Transforming Growth Factor-β1 (TGF-β1) Induces Human Osteoclast Apoptosis by Up-regulating Bim
Open accessAbstract
Transforming growth factor-beta1 (TGF-beta1) is the most abundant TGF-beta isoform detected in bone and is an important functional modulator of osteoclasts. TGF-beta1 can induce osteoclast apoptosis; however, the apoptotic pathways involved in this process are not known. We show here that human osteoclasts express both type-I and type-II TGF-beta receptors. In the absence of survival factors, TGF-beta1 (1 ng/ml) induced osteoclast apoptosis. The expression of activated caspase-9, but not that of caspase-8, was increased by TGF-beta1 stimulation, and the rate of TGF-beta1-induced apoptosis was significantly lower in the presence of a caspase-9 inhibitor. To study further the mechanisms involved in TGF-beta1-induced osteoclast apoptosis, we investigated TGF-beta1 signaling, which primarily involves the Smad pathway, but also other pathways that may interfere with intracellular modulators of apoptosis, such as mitogen-activated protein (MAP) kinases and Bcl2 family members. We show here that early events consisted of a trend toward increased expression of extracellular signal-regulated kinase (ERK), and then TGF-beta1 significantly induced the activation of p38 and Smad2 in a time-dependent manner. These signaling cascades may activate the intrinsic apoptosis pathway, which involves Bim, the expression of which was increased in the presence of TGF-beta1. Furthermore, the rate of TGF-beta1-induced osteoclast apoptosis was lower when Bim expression was suppressed, and inhibiting the Smad pathway abolished Bim up-regulation following TGF-beta stimulation. This could correspond to a regulatory mechanism involved in the inhibition of osteoclast activity by TGF-beta1.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the absence of osteoclast survival factors such as RANKL, TGF-β1 leads to osteoclast apoptosis via upregulation of Bim expression.
“In the absence of osteoclast survival factors such as RANKL, TGF-β1 leads to osteoclast apoptosis via the upregulation of Bim expression.210”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [210]
Cites
Osteoclast differentiation and activation
Boyle, W. J., Simonet, W. S., & Lacey, D. L. (2003) · Nature · doi:10.1038/nature01658 · Cited by 6,670 · see citing works
Smad transcription factorsPreprint
Massagué, J., Seoane, J., & Wotton, D. (2005) · Genes & Development · doi:10.1101/gad.1350705 · Cited by 2,432 · see citing works
Estrogen promotes apoptosis of murine osteoclasts mediated by TGF–β
Hughes, D. E., Dai, A., Tiffee, J. C., Li, H. H., Mundy, G. R., & Boyce, B. F. (1996) · Nature Medicine · doi:10.1038/nm1096-1132 · Cited by 813 · see citing works
TGF‐β receptor‐activated p38 MAP kinase mediates Smad‐independent TGF‐β responses
Yu, L., DeRouen, M. C., & Zhang, Y. E. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf366 · Cited by 721 · see citing works
Transforming Growth Factor-β1 to the Bone
Janssens, K., ten Dijke, P., Janssens, S., & Van Hul, W. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0001 · Cited by 710 · see citing works
Molecular Biology of Bone Metastasis
Kingsley, L. A., Fournier, P. G. J., Chirgwin, J. M., & Guise, T. A. (2007) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-07-0234 · Cited by 437 · see citing works
Javelaud, D., & Mauviel, A. (2005) · Oncogene · doi:10.1038/sj.onc.1208928 · Cited by 400 · see citing works
Riggs, B. L., & PARFITT, A. M. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041114 · Cited by 379 · see citing works
TGF‐β signaling: A tale of two responses
Rahimi, R. A., & Leof, E. B. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21501 · Cited by 371 · see citing works
