Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-25T01:48:48.541Z Has data issue: false hasContentIssue false
  • English
  • Français

Guidelines for using in vitro methods to study the effects of phyto-oestrogens on bone

Published online by Cambridge University Press:  26 October 2011

Michèle Lieberherr ,
Giulia Cournot  and
Simon P. Robins
Michèle Lieberherr*
Affiliation:
Laboratoire de Nutrition et de Sécurité Alimentaire, Institut National de la Recherche Agronomique, F-78350 Jouy-en-Josas, France
Giulia Cournot
Affiliation:
Laboratoire de Nutrition et de Sécurité Alimentaire, Institut National de la Recherche Agronomique, F-78350 Jouy-en-Josas, France
Simon P. Robins
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Dr M. Lieberherr, fax +33 1 34 65 23 11, email [email protected]
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

These guidelines review the relevant literature on the way plant phyto-oestrogens act on bone and the responsiveness of different bone cell systems to phyto-oestrogenic compounds. The primary emphasis is on the experimental conditions used, the markers available for assessing osteoblast and osteoclast function, and their expected sensitivity. Finally, we assess the published results to derive some general recommendations for in vitro experiments in this area of research.

Keywords

Phyto-oestrogensOsteoblastOsteoclastOsteoprogenitor bone marrow cells
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue S1: Effects of Phyto-oestrogens on Bone Health: the VENUS Concerted Action , June 2003 , pp. S59 - S73
Copyright
Copyright © The Nutrition Society 2003

References

Akatsu, T, Tamura, T, Takahashi, N, Udagawa, N, Tanaka, S, Sasaki, T, Yamaguchi, A, Nagata, N & Suda, T (1992) Preparation and characterization of a mouse osteoclast-like multinucleated cell population. Journal of Bone and Mineral Research 7, 1297–1306.CrossRefGoogle ScholarPubMed
American Society for Bone and Mineral Research President's Committee on Nomenclature (2000) Proposed standard nomenclature for new tumor necrosis factor family members involved in the regulation of bone resorption. Journal of Bone and Mineral Research 15, 2293–2296.CrossRefGoogle Scholar
Arnett, TR, Boyde, A, Jones, SJ & Taylor, ML (1994) Effects of medium acidification by alteration of carbon dioxide or bicarbonate concentrations on the resorptive activity of rat osteoclasts. Journal of Bone and Mineral Research 9, 375–379.CrossRefGoogle ScholarPubMed
Arts, J, Kuiper, GGJM, Janssen, JMMF, Gustafsson, J-A, Löwik, CWGM, Pols, HA & Van Leeuwen, JPTM (1997) Differential expression of estrogen receptors α and β mRNA during differentiation of human osteoblast SV-HFO cells. Endocrinology 138, 5067–5070.CrossRefGoogle ScholarPubMed
Aubin, JE (1999) Osteoprogenitor cell frequency in rat bone marrow stromal populations: role for heterotypic cell–cell interactions in osteoblast differentiation. Journal of Cellular Biochemistry 72, 396–410.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Aubin, JE, Heersche, JN, Merrilees, MJ & Sodek, J (1982) Isolation of bone cell clones with differences in growth, hormone responses, and extracellular matrix production. Journal of Cell Biology 92, 452–461.CrossRefGoogle ScholarPubMed
Aubin, JE, Liu, F, Malaval, L & Gupta, A (1995) Quantitative polymerase chain reaction (PCR): potential applications of poly(A) PCR on samples of limited cell number. Calcified Tissue International 56, Suppl. 1, S54–S56.CrossRefGoogle Scholar
Barkhem, T, Carlsson, B, Nilsson, Y, Enmark, E, Gustafsson, J-A & Nilsson, S (1998) Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Molecular Pharmacology 54, 105–112.CrossRefGoogle ScholarPubMed
Baylink, DJ & Liu, CC (1979) The regulation of endosteal bone volume. Journal of Periodontology 50, 43–49.CrossRefGoogle ScholarPubMed
Bellows, CG, Heersche, JN & Aubin, JE (1990) Determination of the capacity for proliferation and differentiation of osteoprogenitor cells in the presence and absence of dexamethasone. Developmental Biology 140, 132–138.CrossRefGoogle ScholarPubMed
Benayahu, D, Fried, A, Zipori, D & Wientroub, S (1991) Subpopulations of marrow stromal cells share a variety of osteoblast markers. Calcified Tissue International 49, 202–207.CrossRefGoogle Scholar
Benayahu, D, Horowitz, M, Zipori, D & Wientroub, S (1992) Hemopoietic functions of marrow-derived osteogenic cells. Calcified Tissue International 51, 195–201.CrossRefGoogle ScholarPubMed
Beresford, JN, Graves, SE & Smoothy, CA (1993) Formation of mineralized nodules by bone derived cells in vitro: a model of bone formation? American Journal of Medical Genetics 45, 163–178.CrossRefGoogle Scholar
