{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,9,26]],"date-time":"2025-09-26T16:57:43Z","timestamp":1758905863571,"version":"3.37.3"},"reference-count":61,"publisher":"Oxford University Press (OUP)","issue":"7","license":[{"start":{"date-parts":[[1994,7,1]],"date-time":"1994-07-01T00:00:00Z","timestamp":773020800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100001742","name":"United States-Israel Binational Science Foundation","doi-asserted-by":"crossref","award":["(BSF 89-482)"],"award-info":[{"award-number":["(BSF 89-482)"]}],"id":[{"id":"10.13039\/501100001742","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Basic Research Foundation of The Israel Academy of Science and Humanities","award":["(88-531)"],"award-info":[{"award-number":["(88-531)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[1994,7,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>This study was aimed at elucidating the relationship between osteogenic activity of marrow stromal cells and their ability to support hematopoiesis followed by the bone-remodeling process. We used the MBA-15 cell line, which expresses osteoblastic phenotype in vitro and forms bone in diffusion chamber. We have compared bone formation and hematopoietic responses elicited in vivo by these cells with the implantation of freshly isolated bone marrow cells (BMC) or demineralized tooth matrix (DTM). Both MBA-15 cells and BMC, implanted under the kidney capsule, yielded intramembraneous bone, but DTM, implanted subcutaneously, elicited endochondral bone. MBA-15 formed primary bone, mimicking only the initial sequential stages of the ossification process. Neither histologic signs of bone resorption and remodeling nor tartrate-resistant acid phosphatase (TRAP)-positive cells and marrow formation were observed. Bone formation was monitored biochemically. Functions for hematopoietic stem and committed cell content were measured by GM-CFU and BFU-E assays that confirmed the morphologic observations. In both BMC and DTM implantation, bone formation was followed by hematopoietic activity, osteoclastogenesis, and remodeling. We conclude that MBA-15 osteoprogenitor cells, despite their extensive bone formation ability, are unable to form a microenvironment supportive for hematopoiesis and osteoclastogenesis or to initiate bone remodeling.<\/jats:p>","DOI":"10.1002\/jbmr.5650090719","type":"journal-article","created":{"date-parts":[[2010,2,3]],"date-time":"2010-02-03T16:33:05Z","timestamp":1265214785000},"page":"1107-1114","source":"Crossref","is-referenced-by-count":23,"title":["Bone formation by marrow osteogenic cells (MBA-15) is not accompanied by osteoclastogenesis and generation of hematopoietic supportive microenvironment"],"prefix":"10.1093","volume":"9","author":[{"given":"D.","family":"DR. Benayahu","sequence":"first","affiliation":[{"name":"Department of Cell Biology, Weizmann Institute of Science, Rehovot, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"O.","family":"Gurevitch","sequence":"additional","affiliation":[{"name":"Department of Histology and Cell Biology, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"D.","family":"Zipori","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Weizmann Institute of Science, Rehovot, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.","family":"Wientroub","sequence":"additional","affiliation":[{"name":"Department of Pediatric Orthopaedics, Dana Children's Hospital, Tel-Aviv Medical Center, Tel-Aviv, Israel"},{"name":"Division of Orthopaedics, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[1994,7,1]]},"reference":[{"key":"2024013113125418000_bib1","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1002\/ajh.2830150211","article-title":"Hemopoietic stromal microen-vironment","volume":"15","author":"Tavassoli","year":"1983","journal-title":"Am J Hematol"},{"key":"2024013113125418000_bib2","first-page":"621","article-title":"Determination of bone marrow stem cell differentiation by stromal hemopoietic inductive microenvironments (HIM)","volume":"65","author":"Trentin","year":"1971","journal-title":"Am J Pathol"},{"key":"2024013113125418000_bib3","first-page":"1","volume-title":"Handbook of the Hemopoietic Microenvironment","author":"Trentin","year":"1989"},{"key":"2024013113125418000_bib4","first-page":"269","article-title":"Embryonic and fetal hemopoiesis, an overview","volume":"17","author":"Tavassoli","year":"1991","journal-title":"Blood Cells"},{"key":"2024013113125418000_bib5","doi-asserted-by":"crossref","first-page":"2691","DOI":"10.1096\/fasebj.6.9.1612293","article-title":"The renewal and differentiation of hemopoietic stem cells","volume":"6","author":"Zipori","year":"1992","journal-title":"FASEB J"},{"key":"2024013113125418000_bib6","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/S0950-3536(11)80006-5","article-title":"Myeloid cell kinetics in response to haemopoietic growth factors","volume":"5\/3","author":"Lord","year":"1992","journal-title":"Baillieres Clin Haematol"},{"key":"2024013113125418000_bib7","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1097\/00007890-197404000-00001","article-title":"Stromal cells responsible for transferring the microenvironment of hemopoietic