p38 MAP kinase: a convergence point in cancer therapy
Olson, J. M., & Hallahan, A. R. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.01.007 · Cited by 335 · see citing works
Takai, H., Kanematsu, M., Yano, K., Tsuda, E., Higashio, K., Ikeda, K., Watanabe, K., & Yamada, Y. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.42.27091 · Cited by 299 · see citing works
Chenu, C., Pfeilschifter, J., Mundy, G. R., & Roodman, G. D. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.15.5683 · Cited by 295 · see citing works
Yoo, J., Ghiassi, M., Jirmanova, L., Balliet, A. G., Hoffman‐Liebermann, B., Fornace, A. J., Liebermann, D. A., Böttinger, E. P., & Roberts, A. B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307869200 · Cited by 261 · see citing works
Akiyama, T., Bouillet, P., Miyazaki, T., Kadono, Y., Chikuda, H., Chung, U., Fukuda, A., Hikita, A., Seto, H., Okada, T., et al. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg635 · Cited by 241 · see citing works
Dual role for TGF-?1 in apoptosis
Sánchez‐Capelo, A. (2005) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2004.11.002 · Cited by 228 · see citing works
Edlund, S., Bu, S., Schuster, N., Aspenström, P., Heuchel, R. L., Heldin, N., ten Dijke, P., Heldin, C., & Landström, M. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.02-03-0037 · Cited by 227 · see citing works
A role for TGFβ1 in osteoclast differentiation and survival
Fuller, K., Lean, J. M., Bayley, K. E., Wani, M. R., & Chambers, T. J. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.13.2445 · Cited by 199 · see citing works
Mohammad, K. S., Chen, C. G., Balooch, G., Stebbins, E. G., McKenna, C. R., Davis, H., Niewolna, M., Peng, X., Nguyen, D. H., Ionova-Martin, S. S., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005275 · Cited by 179 · see citing works
TGF-β coordinately activates TAK1/MEK/AKT/NFkB and SMAD pathways to promote osteoclast survival
Gingery, A., Bradley, E. W., Pederson, L. G., Ruan, M. M., Horwood, N. J., & Oursler, M. J. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.06.006 · Cited by 175 · see citing works
Reffey, S. B., Würthner, J., Parks, W. T., Roberts, A. B., & Duckett, C. S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100331200 · Cited by 147 · see citing works
Karsdal, M. A., Hjorth, P., Henriksen, K., Kirkegaard, T., Nielsen, K. L., Lou, H., Delaissé, J., & Foged, N. T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303905200 · Cited by 137 · see citing works
Upregulation of two BH3-only proteins, Bmf and Bim, during TGFβ-induced apoptosis
Ramjaun, A. R., Tomlinson, S., Eddaoudi, A., & Downward, J. (2006) · Oncogene · doi:10.1038/sj.onc.1209852 · Cited by 131 · see citing works
The p38 MAPK stress pathway as a tumor suppressor or more?
Loesch, M. (2008) · Frontiers in bioscience · doi:10.2741/2951 · Cited by 115 · see citing works
Ohgushi, M., Kuroki, S., Fukamachi, H., O’Reilly, L. A., Kuida, K., Strasser, A., & Yonehara, S. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.22.10017-10028.2005 · Cited by 102 · see citing works
Wildey, G. M., Patil, S. D., & Howe, P. H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211958200 · Cited by 97 · see citing works
Ramesh, S., Qi, X., Wildey, G. M., Robinson, J., Molkentin, J. D., Letterio, J. J., & Howe, P. H. (2008) · EMBO Reports · doi:10.1038/embor.2008.158 · Cited by 87 · see citing works
Karsdal, M. A., Fjording, M. S., Foged, N. T., Delaissé, J.-M., & Lochter, A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008738200 · Cited by 81 · see citing works
Induction of p53 and Bax during TGF-beta 1 initiated apoptosis in rat liver epithelial cells.