Billiau, A, Edy, VG, Heremans, H, Van Damme, J, Desmyter, J, Georgiades, JA & De Somer, P (1977) Human interferon: mass production in a newly established cell line, MG-63. Antimicrobial Agents and Chemotherapy 12, 11–15.CrossRefGoogle Scholar
Boyce, BF, Yoneda, T, Lowe, C, Soriano, P & Mundy, GR (1992) Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. Journal of Clinical Investigation 90, 1622–1627.CrossRefGoogle ScholarPubMed
Boyde, A, Ali, NN & Jones, SJ (1984) Resorption of dentine by isolated osteoclasts in vitro. British Dental Journal 156, 216–220.CrossRefGoogle ScholarPubMed
Cancedda, R, Descalzi-Cancedda, F & Castagnola, P (1995) Chondrocyte differentiation. International Review of Cytology 159, 265–358.CrossRefGoogle ScholarPubMed
Chambers, TJ, McSheehy, PM, Thomson, BM & Fuller, K (1985) The effect of calcium-regulating hormones and prostaglandins on bone resorption by osteoclasts disaggregated from neonatal rabbit bones. Endocrinology 116, 234–239.CrossRefGoogle Scholar
Chambers, TJ & Magnus, CJ (1982) Calcitonin alters behaviour of isolated osteoclasts. Journal of Pathology 136, 27–39.CrossRefGoogle ScholarPubMed
Chambers, TJ, Owens, JM, Hattersley, G, Jat, PS & Noble, MD (1993) Generation of osteoclast-inductive and osteoclastogenic cell lines from the H-2KbtsA58 transgenic mouse. Proceedings of the National Academy of Sciences of the USA 90, 5578–5582.CrossRefGoogle ScholarPubMed
Chambers, TJ, Revell, PA, Fuller, K & Athanasou, NA (1984) Resorption of bone by isolated rabbit osteoclasts. Journal of Cell Science 66, 383–399.CrossRefGoogle ScholarPubMed
Chen, TL & Raisz, LG (1975) The effects of ascorbic acid deficiency on calcium and collagen metabolism in cultured fetal rat bones. Calcified Tissue Research 17, 113–127.CrossRefGoogle ScholarPubMed
Cheng, SL, Lecanda, F, Davidson, MK, Warlow, PM, Zhang, SF, Zhang, L, Suzuki, S, St John, T & Civitelli, R (1998) Human osteoblasts express a repertoire of cadherins, which are critical for BMP-2-induced osteogenic differentiation. Journal of Bone and Mineral Research 13, 633–644.CrossRefGoogle ScholarPubMed
Chyun, YS, Kream, BE & Raisz, LG (1984) Cortisol decreases bone formation by inhibiting periosteal cell proliferation. Endocrinology 114, 477–480.CrossRefGoogle ScholarPubMed
Clover, J & Gowen, M (1994) Are MG-63 and HOS TE85 human osteosarcoma cell lines representative models of the osteoblast phenotype? Bone 15, 585–591.CrossRefGoogle Scholar
Collin-Osdoby, P, Oursler, MJ, Webber, D & Osdoby, P (1991) Osteoclast-specific monoclonal antibodies coupled to magnetic beads provide a rapid and efficient method of purifying avian osteoclasts. Journal of Bone and Mineral Research 6, 1353–1365.CrossRefGoogle ScholarPubMed
Cowin, SC, Moss-Salentijn, L & Moss, ML (1991) Candidates for the mechanosensory system in bone. Journal of Biomechanical Engineering 113, 191–197.CrossRefGoogle ScholarPubMed
Denis, I, Pointillart, A & Lieberherr, M (1994) Cell stage-dependent effects of ascorbic acid on cultured porcine bone cells. Bone and Mineral 25, 149–161.CrossRefGoogle ScholarPubMed
de Vernejoul, M, Horowitz, M, Demignon, J, Neff, L & Baron, R (1988) Bone resorption by isolated chick osteoclasts in culture is stimulated by murine spleen cell supernatant fluids (osteoclast-activating factor) and inhibited by calcitonin and prostaglandin E2. Journal of Bone and Mineral Research 3, 69–80.CrossRefGoogle ScholarPubMed
Dieudonne, SC, Semeins, CM, Goei, SW, Vukicevic, S, Nulend, JK, Sampath, TK, Helder, M & Burger, EH (1994) Opposite effects of osteogenic protein and transforming growth factor beta on chondrogenesis in cultured long bone rudiments. Journal of Bone and Mineral Research1 9, 771–780.CrossRefGoogle ScholarPubMed
Doty, SB & Schofield, BH (1976) Enzyme histochemistry of bone and cartilage cells. Progress in Histochemistry and Cytochemistry 8, 1–38.Google ScholarPubMed
Ecarot-Charrier, B, Glorieux, FH, van der Rest, M & Pereira, G (1983) Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture. Journal of Cell Biology 96, 639–643.CrossRefGoogle ScholarPubMed
Endoh, H, Sasaki, H, Maruyama, K, Takeyama, K, Waga, I, Shimizu, T, Kato, S & Kawashima, H (1997) Rapid activation of MAP kinase by estrogen in the bone cell line. Biochemical and Biophysical Research Communications 235, 99–102.CrossRefGoogle ScholarPubMed
Evans, CE, Galasko, CS & Ward, C (1990) Effect of donor age on the growth in vitro of cells obtained from human trabecular bone. Journal of Orthopaedic Research 8, 234–237.CrossRefGoogle ScholarPubMed