tissues. Cloning in-vitro and retransplantation in-vivo","volume":"17","author":"Friedenstein","year":"1974","journal-title":"Transplantation"},{"key":"2024013113125418000_bib8","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/978-3-642-67319-1_3","volume-title":"Immunology of Bone Marrow Transplantation","author":"Friedenstein","year":"1980"},{"key":"2024013113125418000_bib9","first-page":"505","article-title":"Identification of distinctive stromal elements in erythroid and neutrophil granuloid spleen colonies: Light and electron microscopic study","volume":"5","author":"LaPushin","year":"1977","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib10","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/S0950-3536(11)80015-6","article-title":"Growth restrictions in the regulation of haemopoiesis","volume":"5\/3","author":"Zipori","year":"1992","journal-title":"Baillieres Clin Haematol"},{"key":"2024013113125418000_bib11","doi-asserted-by":"crossref","first-page":"1901","DOI":"10.1083\/jcb.99.6.1901","article-title":"Osteoclast formation from mononuclear phagocytes: Role of bone forming cells","volume":"99","author":"Burger","year":"1984","journal-title":"J Cell Biol"},{"key":"2024013113125418000_bib12","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1007\/BF02556605","article-title":"Evidence for osteoclast production in mixed bone cell culture","volume":"38","author":"Marshall","year":"1986","journal-title":"Calcif Tissue Int"},{"key":"2024013113125418000_bib13","doi-asserted-by":"crossref","first-page":"1630","DOI":"10.1210\/endo-128-3-1630","article-title":"Mouse osteoblastic cells (MC3T3-El) and different stages of differentiation have opposite effects on osteoclastic cell formation","volume":"128","author":"Hiura","year":"1991","journal-title":"Endocrinology"},{"key":"2024013113125418000_bib14","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":"2024013113125418000_bib15","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1038\/345442a0","article-title":"The murine mutation osteopetrosis is the coding region of macrophage colony stimulating factor gene","volume":"345","author":"Yoshida","year":"1990","journal-title":"Nature"},{"key":"2024013113125418000_bib16","doi-asserted-by":"crossref","first-page":"4828","DOI":"10.1073\/pnas.87.12.4828","article-title":"Total absence of colony stimulating factor 1 in the macrophage-deficient osteopetrotic (op\/op) mouse","volume":"87","author":"Wiktor-Jedrzejczak","year":"1990","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024013113125418000_bib17","doi-asserted-by":"crossref","first-page":"2592","DOI":"10.1210\/endo-127-5-2592","article-title":"Macrophage colony stimulating factor prestores in vivo bone resorption in the op\/op osteopetrotic mouse","volume":"127","author":"Felix","year":"1990","journal-title":"Endocrinology"},{"key":"2024013113125418000_bib18","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1002\/jbmr.5650050716","article-title":"Impairment of macrophage colony-stimulating factor production and lack of resident bone marrow macrophages in the osteopetrotic op\/op mouse","volume":"5","author":"Felix","year":"1990","journal-title":"J Bone Miner Res"},{"key":"2024013113125418000_bib19","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1002\/jbmr.5650060912","article-title":"Role of colony-stimulating factors in osteoclast development","volume":"6","author":"Takahashi","year":"1991","journal-title":"J Bone Miner Res"},{"key":"2024013113125418000_bib20","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1210\/endo-128-4-1792","article-title":"Deficiency of osteoclast in osteopetrotic mice is due to a defect in the local microenvironment provided by osteoblastic cells","volume":"128","author":"Takahashi","year":"1991","journal-title":"Endocrinology"},{"key":"2024013113125418000_bib21","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0006-291X(05)81382-8","article-title":"Osteoclast resorption-stimulating activity is associated with the osteoblast cell surface and\/or the extracellular matrix","volume":"181","author":"Fuller","year":"1991","journal-title":"Biochem Biophys Res Commun"},{"key":"2024013113125418000_bib22","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1172\/JCI113089","article-title":"1,25-Dihydroxyvitamin D3 stimulates rat osteoblastic cells to release a soluble factor that increases osteoclastic bone resorption","volume":"80","author":"McSheehy","year":"1987","journal-title":"J Clin Invest"},{"key":"2024013113125418000_bib23","doi-asserted-by":"crossref","first-page":"2075","DOI":"10.1210\/endo-125-4-2075","article-title":"Partial characterization of a parathyroid hormone stimulated resorption factor(s) from osteoblast like cells","volume":"125","author":"Perry","year":"1989","journal-title":"Endocrinology"},{"key":"2024013113125418000_bib24","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1210\/endo-126-3-1783","article-title":"The parathyroid hormone related protein stimulates human osteoclast-like cells to secrete a 9.000 dalton bone resorbing protein","volume":"126","author":"Morris","year":"1990","journal-title":"Endocrinology"},{"key":"2024013113125418000_bib25","doi-asserted-by":"crossref","first-page":"8500","DOI":"10.1073\/pnas.88.19.8500","article-title":"Isolation