Teramoto, T., Kiss, A., & Thorgeirsson, S. (1998) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1006/bbrc.1998.9411 · Cited by 68 · see citing works
Death receptors, Fas and TRAIL receptors, are involved in human osteoclast apoptosis
Roux, S., Lambert-Comeau, P., Saint-Pierre, C., Lépine, M., Sawan, B., & Parent, J. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.05.092 · Cited by 67 · see citing works
Self-citationOsteoprotegerin decreases human osteoclast apoptosis by inhibiting the TRAIL pathway
Chamoux, E., Houde, N., L'Ériger, K., & Roux, S. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21430 · Cited by 65 · see citing works
Self-citationIdentification of the gene transcription and apoptosis mediated by TGF‐β‐Smad2/3‐Smad4 signaling
Yu, J., Zhang, L., Chen, A., Xiang, G., Wang, Y., Wu, J., Mitchelson, K. R., Cheng, J., & Zhou, Y. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21325 · Cited by 59 · see citing works
The death receptor DR5 is involved in TRAIL-mediated human osteoclast apoptosis
Colucci, S. C., Brunetti, G., Cantatore, F. P., Oranger, A., Mori, G., Pignataro, P., Tamma, R., Grassi, F. R., Zallone, A. Z., & Grano, M. (2007) · APOPTOSIS · doi:10.1007/s10495-007-0095-3 · Cited by 58 · see citing works
Zheng, M., Fan, Y., Wysocki, S. J., Lau, A. T., Robertson, T., Beilharz, M. W., Wood, D., & Papadimitriou, J. M. (1994) · PubMed Central · Cited by 54 · see citing works
Osteopetrosis-like phenotype in latent TGF-β binding protein 3 deficient mice
Dabovic, B., Levasseur, R., Zambuto, L., Chen, Y., Karsenty, G., & Rifkin, D. B. (2005) · Bone · doi:10.1016/j.bone.2005.02.021 · Cited by 52 · see citing works
Transforming growth factor-β enables NFATc1 expression during osteoclastogenesis
Fox, S. W., Evans, K. E., & Lovibond, A. C. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.11.120 · Cited by 35 · see citing works
Effects of transforming growth factor‐β on long‐term human cord blood monocyte cultures
Orcel, P., Bielakoff, J., & de Vernejoul, M. C. (1990) · Journal of Cellular Physiology · doi:10.1002/jcp.1041420211 · Cited by 15 · see citing works
TRAIL Is Involved in Human Osteoclast Apoptosis
Brunetti, G., Oranger, A., Mori, G., Tamma, R., Benedetto, A. D., Pignataro, P., Grassi, F. R., Zallone, A. Z., Grano, M., & Colucci, S. C. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1402.011 · Cited by 13 · see citing works
TGF-β Isoform and Receptor Expression in Giant Cell Tumor and Giant Cell Lesions of Bone
Franchi, A., Benvenuti, S., Masi, L., Malentacchi, C., Arganini, L., Brandi, M. L., & Santucci, M. (2001) · Applied immunohistochemistry & molecular morphology · doi:10.1097/00129039-200106000-00010 · Cited by 9 · see citing works
Good (1996) · doi:10.1002/(sici)1097-4652(199609)168:3
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Physiological Bone Remodeling: Systemic Regulation and Growth Factor Involvement
Siddiqui, J. A., & Partridge, N. C. (2016) · Physiology · doi:10.1152/physiol.00061.2014 · Cited by 546 · see citing works
Bone remodeling: an operational process ensuring survival and bone mechanical competence
Bolamperti, S., Villa, I., & Rubinacci, A. (2022) · Bone Research · doi:10.1038/s41413-022-00219-8 · Cited by 482 · see citing works
Wu, M., Wu, S., Chen, W., & Li, Y.-P. (2024) · Cell Research · doi:10.1038/s41422-023-00918-9 · Cited by 445 · see citing works
Roles of Mitogen-Activated Protein Kinases in Osteoclast Biology
Lee, K., Seo, I., Choi, M. H., & Jeong, D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103004 · Cited by 251 · see citing works
Regulation of Bim in Health and Disease
Sionov, R. V., Vlahopoulos, S., & Granot, Z. (2015) · Oncotarget · doi:10.18632/oncotarget.5492 · Cited by 225 · see citing works
Targeting polymer therapeutics to bone
Low, S. A., & Kopec̆ek, J. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2012.01.012 · Cited by 158 · see citing works