Fedarko, NS, Vetter, UK & Robey, PG (1995) Age-related changes in bone matrix structure in vitro. Calcified Tissue International 56, Suppl. 1, S41–S43.CrossRefGoogle Scholar
Fedarko, NS, Vetter, UK, Weinstein, S & Robey, PG (1992) Age related changes in hyaluronan, proteoglycan, collagen, and osteonectin synthesis by human bone cells. Journal of Cellular Physiology 151, 215–227.CrossRefGoogle ScholarPubMed
Fleet, JC & Hock, JM (1994) Identification of osteocalcin mRNA in nonosteoid tissue of rats and humans by reverse transcription–polymerase chain reaction. Journal of Bone and Mineral Research 9, 1565–1573.CrossRefGoogle ScholarPubMed
Fournier, B & Price, PA (1991) Characterization of a new human osteosarcoma cell line OHS-4. Journal of Cell Biology 114, 577–583.CrossRefGoogle ScholarPubMed
Friedenstein, AJ (1990) Osteogenic stem cells in the bone marrow. In Bone and Mineral Research, vol. 7, pp. 243–270 [Heersche, JNM and Kanis, JA, editors]. Amsterdam: Elsevier Science Publishers.CrossRefGoogle Scholar
Gattei, V, Bernabei, PA, Pinto, A, Bezzini, R, Ringressi, A, Formigli, L, Tanini, A, Attadia, V & Brandi, ML (1992) Phorbol ester induced osteoclast-like differentiation of a novel human leukemic cell line (FLG 29.1). Journal of Cell Biology 116, 437–447.CrossRefGoogle ScholarPubMed
Grano, M, Colucci, S, De Bellis, M, Zigrino, P, Argentino, L, Zambonin, G, Serra, M, Scotlandi, K, Teti, A & Zambonin Zallone, A (1994) New model for bone resorption study in vitro: human osteoclast-like cells from giant cell tumors of bone. Journal of Bone and Mineral Research 9, 1013–1020.CrossRefGoogle ScholarPubMed
Grigoriadis, AE, Petkovich, PM, Ber, R, Aubin, JE & Heersche, JN (1985) Subclone heterogeneity in a clonally-derived osteoblast like cell line. Bone 6, 249–256.CrossRefGoogle Scholar
Grigoriadis, AE, Wang, Z-Q, Cecchini, MG, Hofstetter, W, Felix, R & Fleisch, HA (1994) c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodelling. Science 266, 443–448.CrossRefGoogle Scholar
Gronowicz, GA, Fall, PM & Raisz, LG (1994) Prostaglandin E2 stimulates preosteoblast replication: an autoradiographic study in cultured fetal rat calvariae. Experimental Cell Research 212, 314–320.CrossRefGoogle ScholarPubMed
Gronowicz, G, Woodiel, FN, McCarthy, MB & Raisz, LG (1989) In vitro mineralization of fetal rat parietal bones in defined serum-free medium: effect of beta-glycerol phosphate. Journal of Bone and Mineral Research 4, 313–324.CrossRefGoogle ScholarPubMed
Gundle, R & Beresford, JN (1995) The isolation and culture of cells from explants of human trabecular bone. Calcified Tissue International 56, Suppl. 1, S8–S10.CrossRefGoogle Scholar
Gurdon, JB, Lemaire, P & Kato, K (1993) Community effects and related phenomena in development. Cell 75, 831–834.CrossRefGoogle ScholarPubMed
Harris, SA, Enger, RJ, Riggs, BL & Spelsberg, TC (1995) Development and characterization of a conditionally immortalized human fetal osteoblast cell line. Journal of Bone and Mineral Research 10, 178–186.CrossRefGoogle Scholar
Heath, JK, Rodan, SB, Yoon, K & Rodan, GA (1989) Rat calvarial cell lines immortalized with SV-40 large T antigen: constitutive and retinoic acid-inducible expression of osteoblast features. Endocrinology 124, 3060–3068.Google ScholarPubMed
Hentunen, TA, Reddy, SV, Boyce, BF, Devlin, R, Park, HR, Chung, H, Selander, KS, Dallas, M, Kurihara, N, Galson, DL, Goldring, SR, Koop, BA, Windle, JJ & Roodman, GD (1998) Immortalization of osteoclast precursors by targeting Bcl-XL and Simian virus 40 large T antigen to the osteoclast lineage in transgenic mice. Journal of Clinical Investigation 102, 88–97.CrossRefGoogle Scholar
Hock, J, Gunness-Hey, M, Poser, J, Olson, H, Bell, N & Raisz, LG (1968) Stimulation of undermineralized matrix formation by 1,25-dihydroxyvitamin D3 in long bones of rats. Calcified Tissue International 38, 78–86.Google Scholar
Hofstetter, W, Guenther, H, Stutzer, A, Schenk, R, Fleisch, H & Friis, R (1991) Establishment and characterization of two immortalized cell lines of the osteoblast lineage. Journal of Bone and Mineral Research 6, 609–622.CrossRefGoogle Scholar
Howard, G, Bottemiller, B & Baylink, D (1980) Evidence for coupling of bone formation to bone resorption in vivo. Metabolic Bone Disease & Related Research 2, 131–135.CrossRefGoogle Scholar
Hughes, DE, Dai, A, Tiffee, JC, Li, HH, Mundy, GR & Boyce, BF (1996) Estrogen promotes apoptosis of murine osteoclasts mediated by transforming growth factor-beta. Nature Medicine 2, 1132–1136.CrossRefGoogle Scholar
