DOI: 10.1002/jbmr.5650100609. Cell-to-cell communication in osteoblastic networks: Cell line–dependent hormonal regulation of gap junction function

Cell-to-cell communication in osteoblastic networks: Cell line–dependent hormonal regulation of gap junction function

10.1002/jbmr.5650100609

Crossref journal-article

Oxford University Press (OUP)

Journal of Bone and Mineral Research (286)

Abstract

Abstract We have characterized the distribution, expression, and hormonal regulation of gap junctions in primary cultures of rat osteoblast-like cells (ROBs), and three osteosarcoma cell lines, ROS 17/2.8, UMR-106, and SAOS-2, and a continuous osteoblastic cell line, MC3T3-E1. All cell lines we examined were functionally coupled. ROS 17/2.8 were the more strongly coupled, while ROB and MC3T3-E1 were moderately coupled and UMR-106 and SAOS-2 were weakly coupled. Exposure to parathyroid hormone (PTH) for 1 h increased functional coupling in ROB cells in a concentration-dependent manner. Furthermore, PTH (3–34), an analog of PTH with binds to the PTH receptor and thus attenuates PTH-stimulated cAMP accumulation, also attenuated PTH-stimulated functional coupling in ROB. This suggests that PTH increases functional coupling partly through a cAMP-dependent mechanism. A 1 h exposure to PTH did not affect coupling in ROS 17/2.8, UMR-106, MC3T3-E1, or SAOS-2. To examine whether connexin43 (Cx43), a specific gap junction protein, is present in functionally coupled osteoblastic cells, we characterized Cx43 distribution and expression. Indirect immunofluorescence with antibodies to Cx43 revealed that ROS 17/2.8, ROB, and to a lesser extent MC3T3-E1 and UMR-106, expressed Cx43 immunoreactivity. SAOS-2 showed little if any Cx43 immunoreactivity. Cx43 mRNA and Cx43 protein were detected by Northern blot analysis and immunoblot analysis, respectively, in all cell lines examined, including SAOS-2. Our findings suggest that acute exposure to PTH regulates gap junction coupling, in a cell-line dependent manner, in osteoblastic cells. Furthermore, Cx43 is expressed in osteoblastic cells regardless of the degree to which the cells are functionally coupled or the degree to which coupling is regulated by PTH.

Bibliography

Dr. Donahue, H. J., Mcleod, K. J., Rubin, C. T., Andersen, J., Grine, E. A., Hertzberg, E. L., & Brink, P. R. (1995). Cell-to-cell communication in osteoblastic networks: Cell lineâdependent hormonal regulation of gap junction function. Journal of Bone and Mineral Research, 10(6), 881â889.

Authors 7

Henry J. Dr. Donahue (first)
K.J. Mcleod (additional)
C.T. Rubin (additional)
J. Andersen (additional)
E.A. Grine (additional)
E.L. Hertzberg (additional)
P.R. Brink (additional)

