "10.1016/8756-3282(93)90182-A",
      "volume": "14",
      "author": "Brown M.E.A.",
      "year": "1993",
      "journal-title": "Bone"
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    {
      "key": "B6",
      "doi-asserted-by": "crossref",
      "first-page": "987",
      "DOI": "10.1002/jbmr.5650070816",
      "volume": "7",
      "author": "Chen J.",
      "year": "1992",
      "journal-title": "J. Bone Miner. Res."
    },
    {
      "key": "B7",
      "doi-asserted-by": "crossref",
      "first-page": "277",
      "DOI": "10.1210/endo.134.1.8275945",
      "volume": "134",
      "author": "Cheng S.-L.",
      "year": "1994",
      "journal-title": "Endocrinology"
    },
    {
      "key": "B8",
      "doi-asserted-by": "crossref",
      "first-page": "356",
      "DOI": "10.1007/BF00299315",
      "volume": "55",
      "author": "Cheng S.-L.",
      "year": "1994",
      "journal-title": "Calcif. Tissue Int."
    },
    {
      "key": "B9",
      "first-page": "1054",
      "volume": "266",
      "author": "Christ G.J.",
      "year": "1996",
      "journal-title": "J. Pharmacol. Exp. Ther."
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    {
      "key": "B10",
      "doi-asserted-by": "crossref",
      "first-page": "1888",
      "DOI": "10.1172/JCI116406",
      "volume": "91",
      "author": "Civitelli R.",
      "year": "1993",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B11",
      "doi-asserted-by": "crossref",
      "first-page": "8",
      "DOI": "10.1002/(SICI)1097-4644(19980101)68:1<8::AID-JCB2>3.0.CO;2-#",
      "volume": "68",
      "author": "Civitelli R.",
      "year": "1998",
      "journal-title": "J. Cell. Biochem."
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    {
      "key": "B12",
      "doi-asserted-by": "crossref",
      "first-page": "855",
      "DOI": "10.1038/386855a0",
      "volume": "386",
      "author": "Dolmetsh R.E.",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "B13",
      "doi-asserted-by": "crossref",
      "first-page": "1127",
      "DOI": "10.1002/jbmr.5650061015",
      "volume": "6",
      "author": "Dominguez P.",
      "year": "1991",
      "journal-title": "J. Bone Miner. Res."
    },
    {
      "key": "B14",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1007/BF02409482",
      "volume": "33",
      "author": "Doty S.B.",
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      "journal-title": "Calcif. Tissue Int."
    },
    {
      "key": "B15",
      "doi-asserted-by": "crossref",
      "first-page": "2151",
      "DOI": "10.1038/sj.onc.1201393",
      "volume": "15",
      "author": "Duflot-Dancer A.",
      "year": "1997",
      "journal-title": "Oncogene"
    },
    {
      "key": "B16",
      "doi-asserted-by": "crossref",
      "first-page": "51",
      "DOI": "10.1007/BF02557679",
      "volume": "37",
      "author": "Forrest S.M.",
      "year": "1985",
      "journal-title": "Calcif. Tissue Int."
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    {
      "key": "B17",
      "doi-asserted-by": "crossref",
      "first-page": "911",
      "DOI": "10.1016/S0021-9258(19)35439-0",
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      "author": "Fraser J.D.",
      "year": "1988",
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    {
      "key": "B18",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1083/jcb.139.2.497",
      "volume": "139",
      "author": "J\u00f8rgensen N.R.",
      "year": "1997",
      "journal-title": "J. Cell Biol."
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    {
      "key": "B19",
      "doi-asserted-by": "crossref",
      "first-page": "438",
      "DOI": "10.1161/01.RES.70.2.438",
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      "author": "Kanter H.L.",
      "year": "1992",
      "journal-title": "Circ. Res."
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    {
      "key": "B20",
      "doi-asserted-by": "crossref",
      "first-page": "987",
      "DOI": "10.1083/jcb.130.4.987",
      "volume": "130",
      "author": "Koval M.",
      "year": "1995",
      "journal-title": "J. Cell Biol."