of a murine osteoclast colony stimulating factor","volume":"88","author":"Lee","year":"1991","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024013113125418000_bib26","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1016\/0006-291X(91)91419-D","article-title":"Osteoblast-osteoclast relationships in bone resorption: Osteoblasts enhance osteoclast activity in a serum free co-culture system","volume":"179","author":"Teti","year":"1991","journal-title":"Biochem Biophys Res Commun"},{"key":"2024013113125418000_bib27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/jcp.1041400102","article-title":"Bone marrow-derived stromal cell line expressing osteoblastic phenotype in-vitro and osteogenic capacity in-vivo","volume":"140","author":"Benayahu","year":"1989","journal-title":"J Cell Physiol"},{"key":"2024013113125418000_bib28","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1002\/jcp.1041550306","article-title":"Marrow stroma-derived osteogenic clonal cell lines: Putative stages in osteoblastic differentiation","volume":"155","author":"Fried","year":"1993","journal-title":"J Cell Physiol"},{"key":"2024013113125418000_bib29","doi-asserted-by":"crossref","first-page":"634","DOI":"10.3181\/00379727-143-37381","article-title":"Influence of geometry of transplanted tooth and bone on transformation of fibroblasts","volume":"143","author":"Reddi","year":"1973","journal-title":"Proc Soc Exp Biol Med"},{"key":"2024013113125418000_bib30","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1007\/BF02411210","article-title":"Alkaline phosphatase inhibition by parathyroid hormone and isoproterenol in a clonal rat osteosarcoma cell line. Possible mediation by cyclic AMP","volume":"34","author":"Majeska","year":"1982","journal-title":"Calcif Tissue Int"},{"key":"2024013113125418000_bib31","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/0006-291X(90)90719-4","article-title":"Neutral endopeptidase (EC 3.4.24.11) is highly expressed on osteoblastic cells and other marrow stromal cell types","volume":"172","author":"Indig","year":"1990","journal-title":"Biochem Biophys Res Commun"},{"key":"2024013113125418000_bib32","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J Biol Chem"},{"key":"2024013113125418000_bib33","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/0371-1951(60)80089-6","article-title":"The determination of metal in blood serum by atomic absorption spectroscopy. I. Calcium","volume":"16","author":"Willis","year":"1960","journal-title":"Spectrochim Acta"},{"key":"2024013113125418000_bib34","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/S0950-3536(11)80004-1","article-title":"Hemopoietic tissue","volume":"5\/3","author":"Wright","year":"1992","journal-title":"Baillieres Clin Haematol"},{"key":"2024013113125418000_bib35","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1007\/BF00334547","article-title":"Hemopoietic functions of marrow-derived osteogenic cells","volume":"51","author":"Benayahu","year":"1992","journal-title":"Calcif Tissue Int"},{"key":"2024013113125418000_bib36","first-page":"613","article-title":"A study of homologous cancellous bone combined with autologous red marrow after transplantation to a muscular site","volume":"95","author":"Burwell","year":"1961","journal-title":"J Anat"},{"key":"2024013113125418000_bib37","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1097\/00003086-198511000-00021","article-title":"The function of bone marrow in the incorporation of a bone graft","volume":"200","author":"Burwell","year":"1985","journal-title":"Clin Orthop"},{"key":"2024013113125418000_bib38","first-page":"87","article-title":"Bone formation occurring in bone marrow transplantation in diffusion chambers","volume":"12","author":"Petrakova","year":"1963","journal-title":"Bull Exp Biol Med"},{"key":"2024013113125418000_bib39","first-page":"381","article-title":"Osteogenesis in transplants of bone marrow cells","volume":"16","author":"Friedenstein","year":"1966","journal-title":"J Embryol Exp Morphol"},{"key":"2024013113125418000_bib40","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/BF00218212","article-title":"Bone formation in organ cultures of bone marrow","volume":"248","author":"Luria","year":"1987","journal-title":"Cell Tissue Res"},{"key":"2024013113125418000_bib41","first-page":"720","article-title":"Bone formation by mouse marrow cell suspensions in organ cultures","volume":"6","author":"Luria","year":"1988","journal-title":"Bull Exp Biol Med"},{"key":"2024013113125418000_bib42","first-page":"263","article-title":"Bone marrow osteogenic stem cells: In vitro cultivation and transplantation in diffusion chambers","volume":"20","author":"Friedenstein","year":"1987","journal-title":"Cell Tissue Kinet"},{"key":"2024013113125418000_bib43","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1073\/pnas.69.6.1601","article-title":"Biochemical sequences in the transformation of normal fibroblasts in adolescent rats","volume":"69","author":"Reddi","year":"1972","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024013113125418000_bib44","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1083\/jcb.69.3.557","article-title":"Collagenous