References 46 Referenced 143

10.1007/BF02409482 / Calcif Tissue Int / Morphological evidence of gap junctions between bone cells. by Doty (1981)
10.1083/jcb.109.6.3391 / J Cell Biol / Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. by Zhang (1989)
10.1083/jcb.103.1.123 / J Cell Biol / Molecular cloning of cDNA for rat liver gap junction protein. by Paul (1986)
10.1083/jcb.105.6.2621 / J Cell Biol / Connexin 43: A protein from rat heart homologous to a gap junction protein from liver. by Beyer (1987)
10.1083/jcb.108.2.595 / J Cell Biol / Antisera directed against connexin 43 peptides react with a 43 kDa protein localized to gap junctions in myocardium and other tissues. by Beyer (1989)
10.1016/0896-6273(91)90241-Q / Neuron / Gap junctions: New tools, new answers, new questions. by Bennett (1991)
10.1007/BF00334489 / Calcif Tissue Int / Characterization of gap junctions between osteoblast-like cells in culture. by Schirrmacher (1992)
{'issue': '9', 'key': '2024013114230214800_bib8', 'first-page': '1433', 'article-title': 'Hormonal regulation of intercellular communication: Parathyroid hormone increases connexin 43 gene expression and gap junctional communication in osteoblastic cells.', 'volume': '6', 'author': 'Schiller', 'year': '1992', 'journal-title': 'Mol Endocrinol'} / Mol Endocrinol / Hormonal regulation of intercellular communication: Parathyroid hormone increases connexin 43 gene expression and gap junctional communication in osteoblastic cells. by Schiller (1992)
10.1172/JCI116406 / J Clin Invest / Connexin43 mediates direct intercellular communication in human osteoblastic cell networks. by Civitelli (1993)
10.1007/BF01352015 / Calcif Tissue Int / Dye and electric coupling between osteoblast-like cells in culture. by Schirrmacher (1993)
10.1002/j.1460-2075.1994.tb06316.x / EMBO J / Connexin43 and connexin45 form gap junctions with different molecular permeabilities in osteoblastic cells. by Steinberg (1994)
10.1002/jbmr.5650010302 / J Bone Miner Res / Prostaglandins change cell shape and increase intercellular gap junctions in osteoblasts cultured from rat fetal calvaria. by Shen (1986)
10.1016/8756-3282(90)90134-K / Bone / Morphological study of intercellular junctions during osteocyte differentiation. by Palumbo (1990)
10.2106/00004623-198870070-00016 / J Bone Joint Surg / Cortical bone repair: The relationship of the lacunar-canalicular system and intercellular gap junctions to the repair process. by Shapiro (1988)
10.1210/endo-128-6-3299 / Endocrinology / Hormonal control of cell to-cell communication: Regulation by thyrotropin of the gap junction-mediated dye transfer between thyroid cells. by Munari-Silem (1991)
10.1210/edrv-11-2-302 / Endocrine Rev / The hormone-induced regulation of contact-dependent cell-cell communication by phosphorylation. by Stagg (1990)
{'key': '2024013114230214800_bib17', 'first-page': '245', 'article-title': 'Cyclic nucleotides and junctional permeability.', 'volume': '7', 'author': 'DeMello', 'year': '1988', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Cyclic nucleotides and junctional permeability. by DeMello (1988)
10.1073/pnas.84.20.7319 / Proc Natl Acad Sci USA / Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. by Lasater (1987)
10.1073/pnas.86.19.7639 / Proc Natl Acad Sci USA / Horizontal cell gap junctions: Single channel conductance and modulation by dopamine. by McMahon (1989)
{'issue': 'S1', 'key': '2024013114230214800_bib20', 'first-page': '672', 'article-title': 'Cell coupling through functional gap junctions in normal bone cell networks.', 'volume': '6', 'author': 'Civitelli', 'year': '1991', 'journal-title': 'J Bone Miner Res'} / J Bone Miner Res / Cell coupling through functional gap junctions in normal bone cell networks. by Civitelli (1991)
10.1210/endo-123-5-2600 / Endocrinology / Osteoblastic cells are involved in osteoclast formation. by Takahashi (1988)
10.1016/8756-3282(88)90109-3 / Bone / Different roles for calcium and cyclic AMP in the action of PTH: Studies in bone explants and isolated bone cells. by Herrmann-Erlee (1988)
{'key': '2024013114230214800_bib23', 'first-page': 'E708', 'article-title': 'Adenylate cyclase blockers dissociate PTH-stimulated bone resorption from cAMP production.', 'volume': '258', 'author': 'Reid', 'year': '1990', 'journal-title': 'Am J Physiol'} / Am J Physiol / Adenylate cyclase blockers dissociate PTH-stimulated bone resorption from cAMP production. by Reid (1990)