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    {
      "key": "B21",
      "doi-asserted-by": "crossref",
      "first-page": "170",
      "DOI": "10.1210/endo-116-1-170",
      "volume": "116",
      "author": "Majeska R.J.",
      "year": "1985",
      "journal-title": "Endocrinology"
    },
    {
      "key": "B22",
      "doi-asserted-by": "crossref",
      "first-page": "1494",
      "DOI": "10.1210/endo-107-5-1494",
      "volume": "107",
      "author": "Majeska R.J.",
      "year": "1980",
      "journal-title": "Endocrinology"
    },
    {
      "key": "B23",
      "doi-asserted-by": "crossref",
      "first-page": "2757",
      "DOI": "10.1172/JCI117979",
      "volume": "95",
      "author": "Mbalaviele G.",
      "year": "1995",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B24",
      "doi-asserted-by": "crossref",
      "first-page": "231",
      "DOI": "10.1007/BF00234301",
      "volume": "190",
      "author": "Minkoff R.",
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      "journal-title": "Anat. Embryol."
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    {
      "key": "B25",
      "doi-asserted-by": "crossref",
      "first-page": "1429",
      "DOI": "10.1172/JCI117813",
      "volume": "95",
      "author": "Munari-Silem Y.",
      "year": "1995",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B26",
      "doi-asserted-by": "crossref",
      "first-page": "401",
      "DOI": "10.1016/8756-3282(90)90134-K",
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      "author": "Palumbo C.",
      "year": "1990",
      "journal-title": "Bone"
    },
    {
      "key": "B27",
      "doi-asserted-by": "crossref",
      "first-page": "1396",
      "DOI": "10.1172/JCI111096",
      "volume": "72",
      "author": "Parfitt A.M.",
      "year": "1983",
      "journal-title": "J. Clin. Invest."
    },
    {
      "key": "B28",
      "first-page": "4308",
      "volume": "43",
      "author": "Partridge N.C.",
      "year": "1983",
      "journal-title": "Cancer Res."
    },
    {
      "key": "B29",
      "first-page": "E9",
      "volume": "255",
      "author": "Reid I.R.",
      "year": "1988",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "B30",
      "doi-asserted-by": "crossref",
      "first-page": "19934",
      "DOI": "10.1016/S0021-9258(19)47201-3",
      "volume": "264",
      "author": "Rodan S.B.",
      "year": "1989",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B31",
      "first-page": "163",
      "volume": "27",
      "author": "S\u00e1ez J.C.",
      "year": "1993",
      "journal-title": "Adv. Second Messenger Phosphoprotein Res."
    },
    {
      "key": "B32",
      "first-page": "1433",
      "volume": "6",
      "author": "Schiller P.C.",
      "year": "1992",
      "journal-title": "Mol. Endocrinol."
    },
    {
      "key": "B33",
      "doi-asserted-by": "crossref",
      "first-page": "18369",
      "DOI": "10.1016/S0021-9258(19)81369-8",
      "volume": "263",
      "author": "Shigeno C.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B34",
      "doi-asserted-by": "crossref",
      "first-page": "24710",
      "DOI": "10.1074/jbc.272.39.24710",
      "volume": "272",
      "author": "Statuto M.",
      "year": "1997",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "B35",
      "doi-asserted-by": "crossref",
      "first-page": "424",
      "DOI": "10.1210/edrv-14-4-424",
      "volume": "14",
      "author": "Stein G.S.",
      "year": "1993",
      "journal-title": "Endocr. Rev."
    },
    {
      "key": "B36",
      "doi-asserted-by": "crossref",
      "first-page": "3111",
      "DOI": "10.1096/fasebj.4.13.2210157",
      "volume": "4",
      "author": "Stein G.S.",
      "year": "1990",
      "journal-title": "FASEB J."
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