Cytokine-mediated immunomodulation of osteoclastogenesis
Zhou, P., Zheng, T., & Zhao, B. (2022) · Bone · doi:10.1016/j.bone.2022.116540 · Cited by 144 · see citing works
Malhotra, A., Pelletier, M. H., Yu, Y. Y., & Walsh, W. R. (2012) · Archives of Orthopaedic and Trauma Surgery · doi:10.1007/s00402-012-1641-1 · Cited by 130 · see citing works
Jann, J., Gascon, S., Roux, S., & Faucheux, N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207597 · Cited by 129 · see citing works
Self-citationNew Insights Into Osteoclast Biology
McDonald, M. M., Kim, A. S., Mulholland, B. S., & Rauner, M. (2021) · JBMR Plus · doi:10.1002/jbm4.10539 · Cited by 116 · see citing works
Regulation of bone homeostasis: signaling pathways and therapeutic targets
Wu, Z., Li, W., Jiang, K., Lin, Z., Qian, C., Wu, M., Xia, Y., Li, N., Zhang, H., Xiao, H.-X., et al. (2024) · MedComm · doi:10.1002/mco2.657 · Cited by 115 · see citing works
Xia, Y., Inoue, K., Du, Y., Baker, S. J., Reddy, E. P., Greenblatt, M. B., & Zhao, B. (2022) · Nature Communications · doi:10.1038/s41467-022-31475-1 · Cited by 110 · see citing works
Molecular signaling mechanisms behind polyphenol-induced bone anabolism
Torre, E. (2017) · Phytochemistry Reviews · doi:10.1007/s11101-017-9529-x · Cited by 104 · see citing works
The Rising Era of “Immunoporosis”: Role of Immune System in the Pathophysiology of Osteoporosis
Srivastava, R., & Sapra, L. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s351918 · Cited by 79 · see citing works
Mechanisms of Spontaneous Resolution of Acute Gouty Inflammation
Steiger, S., & Harper, J. L. (2013) · Current Rheumatology Reports · doi:10.1007/s11926-013-0392-5 · Cited by 71 · see citing works
Ameln, A. K., Muschter, A., Mamlouk, S., Kalucka, J. M., Prade, I., Franke, K., Rezaei, M., Poitz, D. M., Breier, G., & Wielockx, B. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-3838 · Cited by 70 · see citing works
The Polycomb Group Protein Bmi-1 Is Essential for the Growth of Multiple Myeloma Cells
Jagani, Z., Wiederschain, D., Loo, A. T., He, D., Mosher, R. E., Fordjour, P., Monahan, J. E., Morrissey, M., Yao, Y.-M., Christoph Lengauer, C., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4229 · Cited by 70 · see citing works
Genetics in Endocrinology: Autosomal dominant osteopetrosis revisited: lessons from recent studies
Bollerslev, J., Henriksen, K., Nielsen, M. F., Brixen, K., & Hul, W. V. (2013) · European Journal of Endocrinology · doi:10.1530/eje-13-0136 · Cited by 69 · see citing works
The adaptor protein p62/SQSTM1 in osteoclast signaling pathways
McManus, S., & Roux, S. (2012) · Journal of Molecular Signaling · doi:10.1186/1750-2187-7-1 · Cited by 68 · see citing works
Self-citationCash, T. P., Gruber, J. J., Hartman, T. R., Henske, E. P., & Simon, M. C. (2011) · Oncogene · doi:10.1038/onc.2010.628 · Cited by 59 · see citing works
Li, M., Chen, X., Yan, J., Zhou, L., Wang, Y., He, F., Lin, J., Zhu, C., Pan, G., Yu, J., et al. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.03.003 · Cited by 51 · see citing works
The Molecular Mechanisms of Regulatory T Cell Immunosuppression
Pandiyan, P., Zheng, L., & Lenardo, M. J. (2011) · Frontiers in Immunology · doi:10.3389/fimmu.2011.00060 · Cited by 50 · see citing works
A dual role of TGF-β in human osteoclast differentiation mediated by Smad1 versus Smad3 signaling
Lee, B., Oh, Y., Jo, S., Kim, T., & Ji, J. D. (2018) · Immunology Letters · doi:10.1016/j.imlet.2018.12.003 · Cited by 50 · see citing works
Garcia, V. G., da Conceição, J. M., Fernandes, L. A., de Almeida, J. M., Nagata, M. J. H., Bosco, Á. F., & Theodoro, L. H. (2012) · Lasers in Medical Science · doi:10.1007/s10103-012-1068-5 · Cited by 50 · see citing works
Positive and negative regulators of osteoclast apoptosis