10.1016/S0021-9258(18)68273-0 / J Biol Chem / Differential effects of parathyroid hormone and its analogues on cytosolic calcium ion and cAMP levels in cultured rat osteoblast-like cells. by Donahue (1988)
10.1210/endo-126-3-1471 / Endocrinology / Structure-function relationships for full-length recombinant parathyroid hormone-related peptide and its amino-terminal fragments: effects on cytosolic calcium ion mobilization and adenylate cyclase activation in rat osteoblast-like cells. by Donahue (1990)
{'issue': '1', 'key': '2024013114230214800_bib26', 'first-page': '69', 'article-title': 'Gap junctions: biochemical properties and functional regulation under physiological and toxicological conditions.', 'volume': '3', 'author': 'Saez', 'year': '1990', 'journal-title': 'In Vitro Toxicol'} / In Vitro Toxicol / Gap junctions: biochemical properties and functional regulation under physiological and toxicological conditions. by Saez (1990)
10.1016/0006-8993(90)90415-8 / Brain Res / LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain. by Yamamoto (1990)
10.1002/cne.903020414 / J Comp Neurol / On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. by Yamamoto (1990)
10.1002/jbmr.5650071111 / J Bone Miner Res / Altered regulation of cytoplasmic calcium concentration in tetracycline treated osteoclasts. by Donahue (1992)
10.1002/jbmr.5650081003 / J Bone Miner Res / Regulation of cytokine expression in osteoblasts by parathyroid hormone: rapid stimulation of interleukin-6 and leukemia inhibiting factor mRNA. by Greenfield (1993)
10.1016/S0021-9258(18)54209-5 / J Biol Chem / Connexin 56, A novel lens gap junction protein: Molecular cloning and functional expression. by Rup (1993)
10.1016/0003-2697(87)90021-2 / Anal Biochem / Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. by Chomczynski (1987)
10.1021/bi00491a020 / Biochemistry / micF RNA binds to the 5′ end of ompF mRNA and to a protein from escherichia coli. by Andersen (1990)
10.1083/jcb.111.2.589 / J Cell Biol / Molecular characterization and functional expression of the human cardiac gap junction channel. by Fishman (1990)
10.1161/01.RES.73.1.71 / Circ Res / Connexin expression in the developing avian cardiovascular system. by Minkoff (1993)
10.1242/dev.111.2.509 / Development / Analysis of distribution patterns of gap junctions during development of embryonic chick facial primordia. by Minkoff (1991)
{'year': '1994', 'author': 'Minkoff', 'key': '2024013114230214800_bib37'} by Minkoff (1994)
{'key': '2024013114230214800_bib38', 'article-title': 'Biological Science Series', 'volume-title': 'Biostatistical Analysis', 'author': 'Zar', 'year': '1974'} / Biostatistical Analysis / Biological Science Series by Zar (1974)
10.1007/BF01868674 / J Membr Biol / Expression of the gap junction protein connexin43 in embryonic chick lens: molecular cloning, ultrastructural localization, biosynthesis, and post-translational phosphorylation. by Musil (1990)
10.1016/S0021-9258(18)38149-3 / J Biol Chem / Molecular cloning and characterization of a new member of the gap junction gene family, connexin-31. by Hoh (1991)
10.1016/0092-8674(89)90180-3 / Cell / Formation of gap junctions by expression of connexins in xenopus oocyte pairs. by Swenson (1989)
10.1177/00220345790580042101 / J Dent Res / Cell-to-cell communication of osteoblasts. by Jeansonne (1979)
10.1016/S0021-9258(18)47626-0 / J Biol Chem / Parathyroid hormone-activated calcium channels in an osteoblast-like clonal osteosarcoma cell line. by Yamaguchi (1987)
{'key': '2024013114230214800_bib44', 'first-page': 'E45', 'article-title': 'Parathyroid hormone acutely elevates intracellular calcium in osteoblast-like cells.', 'volume': '252', 'author': 'Reid', 'year': '1987', 'journal-title': 'Am J Physiol'} / Am J Physiol / Parathyroid hormone acutely elevates intracellular calcium in osteoblast-like cells. by Reid (1987)
{'key': '2024013114230214800_bib45', 'first-page': 'E9', 'article-title': 'Parathyroid hormone depresses cytosolic pH and DNA synthesis in osteoblast-like cells.', 'volume': '255', 'author': 'Reid', 'year': '1988', 'journal-title': 'Am J Physiol'} / Am J Physiol / Parathyroid hormone depresses cytosolic pH and DNA synthesis in osteoblast-like cells. by Reid (1988)
10.1002/jcp.1041520105 / J Cell Physiol / Second messenger signaling in the regulation of cytosolic pH and DNA synthesis by parathyroid hormone (PTH) and PTH-related peptide in osteoblastic osteosarcoma cells: Role of Na+/H+ exchange. by Sugimoto (1992)