Hunter, I, McGregor, DP & Robins, SP (2001) Caspase-dependent cleavage of cadherins and catenins during osteoblast apoptosis. Journal of Bone and Mineral Research 16, 466–477.CrossRefGoogle ScholarPubMed
Jacenko, O & Tuan, RS (1986) Calcium deficiency induces expression of cartilage-like phenotype in chick embryonic calvaria. Developmental Biology 115, 215–232.CrossRefGoogle ScholarPubMed
James, IE, Dodds, RA, Lee-Rykaczewski, E, Eichman, CF, Connor, JR, Hart, TK, Maleeff, BE, Lackman, RD & Gowen, M (1996) Purification and characterization of fully functional human osteoclast precursors. Journal of Bone and Mineral Research 11, 1608–1618.CrossRefGoogle ScholarPubMed
Jat, PS & Sharp, PA (1986) Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts. Journal of Virology 59, 746–750.CrossRefGoogle Scholar
Jones, JI & Clemmons, DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 16, 3–34.Google ScholarPubMed
Katzburg, S, Lieberherr, M, Ornoy, A, Klein, BY, Hendel, D & Somjen, D (1999) Isolation and hormonal responsiveness of primary cultures of human bone-derived cells: gender and age differences. Bone 25, 667–673.CrossRefGoogle ScholarPubMed
Keck, E, Schartl, A, West, TB, Kruskemper, HL & Delling, G (1984) Influence of prostaglandins on electrolyte metabolism of human trabecular bone in vitro. Prostaglandins 28, 455–467.CrossRefGoogle ScholarPubMed
Keeting, PE, Scott, RE, Colvard, DS, Anderson, MA, Oursler, MJ, Spelsberg, TC & Riggs, BL (1992) Development and characterization of a rapidly proliferating, well-differentiated cell line derived from normal adult human osteoblast-like cells transfected with SV40 large T antigen. Journal of Bone and Mineral Research, 127–136.Google Scholar
Kream, BE, Petersen, DN & Raisz, LG (1990) Cortisol enhances the anabolic effects of insulin-like growth factor I on collagen synthesis and procollagen messenger ribonucleic acid levels in cultured 21-day fetal rat calvariae. Endocrinology 126, 1576–1583.CrossRefGoogle ScholarPubMed
Kudo, Y, Iwashita, M, Itatsu, S, Iguchi, T & Takeda, Y (1996) Regulation of insulin-like growth factor-binding protein-4 protease activity by estrogen and parathyroid hormone in SaOS-2 cells: implications for the pathogenesis of postmenopausal osteoporosis. Journal of Endocrinology 150, 223–229.CrossRefGoogle ScholarPubMed
Kuiper, GGJM, Carlsson, B, Gardien, K, Enmark, E, Häggblad, J, Nilsson, S & Gustafsson, J-A (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 138, 863–870.CrossRefGoogle ScholarPubMed
Labarca, C & Paigen, K (1980) A simple, rapid, and sensitive DNA assay procedure. Analytical Biochemistry 102, 344–352.CrossRefGoogle ScholarPubMed
Lee, KL, Aubin, JE & Heersche, JN (1992 a) beta-Glycerophosphate-induced mineralization of osteoid does not alter expression of extracellular matrix components in fetal rat calvarial cell cultures. Journal of Bone and Mineral Research 7, 1211–1219.CrossRefGoogle Scholar
Lee, MY, Lottsfeldt, JL & Fevold, KL (1992 b) Identification and characterization of osteoclast progenitors by clonal analysis of haematopoietic cells. Blood 80, 1710–1716.CrossRefGoogle Scholar
Liu, B & Marks, JD (2000) Applying phage antibodies to proteomics: selecting single chain Fv antibodies to antigens blotted on nitrocellulose. Analytical Biochemistry 286, 119–128.CrossRefGoogle ScholarPubMed
Lomri, A, Fromigue, O, Hott, M & Marie, PJ (1999) Genomic insertion of the SV-40 large T oncogene in normal adult human trabecular osteoblast cells induces cell growth without loss of the differentiated phenotype. Calcified Tissue International 64, 394–401.CrossRefGoogle Scholar
Long, MW, Robinson, JA, Ashcraft, EA & Mann, KG (1995) Regulation of human bone marrow-derived osteoprogenitor cells by osteogenic growth factors. Journal of Clinical Investigation 95, 881–887.CrossRefGoogle ScholarPubMed
Luben, RA, Wong, GL & Cohn, DV (1976) Biochemical characterization with parathormone and calcitonin of isolated bone cells: provisional identification of osteoclasts and osteoblasts. Endocrinology 99, 526–534.CrossRefGoogle ScholarPubMed
McCabe, MJ Jr & Orrenius, S (1993) Genistein induces apoptosis in immature human thymocytes by inhibiting topoisomerase-II. Biochemical and Biophysical Research Communications 194, 944–950.CrossRefGoogle ScholarPubMed
McCafferty, J, Griffiths, AD, Winter, G & Chiswell, DJ (1990) Phage antibodies: filamentous phage displaying antibody variable domains. Nature 348, 552–554.CrossRefGoogle ScholarPubMed