Soysa, N. S., & Alles, N. (2019) · Bone Reports · doi:10.1016/j.bonr.2019.100225 · Cited by 49 · see citing works
A mechanobiological model of orthodontic tooth movement
Schepdael, A. V., Sloten, J. V., & Geris, L. (2012) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-012-0396-5 · Cited by 48 · see citing works
General analysis of mathematical models for bone remodeling
Zumsande, M., Stiefs, D., Siegmund, S., & Groß, T. (2010) · Bone · doi:10.1016/j.bone.2010.12.010 · Cited by 47 · see citing works
Zhao, H., Zhang, J., Shao, H., Liu, J., Jin, M., Chen, J., & Huang, Y. (2017) · Molecules and Cells · doi:10.14348/molcells.2017.2303 · Cited by 44 · see citing works
C5aR1 interacts with TLR 2 in osteoblasts and stimulates the osteoclast‐inducing chemokine CXCL 10
Mödinger, Y., Rapp, A. E., Pázmándi, J., Vikman, A., Holzmann, K., Haffner‐Luntzer, M., Huber-Lang, M. S., & Ignatius, A. A. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13873 · Cited by 41 · see citing works
The Effects of TGF-β Signaling on Cancer Cells and Cancer Stem Cells in the Bone Microenvironment
Futakuchi, M., Lami, K., Tachibana, Y., Yamamoto, Y., Furukawa, M., & Fukuoka, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205117 · Cited by 40 · see citing works
Platelet‐rich plasma impairs osteoclast generation from human precursors of peripheral blood
Cenni, E., Avnet, S., Fotia, C., Salerno, M., & Baldini, N. (2010) · Journal of Orthopaedic Research® · doi:10.1002/jor.21073 · Cited by 39 · see citing works
Zhao, H., Zhang, J., Shao, H., Liu, J., Jin, M., Chen, J., & Huang, Y. (2017) · Molecules and Cells · doi:10.14348/molcells.2017.1303 · Cited by 38 · see citing works
Role of TGF-β in a Mouse Model of High Turnover Renal Osteodystrophy
Liu, S., Song, W., Boulanger, J., Tang, W., Sabbagh, Y., Kelley, B., Gotschall, R. R., Ryan, S., Phillips, L. A., Malley, K., et al. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2120 · Cited by 35 · see citing works
MicroRNAs Are Critical Regulators of Osteoclast Differentiation
Hrdlicka, H. C., Lee, S., & Delany, A. M. (2019) · Current Molecular Biology Reports · doi:10.1007/s40610-019-0116-3 · Cited by 35 · see citing works
Tong, D., Qu, H., Meng, X., Jiang, Y., LIU, D., Ye, S., CHEN, H., Jin, Y., Fu, S., & Geng, J. (2014) · Oncology Reports · doi:10.3892/or.2014.3295 · Cited by 32 · see citing works
Different Effects of Fluoride Exposure on the Three Major Bone Cell Types
Jiang, N., Guo, F., Sun, B., Zhang, X., & Xu, H. J. (2019) · Biological Trace Element Research · doi:10.1007/s12011-019-01684-9 · Cited by 29 · see citing works
Fowler, T. W., Kamalakar, A., Akel, N. S., Kurten, R. C., Suva, L. J., & Gaddy, D. (2015) · Journal of Cell Science · doi:10.1242/jcs.157834 · Cited by 28 · see citing works
Zhu, S.-Y., Zhou, J., & Xie, Z.-G. (2024) · Immunity, Inflammation and Disease · doi:10.1002/iid3.70011 · Cited by 24 · see citing works
Matsubara, R., Kukita, T., Ichigi, Y., Takigawa, I., Qu, P., Funakubo, N., Miyamoto, H., Nonaka, K., & Kukita, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047930 · Cited by 20 · see citing works
Egg White Ovotransferrin Attenuates RANKL-Induced Osteoclastogenesis and Bone Resorption
Shang, N., & Wu, J. (2019) · Nutrients · doi:10.3390/nu11092254 · Cited by 23 · see citing works
Gene expression profile in osteoclasts from patients with Paget's disease of bone
Michou, L., Chamoux, E., Couture, J., Morissette, J., Brown, J. P., & Roux, S. (2009) · Bone · doi:10.1016/j.bone.2009.11.012 · Cited by 23 · see citing works
Self-citationBreast cancer cells inhibit spontaneous and bisphosphonate-induced osteoclast apoptosis
Hussein, O., Tiedemann, K., & Komarova, S. V. (2010) · Bone · doi:10.1016/j.bone.2010.09.006 · Cited by 21 · see citing works
Immunology of Gut-Bone Signaling