Dates

Type	When
Created	15 years, 6 months ago (Feb. 3, 2010, 11:08 a.m.)
Deposited	1 year, 5 months ago (March 13, 2024, 11 a.m.)
Indexed	3 months, 2 weeks ago (May 19, 2025, 8:08 a.m.)
Issued	30 years, 3 months ago (June 1, 1995)
Published	30 years, 3 months ago (June 1, 1995)
Published Online	30 years, 3 months ago (June 1, 1995)
Published Print	30 years, 3 months ago (June 1, 1995)

Funders 3

NIH
Awards3
1. AG10199 (HJD)
2. GM30667 (ELH)
3. HL31299 (PRB)
American Federation for Aging Research 10.13039/100000965
Region: Americas
gov (Trusts, charities, foundations (both public and private))
Labels2
1. American Federation for Aging Research, Inc.
2. AFAR
Electric Power Research Institute 10.13039/100008421
Region: Americas
pri (Other non-profit organizations)
Labels1
1. EPRI
Awards1
1. RFP 2965–21 (KJM)

BibTeX

@article{Dr_Donahue_1995, title={Cell-to-cell communication in osteoblastic networks: Cell line–dependent hormonal regulation of gap junction function}, volume={10}, ISSN={1523-4681}, url={http://dx.doi.org/10.1002/jbmr.5650100609}, DOI={10.1002/jbmr.5650100609}, number={6}, journal={Journal of Bone and Mineral Research}, publisher={Oxford University Press (OUP)}, author={Dr. Donahue, Henry J. and Mcleod, K.J. and Rubin, C.T. and Andersen, J. and Grine, E.A. and Hertzberg, E.L. and Brink, P.R.}, year={1995}, month=jun, pages={881–889} }