Malaval, L, Liu, F, Roche, P & Aubin, JE (1999) Kinetics of osteoprogenitor proliferation and osteoblast differentiation in vitro. Journal of Cellular Biochemistry 74, 616–627.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Malaval, L, Modrowski, D, Gupta, AK & Aubin, JE (1994) Cellular expression of bone-related proteins during in vitro osteogenesis in rat bone marrow stromal cell cultures. Journal of Cellular Physiology 158, 555–572.CrossRefGoogle ScholarPubMed
Malluche, HH & Faugere, M-C (1986) Atlas of Mineralized Bone Histology. Basel: Karger.Google Scholar
Marie, PJ (1994) Human osteoblast cells: a potential tool to assess the etiology of pathologic bone formation. Journal of Bone and Mineral Research1 9, 1847–1850.CrossRefGoogle Scholar
Marie, PJ, Lomri, A, Sabbagh, A & Basle, M (1989) Culture and behavior of osteoblast cells isolated from normal trabecular bone surfaces. In Vitro Cell Developmental Biology 25, 373–380.CrossRefGoogle ScholarPubMed
Markovits, J, Linassier, C, Fosse, P, Couprie, J, Pierre, J, Jacquemin-Sablon, A, Saucier, JM, Le Pecq, JB & Larsen, AK (1989) Inhibitory effects of the tyrosine kinase inhibitor genistein on mammalian DNA topoisomerase II. Cancer Research 49, 5111–5117.Google ScholarPubMed
Massey, HM & Flanagan, AM (1999) Human osteoclasts derive from CD14-positive monocytes. British Journal of Haematology 106, 167–170.CrossRefGoogle ScholarPubMed
Matsuyama, T, Lau, KH & Wergedal, JE (1990) Monolayer cultures of normal human bone cells contain multiple subpopulations of alkaline phosphatase positive cells. Calcified Tissue International 47, 276–283.CrossRefGoogle ScholarPubMed
Matsuzaki, K, Udagawa, N, Takahashi, N, Yamaguchi, K, Yasuda, H, Shima, N, Morinaga, T, Toyama, Y, Yabe, Y, Higashio, K & Suda, T (1998) Osteoclast differentiation factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochemical and Biophysical Research Communications 246, 199–204.CrossRefGoogle ScholarPubMed
Miyamoto, A, Kunisada, T, Yamazaki, H, Miyake, K, Nishikawa, SI, Sudo, T, Shultz, LD & Hayashi, SI (1998) Establishment and characterization of pro-B cell lines from motheaten mutant mouse defective in SHP-1 protein tyrosine phosphatase. Immunology Letters 63, 75–82.CrossRefGoogle ScholarPubMed
Mochizuki, H, Hakeda, Y, Wakatsuki, N, Usui, N, Akashi, S, Sato, T, Tanaka, K & Kumegawa, M (1992) Insulin-like growth factor-I supports formation and activation of osteoclasts. Endocrinology 131, 1075–1080.CrossRefGoogle ScholarPubMed
Mohan, S & Baylink, DJ (1991) Bone growth factors. Clinical Orthopaedics and Related Research 263, 30–48.CrossRefGoogle Scholar
Mohan, S & Baylink, DJ (1993) Characterization of the insulin-like growth factor regulatory system in bone. Advances in Experimental Medicine and Biology 343, 397–406.CrossRefGoogle ScholarPubMed
Most, W, Schot, L, Ederveen, A, van der Wee-Pals, L, Papapoulos, S & Lowik, C (1995) In vitro and ex vivo evidence that estrogens suppress increased bone resorption induced by ovariectomy or parathyroid hormone stimulation through an effect on osteoclastogenesis. Journal of Bone and Mineral Research 10, 1523–1530.CrossRefGoogle ScholarPubMed
Muguruma, Y & Lee, MY (1998) Isolation and characterization of murine clonogenic osteoclast progenitors by cell surface phenotype analysis. Blood 91, 1272–1279.CrossRefGoogle ScholarPubMed
Murakami, T, Yamamoto, M, Ono, K, Nishikawa, M, Nagata, N, Motoyoshi, K & Akatsu, T (1998) Transforming growth factor-betal increases mRNA levels of osteoclastogenesis inhibitory factor in osteoblast/stromal cells and inhibits the survival of murine osteoclast-like cells. Biochemical and Biophysical Research Communications 252, 747–752.CrossRefGoogle Scholar
Murrills, RJ, Stein, LS & Dempster, DW (1993) Stimulation of bone resorption and osteoclast clear zone formation by low pH: a time-course study. Journal of Cellular Physiology 154, 511–518.CrossRefGoogle Scholar
Murrills, RJ, Stein, LS, Fey, CP & Dempster, DW (1990) The effects of parathyroid hormone (PTH) and parathyroid hormone-related peptide on osteoclast resorption of bone slices in vitro: an analysis of pit size and the resorption focus. Endocrinology 127, 2648–2653.CrossRefGoogle ScholarPubMed
Nakahara, H, Bruder, SP, Haynesworth, SE, Holecek, JJ, Baber, MA, Goldberg, VM & Caplan, AI (1990) Bone and cartilage formation in diffusion chambers by subcultured cells derived from the periosteum. Bone 11, 181–188.CrossRefGoogle ScholarPubMed
Ng, KW, Gummer, PR, Michelangeli, VP, Bateman, JF, Mascara, T, Cole, WG & Martin, TJ (1988) Regulation of alkaline phosphatase expression in a neonatal rat clonal calvarial cell strain by retinoic acid. Journal of Bone and Mineral Research 3, 53–61.CrossRefGoogle Scholar