Collins, F. L., Schepper, J. D., Rios‐Arce, N. D., Steury, M. D., Kang, H. J., Mallin, H., Schoenherr, D. T., Camfield, G., Chishti, S., McCabe, L. R., et al. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-66653-2_5 · Cited by 21 · see citing works
Zhang, B., Dai, J., Wang, H., Wei, H., Zhao, J., Guo, Y., & Fan, K. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.08.149 · Cited by 21 · see citing works
Schierano, G., Canuto, R. A., von Degerfeld, M. M., Navone, R., Peirone, B., Preti, G., & Muzio, G. (2021) · Materials · doi:10.3390/ma14092185 · Cited by 20 · see citing works
Prostaglandin D2 induces apoptosis of human osteoclasts through ERK1/2 and Akt signaling pathways
Li, Y., Haroun, S., Parent, J., & de Brum-Fernandes, A. J. (2013) · Bone · doi:10.1016/j.bone.2013.12.011 · Cited by 20 · see citing works
Li, Y., Durand, M., Jacob, M. C. L., Hogan, P., McManus, S., Roux, S., & de Brum-Fernandes, A. J. (2012) · Bone · doi:10.1016/j.bone.2012.06.003 · Cited by 19 · see citing works
Self-citationROSS, D. S., Mehta, K., & Cabal, A. (2016) · Bulletin of Mathematical Biology · doi:10.1007/s11538-016-0229-2 · Cited by 18 · see citing works
Akiyama, T., & Tanaka, S. (2011) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-011-0126-1 · Cited by 17 · see citing works
Jörg, D. J., Fuertinger, D. H., Cherif, A., Bushinsky, D. A., Mermelstein, A., Raimann, J. G., & Kotanko, P. (2022) · eLife · doi:10.7554/elife.76228 · Cited by 15 · see citing works
Wu, H. C., Yin, G., Pu, X., Wang, J., Liao, X., & Huang, Z. (2022) · ACS Applied Bio Materials · doi:10.1021/acsabm.2c00264 · Cited by 15 · see citing works
Rahaman, S. N., Lishadevi, M., & Anandasadagopan, S. K. (2025) · Phytotherapy Research · doi:10.1002/ptr.8455 · Cited by 15 · see citing works
Baratchart, E., Lo, C.-H., Lynch, C., & Basanta, D. (2021) · bioRxiv · doi:10.1371/journal.pcbi.1009839 · Cited by 14 · see citing works
McManus, S., Chamoux, E., Bisson, M., & Roux, S. (2011) · APOPTOSIS · doi:10.1007/s10495-011-0662-5 · Cited by 14 · see citing works
Self-citationKabashima, H., Sakai, T., Mizobe, K., Nakamuta, H., Kurita, K., & Terada, Y. (2013) · Journal of Oral Science · doi:10.2334/josnusd.55.363 · Cited by 13 · see citing works
Opposite Function of ERα and ERβ in Controlling 17β-Estradiol-mediated Osteogenesis in Osteoblasts
Wang, Y., Li, M., Zhang, H., Tang, M., Guo, C., Deng, A., Chen, Y., & Xiao, L. (2016) · Archives of Medical Research · doi:10.1016/j.arcmed.2016.07.002 · Cited by 11 · see citing works
Piszczorowicz, Ł., Król, D., & Dyląg, S. (2020) · Journal of Transfusion Medicine · doi:10.5603/jtm.2020.0004 · Cited by 11 · see citing works
The Role of Oral and Gut Microbiota in Bone Health: Insights from Bacterial Extracellular Vesicles
Liang, P., Chen, X., Su, Z., Luo, Y., Wang, T., Jiang, L., Guo, L., & Luo, T. (2025) · Microorganisms · doi:10.3390/microorganisms13102254 · Cited by 10 · see citing works
Wang, L., Tian, Y., Liu, M., He, Z., Xiao, Y., Yuan, X. H., & Zhang, Q. (2022) · Journal of Oral Rehabilitation · doi:10.1111/joor.13360 · Cited by 8 · see citing works
Association of SMAD2 polymorphisms with bone mineral density in postmenopausal Korean women
Kim, B., Hwang, J. Y., Han, B. G., Lee, J., Lee, J., Park, E. K., Lee, S. H., Chung, Y. E., Kim, G. S., Kim, S.-Y., et al. (2010) · Osteoporosis International · doi:10.1007/s00198-010-1450-8 · Cited by 8 · see citing works
Kylmäoja, E., Nakamura, M., Kokkonen, H. E., Ronkainen, V., Lehenkari, P. P., & Tuukkanen, J. (2018) · Heliyon · doi:10.1016/j.heliyon.2018.e00621 · Cited by 8 · see citing works
Effects of TGF‑β1 on the migration and morphology of RAW264.7 cells in vitro
Ueta, M., Takaoka, K., Yamamura, M., Maeda, H., Tamaoka, J., Nakano, Y., Noguchi, K., & Kishimoto, H. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.10662 · Cited by 7 · see citing works
Chen, Z., Yang, G., Su, W., He, S., & Wang, Y.-W. (2024) · European Spine Journal · doi:10.1007/s00586-024-08553-7 · Cited by 6 · see citing works