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    {
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      "article-title": "Antisera directed against connexin 43 peptides react with a 43 kDa protein localized to gap junctions in myocardium and other tissues.",
      "volume": "108",
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      "first-page": "285",
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      "author": "Schirrmacher",
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      "author": "Shapiro",
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      "first-page": "302",
      "DOI": "10.1210/edrv-11-2-302",
      "article-title": "The hormone-induced regulation of contact-dependent cell-cell communication by phosphorylation.",
      "volume": "11",
      "author": "Stagg",
      "year": "1990",
      "journal-title": "Endocrine Rev"
    },
    {
      "key": "2024013114230214800_bib17",
      "first-page": "245",
      "article-title": "Cyclic nucleotides and junctional permeability.",
      "volume": "7",
      "author": "DeMello",
      "year": "1988",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "2024013114230214800_bib18",
      "doi-asserted-by": "crossref",
      "first-page": "7319",
      "DOI": "10.1073/pnas.84.20.7319",
      "article-title": "Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase.",
      "volume": "84",
      "author": "Lasater",
      "year": "1987",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2024013114230214800_bib19",
      "doi-asserted-by": "crossref",
      "first-page": "7639",
      "DOI": "10.1073/pnas.86.19.7639",
      "article-title": "Horizontal cell gap junctions: Single channel conductance and modulation by dopamine.",
      "volume": "86",
      "author": "McMahon",
      "year": "1989",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "issue": "S1",
      "key": "2024013114230214800_bib20",
      "first-page": "672",
      "article-title": "Cell coupling through functional gap junctions in normal bone cell networks.",
      "volume": "6",
      "author": "Civitelli",
      "year": "1991",
      "journal-title": "J Bone Miner Res"
    },
    {
      "key": "2024013114230214800_bib21",
      "doi-asserted-by": "crossref",
      "first-page": "2600",
      "DOI": "10.1210/endo-123-5-2600",
      "article-title": "Osteoblastic cells are involved in osteoclast formation.",
      "volume": "123",
      "author": "Takahashi",
      "year": "1988",
      "journal-title": "Endocrinology"
    },
    {
      "key": "2024013114230214800_bib22",
      "doi-asserted-by": "crossref",
      "first-page": "93",
      "DOI": "10.1016/8756-3282(88)90109-3",
      "article-title": "Different roles for calcium and cyclic AMP in the action of PTH: Studies in bone explants and isolated bone cells.",
      "volume": "9",
      "author": "Herrmann-Erlee",
      "year": "1988",
      "journal-title": "Bone"
    },
    {
      "key": "2024013114230214800_bib23",
      "first-page": "E708",
      "article-title": "Adenylate cyclase blockers dissociate PTH-stimulated bone resorption from cAMP production.",
      "volume": "258",
      "author": "Reid",
      "year": "1990",
      "journal-title": "Am J Physiol"
    },
    {
      "key": "2024013114230214800_bib24",
      "doi-asserted-by": "crossref",
      "first-page": "13522",
      "DOI": "10.1016/S0021-9258(18)68273-0",
      "article-title": "Differential effects of parathyroid hormone and its analogues on cytosolic calcium ion and cAMP levels in cultured rat osteoblast-like cells.",
      "volume": "262",
      "author": "Donahue",
      "year": "1988",
      "journal-title": "J Biol Chem"
    },
    {
      "issue": "3",
      "key": "2024013114230214800_bib25",
      "doi-asserted-by": "crossref",
      "first-page": "1471",
      "DOI": "10.1210/endo-126-3-1471",
      "article-title": "Structure-function relationships for full-length recombinant parathyroid hormone-related peptide and its amino-terminal fragments: effects on cytosolic calcium ion mobilization and adenylate cyclase activation in rat osteoblast-like cells.",
      "volume": "126",
      "author": "Donahue",
      "year": "1990",
      "journal-title": "Endocrinology"
    },
    {
      "issue": "1",
      "key": "2024013114230214800_bib26",
      "first-page": "69",
      "article-title": "Gap junctions: biochemical properties and functional regulation under physiological and toxicological conditions.",
      "volume": "3",
      "author": "Saez",
      "year": "1990",
      "journal-title": "In Vitro Toxicol"
    },
    {
      "key": "2024013114230214800_bib27",
      "doi-asserted-by": "crossref",
      "first-page": "313",
      "DOI": "10.1016/0006-8993(90)90415-8",
      "article-title": "LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain.",
      "volume": "508",
      "author": "Yamamoto",
      "year": "1990",
      "journal-title": "Brain Res"
    },
    {
      "key": "2024013114230214800_bib28",
      "doi-asserted-by": "crossref",
      "first-page": "853",
      "DOI": "10.1002/cne.903020414",
      "article-title": "On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression.",
      "volume": "302",
      "author": "Yamamoto",
      "year": "1990",
      "journal-title": "J Comp Neurol"
    },
    {
      "key": "2024013114230214800_bib29",
      "doi-asserted-by": "crossref",
      "first-page": "1313",
      "DOI": "10.1002/jbmr.5650071111",
      "article-title": "Altered regulation of cytoplasmic calcium concentration in tetracycline treated osteoclasts.",
      "volume": "7",
      "author": "Donahue",
      "year": "1992",
      "journal-title": "J Bone Miner Res"
    },
    {
      "key": "2024013114230214800_bib30",
      "doi-asserted-by": "crossref",
      "first-page": "1163",
      "DOI": "10.1002/jbmr.5650081003",