Nijweide, PJ, van der Plas, A & Scherft, JP (1981) Biochemical and histological studies on various bone cell preparations. Calcified Tissue International 33, 529–540.CrossRefGoogle ScholarPubMed
Nomura, S, Wills, AJ, Edwards, DR, Heath, JK & Hogan, BL (1988) Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization. Journal of Cell Biology 106, 441–450.CrossRefGoogle ScholarPubMed
Oreffo, RO, Kusec, V, Virdi, AS, Flanagan, AM, Grano, M, Zambonin-Zallone, A & Triffitt, JT (1999) Expression of estrogen receptor-alpha in cells of the osteoclastic lineage. Histochemistry and Cell Biology 111, 125–133.CrossRefGoogle ScholarPubMed
Oreffo, RO, Teti, A, Triffitt, JT, Francis, MJ, Carano, A & Zallone, AZ (1988) Effect of vitamin A on bone resorption: evidence for direct stimulation of isolated chicken osteoclasts by retinol and retinoic acid. Journal of Bone and Mineral Research 3, 203–210.CrossRefGoogle Scholar
Oursler, MJ, Collin-Osdoby, P, Anderson, F, Li, L, Webber, D & Osdoby, P (1991) Isolation of avian osteoclasts: improved techniques to preferentially purify viable cells. Journal of Bone and Mineral Research 6, 375–385.CrossRefGoogle ScholarPubMed
Owen, TA, Aronow, M, Shalhoub, V, Barone, LM, Wilming, L, Tassinari, MS, Kennedy, MB, Pockwinse, S, Lian, JB & Stein, GS (1990) Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. Journal of Cellular Physiology 143, 420–430.CrossRefGoogle ScholarPubMed
Paech, K, Webb, P, Kuiper, GG, Nilsson, S, Gustafsson, J, Kushner, PJ & Scanlan, TS (1997) Differential ligand activation of estrogen receptors estrogen receptoralpha and oestrogen receptorbeta at API sites. Science 277, 1508–1510.CrossRefGoogle Scholar
Parfitt, AM (1995) Problems in the application of in vitro systems to the study of human bone remodeling. Calcified Tissue International 56, Suppl. 1, S5–S7.CrossRefGoogle Scholar
Partridge, NC, Alcorn, D, Michelangeli, VP, Ryan, G & Martin, TJ (1983) Morphological and biochemical characterization of four clonal osteogenic sarcoma cell lines of rat origin. Cancer Research 43, 4308–4314.Google ScholarPubMed
Peck, WA, Birge, SJ & Fedak, SA (1984) Bone cells: biochemical and biological studies after enzymatic isolation. Science 146, 1476–1477.CrossRefGoogle Scholar
Peterkofsky, B & Diegelmann, R (1971) Use of a mixture of proteinase-free collagenases for the specific assay of radio active collagen in the presence of other proteins. Biochemistry 10, 988–994.CrossRefGoogle Scholar
Pike, AC, Brzozowski, AM, Hubbard, RE, Bonn, T, Thorsell, AG, Engstrom, O, Ljunggren, J, Gustafsson, J-A & Carlquist, M (1999) Structure of the ligand-binding domain of estrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO Journal 18, 4608–4618.CrossRefGoogle Scholar
Quarles, LD, Yohay, DA, Lever, LW, Caton, R & Wenstrup, RJ (1992) Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. Journal of Bone and Mineral Research 7, 683–692.CrossRefGoogle Scholar
Raisz, LG (1963) Stimulation of bone resorption by parathyroid hormone in tissue culture. Nature 197, 1015–1016.CrossRefGoogle ScholarPubMed
Rajah, R, Valentinis, B & Cohen, P (1997) Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-beta 1 on programmed cell death through a p53- and insulin-like growth factor-independent mechanism. Journal of Biological Chemistry 272, 12181–12188.CrossRefGoogle Scholar
Rajaram, S, Baylink, DJ & Mohan, S (1997) Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocrine Reviews 18, 801–831.Google ScholarPubMed
Ramp, WK & Neuman, WF (1971) Some factors affecting mineralization of bone in tissue culture. American Journal of Physiology 220, 270–274.CrossRefGoogle ScholarPubMed
Rassi, CM, Lieberherr, M, Chaumaz, G, Pointillart, A & Cournot, G (2002) Down-regulation of osteoclast differentiation by daidzein via caspase 3. Journal of Bone and Mineral Research 17, 630–638.CrossRefGoogle ScholarPubMed
Robey, PG (1995) Collagenase-treated trabecular bone fragments: a reproducible source of cells in the osteoblast lineage. Calcified Tissue International 56, Suppl. 1, S11–S12.CrossRefGoogle Scholar
Robey, PG & Termine, JD (1985) Human bone cells in vitro. Calcified Tissue International 37, 453–460.CrossRefGoogle ScholarPubMed
Rodan, GA & Noda, M (1991) Gene expression in osteoblast cells. Critical Reviews in Eukaryotic Gene Expression 1, 85–98.Google Scholar
Rodan, GA & Rodan, SB (1984) Expression of the osteoblast phenotype. In Bone and Mineral Research Annual 2, pp. 244–285 [Peck, WA, editor]. Amsterdam: Excerpta Medica.Google Scholar
Rodan, SB, Imai, Y, Thiede, MA, Wesolowski, G, Thompson, D, Bar-Shavit, Z, Shull, S, Mann, K & Rodan, GA (1987) Characterization of a human osteosarcoma cell line (Saos-2) with osteoblast properties. Cancer Research 47, 4961–4966.Google Scholar