Shahrani, M. M. A., Abohassan, M., Alshahrani, M. Y., Gahtani, R. M., & Rajagopalan, P. (2025) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.151225 · Cited by 6 · see citing works
Kim, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015342 · Cited by 6 · see citing works
A novel role for TGF-β1 in bone remodeling
Nishimura, R. (2009) · IBMS BoneKEy · doi:10.1138/20090409 · Cited by 5 · see citing works
Bär, I., Ast, V., Meyer, D., König, R., Rauner, M., Hofbauer, L. C., & Müller, J. P. (2020) · Cells · doi:10.3390/cells9112443 · Cited by 5 · see citing works
Postmenopausal Osteoporosis: A Mini Review
Shuai, Y., Zhang, Z., Guo, T., Yang, R., Lei, J., & Liu, W. (2019) · EMJ Rheumatology · doi:10.33590/emjrheumatol/10311765 · Cited by 5 · see citing works
Хвисюк, О. М., Babalian, V. O., PAVLOV, S. B., & Pavlova, G. B. (2020) · Wiadomości Lekarskie · doi:10.36740/wlek202002110 · Cited by 4 · see citing works
Carroll, M., Alliston, T. N., & Dole, N. S. (2023) · Current Osteoporosis Reports · doi:10.1007/s11914-023-00802-w · Cited by 4 · see citing works
MODEL-BASED ANALYSIS OF IGF-1 EFFECT ON OSTEOBLAST AND OSTEOCLAST REGULATION IN BONE TURNOVER
Lee, W., & Okos, M. R. (2016) · Journal of Biological Systems · doi:10.1142/s0218339016500042 · Cited by 4 · see citing works
Extension of Generalized Modeling and Application to Problems from Cell Biology
Zumsande, M. (2011) · Qucosa (Saxon State and University Library Dresden) · Cited by 3 · see citing works
Abdelmagid, S. M., Zajac, A. L., Salhab, I., & Nah, H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.01.321976 · Cited by 3 · see citing works
Ross, F. P. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-381978-9.10018-6 · Cited by 2 · see citing works
Development of Novel Models for Studying Osteoclasts
Thudium, C. S. (2014) · Lund University Publications (Lund University) · Cited by 2 · see citing works
The Potential Role of Integrin Regulation by Par6 in TGF-beta-induced Apoptosis
Avery-Cooper, G. (2011) · The Atrium (University of Guelph)
The Molecular Mechanisms of Regulatory T cell Immunosuppression
(2013) · Frontiers research topics · doi:10.3389/978-2-88919-093-5
Clinical and basic research papers – October 2009
Ferrari, S., Seeman, E., Deng, H., Little, D. G., & Matsumoto, T. (2009) · IBMS BoneKEy · doi:10.1138/20090398
Babalian, V. O., Pavlov, S., & Khvysyuk, О. (2020) · ORTHOPAEDICS TRAUMATOLOGY and PROSTHETICS · doi:10.15674/0030-59872020188-98
A mechanistic model for genetic regulation of postmenopausal bone lossPreprint
Rattsev, I., Gabhann, F. M., Hertz, D. L., & Taylor, C. O. (2026) · medRxiv · doi:10.64898/2026.06.04.26354968
- Authors
- Houde, N., Chamoux, E., Bisson, M., & Roux, S.
- Affiliations
- Université de Sherbrooke (CA)
- Corresponding author
- Roux, Sophie
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 284
- Issue
- 35
- Pages
- 23397-23404
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2749113
- OpenAlex
- W2070825285
- Cited by
- 80
- References
- 39
- Citations by year
- 2025: 3 · 2024: 4 · 2023: 2 · 2022: 8 · 2021: 2 · 2020: 6 · 2019: 7 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 2 · 2014: 3 · 2013: 6 · 2012: 7
- FWCI
- 3.22
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- TGF-β1, osteoclast apoptosis, building information modeling, Smad signaling, caspase-9, p38 MAPK, ERK, Smad2, TGF-beta receptor, mitochondrial apoptosis, Bcl-2 family proteins
- MeSH terms
- Bcl-2-Like Protein 11, Cells, Cultured, Female, Humans, Membrane Proteins, Osteoclasts, Proto-Oncogene Proteins, Signal Transduction, Up-Regulation, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Apoptosis Regulatory Proteins, Caspase 8, Caspase 9, Transforming Growth Factor beta1
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review