      "article-title": "Regulation of cytokine expression in osteoblasts by parathyroid hormone: rapid stimulation of interleukin-6 and leukemia inhibiting factor mRNA.",
      "volume": "8",
      "author": "Greenfield",
      "year": "1993",
      "journal-title": "J Bone Miner Res"
    },
    {
      "key": "2024013114230214800_bib31",
      "doi-asserted-by": "crossref",
      "first-page": "706",
      "DOI": "10.1016/S0021-9258(18)54209-5",
      "article-title": "Connexin 56, A novel lens gap junction protein: Molecular cloning and functional expression.",
      "volume": "268",
      "author": "Rup",
      "year": "1993",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2024013114230214800_bib32",
      "doi-asserted-by": "crossref",
      "first-page": "156",
      "DOI": "10.1016/0003-2697(87)90021-2",
      "article-title": "Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.",
      "volume": "162",
      "author": "Chomczynski",
      "year": "1987",
      "journal-title": "Anal Biochem"
    },
    {
      "key": "2024013114230214800_bib33",
      "doi-asserted-by": "crossref",
      "first-page": "9249",
      "DOI": "10.1021/bi00491a020",
      "article-title": "micF RNA binds to the 5\u2032 end of ompF mRNA and to a protein from escherichia coli.",
      "volume": "29",
      "author": "Andersen",
      "year": "1990",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2024013114230214800_bib34",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1083/jcb.111.2.589",
      "article-title": "Molecular characterization and functional expression of the human cardiac gap junction channel.",
      "volume": "111",
      "author": "Fishman",
      "year": "1990",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2024013114230214800_bib35",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1161/01.RES.73.1.71",
      "article-title": "Connexin expression in the developing avian cardiovascular system.",
      "volume": "73",
      "author": "Minkoff",
      "year": "1993",
      "journal-title": "Circ Res"
    },
    {
      "key": "2024013114230214800_bib36",
      "doi-asserted-by": "crossref",
      "first-page": "509",
      "DOI": "10.1242/dev.111.2.509",
      "article-title": "Analysis of distribution patterns of gap junctions during development of embryonic chick facial primordia.",
      "volume": "111",
      "author": "Minkoff",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "year": "1994",
      "author": "Minkoff",
      "key": "2024013114230214800_bib37"
    },
    {
      "key": "2024013114230214800_bib38",
      "article-title": "Biological Science Series",
      "volume-title": "Biostatistical Analysis",
      "author": "Zar",
      "year": "1974"
    },
    {
      "key": "2024013114230214800_bib39",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1007/BF01868674",
      "article-title": "Expression of the gap junction protein connexin43 in embryonic chick lens: molecular cloning, ultrastructural localization, biosynthesis, and post-translational phosphorylation.",
      "volume": "116",
      "author": "Musil",
      "year": "1990",
      "journal-title": "J Membr Biol"
    },
    {
      "issue": "10",
      "key": "2024013114230214800_bib40",
      "doi-asserted-by": "crossref",
      "first-page": "6524",
      "DOI": "10.1016/S0021-9258(18)38149-3",
      "article-title": "Molecular cloning and characterization of a new member of the gap junction gene family, connexin-31.",
      "volume": "266",
      "author": "Hoh",
      "year": "1991",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2024013114230214800_bib41",
      "doi-asserted-by": "crossref",
      "first-page": "145",
      "DOI": "10.1016/0092-8674(89)90180-3",
      "article-title": "Formation of gap junctions by expression of connexins in xenopus oocyte pairs.",
      "volume": "57",
      "author": "Swenson",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "issue": "4",
      "key": "2024013114230214800_bib42",
      "doi-asserted-by": "crossref",
      "first-page": "1415",
      "DOI": "10.1177/00220345790580042101",
      "article-title": "Cell-to-cell communication of osteoblasts.",
      "volume": "58",
      "author": "Jeansonne",
      "year": "1979",
      "journal-title": "J Dent Res"
    },
    {
      "key": "2024013114230214800_bib43",
      "doi-asserted-by": "crossref",
      "first-page": "7711",
      "DOI": "10.1016/S0021-9258(18)47626-0",
      "article-title": "Parathyroid hormone-activated calcium channels in an osteoblast-like clonal osteosarcoma cell line.",
      "volume": "262",
      "author": "Yamaguchi",
      "year": "1987",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2024013114230214800_bib44",
      "first-page": "E45",
      "article-title": "Parathyroid hormone acutely elevates intracellular calcium in osteoblast-like cells.",
      "volume": "252",
      "author": "Reid",
      "year": "1987",
      "journal-title": "Am J Physiol"
    },
    {
      "key": "2024013114230214800_bib45",
      "first-page": "E9",
      "article-title": "Parathyroid hormone depresses cytosolic pH and DNA synthesis in osteoblast-like cells.",
      "volume": "255",
      "author": "Reid",
      "year": "1988",
      "journal-title": "Am J Physiol"
    },
    {
      "key": "2024013114230214800_bib46",
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      "first-page": "28",
      "DOI": "10.1002/jcp.1041520105",
      "article-title": "Second messenger signaling in the regulation of cytosolic pH and DNA synthesis by parathyroid hormone (PTH) and PTH-related peptide in osteoblastic osteosarcoma cells: Role of Na+/H+ exchange.",
      "volume": "152",
      "author": "Sugimoto",
      "year": "1992",
      "journal-title": "J Cell Physiol"
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