bone matrix-induced endochondral ossification and hematopoiesis","volume":"69","author":"Reddi","year":"1976","journal-title":"J Cell Biol"},{"key":"2024013113125418000_bib45","first-page":"135","article-title":"Bone marrow regeneration after local injury: A review","volume":"3","author":"Patt","year":"1975","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib46","first-page":"225","volume-title":"Stem Cells of Renewing Cell Populations","author":"Trentin","year":"1976"},{"issue":"12","key":"2024013113125418000_bib47","first-page":"153","article-title":"Matrix-induced bone and marrow development: A model for postfetal hematopoiesis","volume":"10","author":"Wientroub","year":"1982","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib48","first-page":"131","article-title":"Establishment of the hematopoietic microenvironment in the marrow of matrix-induced endochondral bone","volume":"12","author":"McCarthy","year":"1984","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib49","first-page":"309","article-title":"New bone formation and bone marrow differentiation induced in rats by extracellular bone matrix implantation: Effect of local preirradiation on the process","volume":"15","author":"Bleiberg","year":"1987","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib50","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1002\/stem.5530080206","article-title":"The ability of induced osteo-progenitor cells to maintain and rebuild long-term ectopic osteo-hematopoietic foci in vivo","volume":"8","author":"Gurevitch","year":"1990","journal-title":"Int J Cell Cloning"},{"key":"2024013113125418000_bib51","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1002\/stem.5530110110","article-title":"Ability of the hemopoietic microenvironment in the induced bone to maintain the proliferative potential of early hemopoietic precursors","volume":"11","author":"Gurevitch","year":"1993","journal-title":"Stem Cells"},{"key":"2024013113125418000_bib52","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1182\/blood.V76.6.1059.1059","article-title":"Molecular basis of homing of intravenously transplanted stem cells to the marrow","volume":"76","author":"Tavassoli","year":"1990","journal-title":"Blood"},{"key":"2024013113125418000_bib53","doi-asserted-by":"crossref","first-page":"3180","DOI":"10.1073\/pnas.85.9.3180","article-title":"Molecular basis of the recognition of intravenously transplanted hemopoietic cells by bone marrow","volume":"85","author":"Aizawa","year":"1988","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024013113125418000_bib54","first-page":"65","article-title":"Murine spleen culture: Homing of hemopoietic progenitor cells to spleen is not mediated by a similar mechanism as in the marrow","volume":"18","author":"Konno","year":"1990","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib55","first-page":"54","volume-title":"Textbook of Hematology","author":"Tavassoli","year":"1990","edition":"4th ed."},{"key":"2024013113125418000_bib56","first-page":"636","article-title":"Homing of a cloned multipotential stem cell line in spleen and intraperitoneal membrane","volume":"14","author":"Hardy","year":"1986","journal-title":"Exp Hematol"},{"key":"2024013113125418000_bib57","first-page":"811","article-title":"Marrow uptake of galactosyl-containing neoglycoprotein: Implications in stem cell homing","volume":"16","author":"Aizawa","year":"1988","journal-title":"Exp Hematol"},{"year":"1994","author":"Benayahu","key":"2024013113125418000_bib58"},{"key":"2024013113125418000_bib59","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/0045-6039(87)90479-9","article-title":"Impaired recruitment and differentiation of osteoclast progenitors by osteocalcin-deplete bone implants","volume":"21","author":"Glowacki","year":"1987","journal-title":"Cell Differ"},{"key":"2024013113125418000_bib60","first-page":"66","article-title":"Modulation of osteoclast differentiation","volume":"13","author":"Suda","year":"1992","journal-title":"Endocr Rev"},{"key":"2024013113125418000_bib61","first-page":"108","volume-title":"Cell and Molecular Biology of Vertabrate Hard Tissue","author":"Osdoby","year":"1988"}],"container-title":["Journal of Bone and Mineral Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fjbmr.5650090719","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/9\/7\/1107\/56496866\/5650090719.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/9\/7\/1107\/56496866\/5650090719.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,13]],"date-time":"2024-03-13T14:58:39Z","timestamp":1710341919000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jbmr\/article\/9\/7\/1107-1114\/7501039"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1994,7,1]]},"references-count":61,"journal-issue":{"issue":"7","published-online":{"date-parts":[[1994,7,1]]},"published-print":{"date-parts":[[1994,7,1]]}},"URL":"https:\/\/doi.org\/10.1002\/jbmr.5650090719","relation":{},"ISSN":["0884-0431","1523-4681"],"issn-type":[{"type":"print","value":"0884-0431"},{"type":"electronic","value":"1523-4681"}],"subject":[],"published-other":{"date-parts":[[1994,7,1]]},"published":{"date-parts":[[1994,7,1]]}}}