Rodan, SB, Majeska, RJ & Rodan, GA (1994) Osteosarcoma cells as models for osteoblasts. In Frontiers of Osteosarcoma Research, pp. 193–203 [Novak, JF and MacMaster, JH, editors]. Seattle WA: Holgrefe and Huber.Google Scholar
Rowe, DW & Kream, BE (1982) Regulation of collagen synthesis in fetal rat calvaria by 1,25-dihydroxyvitamin D3. Journal of Biological Chemistry 257, 8009–8015.CrossRefGoogle Scholar
Salti, GI, Grewal, S, Mehta, RR, Das Gupta, TK, Boddie, AW Jr & Constantinou, AI (2000) Genistein induces apoptosis and topoisomerase II-mediated DNA breakage in colon cancer cells. European Journal of Cancer 36, 796–802.CrossRefGoogle ScholarPubMed
Sarma, U & Flanagan, AM (1996) Macrophage colony-stimulating factor induces substantial osteoclast generation and bone resorption in human bone marrow cultures. Blood 88, 2531–2540.CrossRefGoogle ScholarPubMed
Satomura, K, Hiraiwa, K & Nagayama, M (1991) Mineralized nodule formation in rat bone marrow stromal cell culture with out beta-glycerophosphate. Bone and Mineral 14, 41–54.CrossRefGoogle Scholar
Schmid, C (1995) Insulin-like growth factors. Cell Biology International 19, 445–457.CrossRefGoogle ScholarPubMed
Schmidt, R & Kulbe, KD (1993) Long-term cultivation of human osteoblasts. Bone and Mineral 20, 211–221.CrossRefGoogle ScholarPubMed
Sells Galvin, RJ, Gatlin, CL, Horn, JW & Fuson, TR (1999) Transforming growth factor-beta enhances osteoclast differentiation in haematopoietic cell cultures stimulated with receptor activator of NF-κB ligand and macrophage-colony stimulating factor. Biochemical and Biophysical Research Communications 265, 233–239.CrossRefGoogle Scholar
Service, RF (2000) Protein arrays step out of DNA's shadow. Science 289, 1673.CrossRefGoogle ScholarPubMed
Sly, WS, Hewett-Emmett, D, Whyte, MP, Yu, YS & Tashian, RE (1983) Carbonic anhydrase II deficiency identified as the primary defect in autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification. Proceedings of The National Academy of Sciences of the USA 80, 2752–2756.CrossRefGoogle ScholarPubMed
Smith, EP, Boyd, J, Frank, GR, Takahashi, H, Cohen, RM, Specker, B, Williams, TC, Lubahn, DB & Korach, KS (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. New England Journal of Medicine 331, 1056–1061.CrossRefGoogle ScholarPubMed
Sodek, J & Berkman, FA (1987) Bone cell cultures. In Methods of Enzymology, vol. 15, part E, pp. 303–324 [Cunningham, LW, editor]. Orlando, FL: Academic Press.Google Scholar
Solari, F, Flamant, F, Cherel, Y, Wyers, M & Jurdic, P (1996) The osteoclast generation: an in vitro and in vivo study with a genetically labelled avian monocytic cell line. Journal of Cell Science 109, 1203–1213.CrossRefGoogle Scholar
Soriano, P, Montgomery, C, Geske, R & Bradley, A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693–702.CrossRefGoogle ScholarPubMed
Soskolne, WA, Schwartz, Z & Ornoy, A (1986) The development of fetal mice long bones in vitro: an assay of bone modeling. Bone 7, 41–48.CrossRefGoogle ScholarPubMed
Srivastava, S, Weitzmann, MN, Kimble, RB, Rizzo, M, Zahner, M, Milbrandt, J, Ross, FP & Pacifici, R (1998) Estrogen blocks macrophage-colony stimulating factor gene expression and osteoclast formation by regulating phosphorylation of Egr-1 and its interaction with Sp-1. Journal of Clinical Investigation 102, 1850–1859.CrossRefGoogle ScholarPubMed
Stein, GS, Lian, JB, Stein, JL, van Wijnen, AJ, Frenkel, B & Montecino, M (1996) Mechanisms regulating osteoblast pro liferation and differentiation. In Principles of Bone Biology, pp. 69–86 [Bilezikian, JP, Raisz, LG and Rodan, GA, editors]. New York: Academic Press.Google Scholar
Stern, P & Raisz, LG (1979) Organ culture of bone. In Skeletal Research: An Experimental Approach, pp. 21–59 [Simmons, D and Kunin, A, editors]. New York: Academic Press.CrossRefGoogle Scholar
Suda, T, Takahashi, N, Udagawa, N, Jimi, E, Gillespie, MT & Martin, TJ (1999) Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocrine Reviews 20, 345–357.CrossRefGoogle ScholarPubMed
Sudo, H, Kodama, HA, Amagai, Y, Yamamoto, S & Kasai, S (1983) In vitro differentiation and calcification in a new clonal osteogenic cell line derived from new-born mouse calvaria. Journal of Cell Biology 96, 191–198.CrossRefGoogle Scholar
Sykes, B, Puddle, B, Francis, M & Smith, R (1976) The estimation of two collagens from human dermis by interrupted gel electrophoresis. Biochemical and Biophysical Research Communications 72, 1472–1480.CrossRefGoogle ScholarPubMed
Takahashi, N, Yamana, H, Yoshiki, S, Roodman, GD, Mundy, GR, Jones, SJ, Boyde, A & Suda, T (1988) Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology 122, 1373–1382.CrossRefGoogle ScholarPubMed
Tenenbaum, HC & Heersche, JN (1986) Differentiation of osteoid producing cells in vitro: possible evidence for the requirement of a microenvironment. Calcified Tissue International 38, 262–267.CrossRefGoogle ScholarPubMed
Tezuka, K, Sato, T, Kamioka, H, Nijweide, PJ, Tanaka, K, Matsuo, T, Ohta, M, Kurihara, N, Hakeda, Y & Kumegawa, M (1992) Identification of osteopontin in isolated rabbit osteoclasts. Biochemical and Biophysical Research Communications 186, 911–917.CrossRefGoogle ScholarPubMed
Udagawa, N, Takahashi, N, Akatsu, T, Sasaki, T, Yamaguchi, A, Kodama, H, Martin, TJ & Suda, T (1989) The bone marrow derived stromal cell lines MC3T3-G2/PA6 and ST2 support osteoclast-like cell differentiation in cocultures with mouse spleen cells. Endocrinology 125, 1805–1813.CrossRefGoogle ScholarPubMed
Udagawa, N, Takahashi, N, Akatsu, T, Tanaka, H, Sasaki, T, Nishihara, T, Koga, T, Martin, TJ & Suda, T (1990) Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proceedings of the National Academy of Sciences of the USA 87, 7260–7264.CrossRefGoogle Scholar
van der Plas, A, Aarden, EM, Feijen, JH, de Boer, AH, Wiltink, A, Alblas, MJ, de Leij, L & Nijweide, PJ (1994) Characteristics and properties of osteocytes in culture. Journal of Bone and Mineral Research 9, 1697–1704.CrossRefGoogle ScholarPubMed
van der Pluijm, G, Mouthaan, H, Baas, C, de Groot, H, Papapoulos, S & Lowik, C (1994) Integrins and osteoclastic resorption in three bone organ cultures: differential sensitivity to synthetic Arg-Gly-Asp peptides during osteoclast formation. Journal of Bone and Mineral Research1 9, 1021–1028.CrossRefGoogle ScholarPubMed
Walsh, S, Dodds, RA, James, IE, Bradbeer, JN & Gowen, M (1994) Monoclonal antibodies with selective reactivity against osteoblasts and osteocytes in human bone. Journal of Bone and Mineral Research 9, 1687–1696.CrossRefGoogle ScholarPubMed
Wesolowski, G, Duong, LT, Lakkakorpi, PT, Nagy, RM, Tezuka, K, Tanaka, H, Rodan, GA & Rodan, SB (1995) Isolation and characterization of highly enriched, prefusion mouse osteoclastic cells. Experimental Cell Research 219, 679–686.CrossRefGoogle ScholarPubMed
Whitson, SW, Whitson, MA, Bowers, DE Jr & Falk, MC (1992) Factors influencing synthesis and mineralization of bone matrix from fetal bovine bone cells grown in vitro. Journal of Bone and Mineral Research 7, 727–741.CrossRefGoogle ScholarPubMed
Williams, JP, Jordan, SE, Barnes, S & Blair, HC (1998) Tyrosine kinase inhibitor effects on avian osteoclastic acid transport. American Journal of Clinical Nutrition 68, 1369S–1374S.CrossRefGoogle ScholarPubMed
Wong, GL & Ng, MC (1992) Maturation-associated changes in the cellular composition of mouse calvariae and in the biochemical characteristics of calvarial cells separated into subclasses on Percoll density gradients. Journal of Bone and Mineral Research 7, 701–708.CrossRefGoogle ScholarPubMed
Wuthier, RE & Register, TC (1984) Role of alkaline phosphatase, a polyfunctional enzyme, in mineralizing tissues. In The Chemistry and Biology of Mineralized Tissues, pp. 113–124 [Butler, WT, editor]. Birmingham: Ebsco Media.Google Scholar
Yamaguchi, A & Kahn, AJ (1991) Clonal osteogenic cell lines express myogenic and adipocytic developmental potential. Calcified Tissue International 49, 221–225.CrossRefGoogle ScholarPubMed
Yee, JA (1983) Properties of osteoblast-like cells isolated from the cortical endosteal bone surface of adult rabbits. Calcified Tissue International 35, 571–577.CrossRefGoogle ScholarPubMed
Yoon, H, Chen, K, Baylink, DJ & Lau, KH (1998) Differential effects of two protein tyrosine kinase inhibitors, tyrphostin and genistein, on human bone cell proliferation as compared with differentiation. Calcified Tissue International 63, 243–249.CrossRefGoogle ScholarPubMed
Yoshida, H, Hayashi, S, Kunisada, T, Ogawa, M, Nishikawa, S, Okamura, H, Sudo, T, Shultz, LD & Nishikawa, S (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345, 442–444.CrossRefGoogle ScholarPubMed
Zambonin Zallone, A, Teti, A & Primavera, MV (1982) Isolated osteoclasts in primary culture: first observations on structure and survival in culture media. Anatomy and Embryology 165, 405–413.CrossRefGoogle ScholarPubMed
Zhang, RW, Simmons, DJ, Crowther, RS, Mohan, S & Baylink, DJ (1991) Contribution of marrow stromal cells to the regulation of osteoblast proliferation in rats: evidence for the involvement of insulin-like growth factors. Anatomy and Embryology 13, 201–215.Google Scholar