The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene
Abstract
Mice homozygous for the recessive mutation osteopetrosis (op) on chromosome 3 have a restricted capacity for bone remodelling, and are severely deficient in mature macrophages and osteoclasts. Both cell populations originate from a common haemopoietic progenitor. As op/op mice are not cured by transplants of normal bone marrow cells, the defects in op/op mice may be associated with an abnormal haematopoietic microenvironment rather than with an intrinsic defect in haematopoietic progenitors. To investigate the molecular and biochemical basis of the defects caused by the op mutation, we established primary fibroblast cell lines from op/op mice and tested the ability of these cell lines to support the proliferation of macrophage progenitors. We show that op/op fibroblasts are defective in production of functional macrophage colony-stimulating factor (M-CSF), although its messenger RNA (Csfm mRNA) is present at normal levels. This defect in M-CSF production and the recent mapping of the Csfm structural gene near op on chromosome 3 suggest that op is a mutation within the Csfm gene itself. We have sequenced Csfm complementary DNA prepared from op/op fibroblasts and found a single base pair insertion in the coding region of the Csfm gene that generates a stop codon 21 base pairs downstream. Thus, the op mutation is within the Csfm coding region and we conclude that the pathological changes in this mutant result from the absence of M-CSF.
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M-CSF binds to its receptor (cFMS) present in osteoclast precursors, which stimulates their proliferation and inhibits their apoptosis.
“M-CSF binds to its receptor (cFMS) present in osteoclast precursors, which stimulates their proliferation and inhibits their apoptosis [82, 85].”
From Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells (2015) · cites this paper as [85]
Cites
Primer-Directed Enzymatic Amplification of DNA with a Thermostable DNA Polymerase
Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., & Erlich, H. A. (1988) · Science · doi:10.1126/science.2448875 · Cited by 17,719 · see citing works
Metcalf, D. (1989) · Nature · doi:10.1038/339027a0 · Cited by 1,023 · see citing works
CSF‐1—A mononuclear phagocyte lineage‐specific hemopoietic growth factor
Stanley, E. R., Guilbert, L. J., Tushinski, R. J., & Bartelmez, S. H. (1983) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240210206 · Cited by 516 · see citing works
Apparent role of the macrophage growth factor, CSF-1, in placental development
Pollard, J. W., Bartocci, A., Arceci, R. J., Orlofsky, A., Ladner, M. B., & Stanley, E. R. (1987) · Nature · doi:10.1038/330484a0 · Cited by 482 · see citing works
Osteopetrosis, a New Recessive Skeletal Mutation on Chromosome 12 of the Mouse
Marks, S. C., & LANE, P. W. (1976) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a108657 · Cited by 310 · see citing works
Wiktor-Jędrzejczak, W., Ahmed, A. A., Szczylik, C. A., & Skelly, R. R. (1982) · The Journal of Experimental Medicine · doi:10.1084/jem.156.5.1516 · Cited by 293 · see citing works
Ogawa, M., Nishikawa, S.-I., Ikuta, K., Yamamura, F., Naito, M., Takahashi, K., & Nishikawa, S.-I. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb02949.x · Cited by 281 · see citing works
Self-citationHuman CSF‐1: gene structure and alternative splicing of mRNA precursors.
Ladner, M. B., Martin, G. A., Noble, J. A., Nikoloff, D. M., Tal, R., Kawasaki, E. S., & White, T. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb02561.x · Cited by 228 · see citing works
The Molecular Control of Blood Cell Development
Sachs, L. (1987) · Science · doi:10.1126/science.3317831 · Cited by 227 · see citing works
Expression of the c-fms proto-oncogene and of the cytokine, CSF-1, during mouse embryogenesis
Regenstreif, L. J., & Rossant, J. (1989) · Developmental Biology · doi:10.1016/0012-1606(89)90319-9 · Cited by 188 · see citing works
Genetically Determined Murine Models of Immunodeficiency
Shultz, L. D., & Sidman, C. L. (1987) · Annual Review of Immunology · doi:10.1146/annurev.iy.05.040187.002055 · Cited by 178 · see citing works
Self-citationNishikawa, S., Ogawa, M., Nishikawa, S., Kunisada, T., & Kodama, H. (1988) · European Journal of Immunology · doi:10.1002/eji.1830181117 · Cited by 174 · see citing works
Self-citationcDNA cloning and expression of murine macrophage colony-stimulating factor from L929 cells.
Ladner, M. B., Martin, G. A., Noble, J. A., Wittman, V., Warren, M. K., McGrogan, M. P., & Stanley, E. R. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.18.6706 · Cited by 143 · see citing works
Growth of B-lymphocytes clones in semisolid culture is mitogen dependent.
Kincade, P. W., Ralph, P., & Moore, M. A. S. (1976) · The Journal of Experimental Medicine · doi:10.1084/jem.143.5.1265 · Cited by 110 · see citing works
Cloning and tissue-specific expression of mouse macrophage colony-stimulating factor mRNA.
Rajavashisth, T. B., Eng, R. D., Shadduck, R. K., Waheed, A., Ben-Avram, C. M., Shively, J. E., & Lusis, A. J. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.5.1157 · Cited by 97 · see citing works
Marks, S. C., Seifert, M. F., & McGuire, J. L. (1984) · Metabolic Bone Disease and Related Research · doi:10.1016/0221-8747(84)90027-4 · Cited by 57 · see citing works
Buchberg, A. M. (1989) · Genomics · doi:10.1016/0888-7543(89)90071-2 · Cited by 30 · see citing works
The murine M-CSF gene is localized on chromosome 3
Gisselbrecht, S., Sola, B., Fichelson, S., Bordereaux, D., Tambourin, P. E., Mattéi, M., Simon‐Chazottes, D., & Jl, G. (1989) · Blood · doi:10.1182/blood.v73.6.1742a.1742a · Cited by 29 · see citing works
Takahashi, M., Hirato, T., Takano, M., Nishida, T., Nagamura, K., Kamogashira, T., Nakai, S., & Hirai, Y. (1989) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(89)92683-1 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Obesity is associated with macrophage accumulation in adipose tissue
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319246 · Cited by 10,041 · see citing works
Monocyte and macrophage heterogeneity
Gordon, S., & Taylor, P. R. (2005) · Nature Reviews Immunology · doi:10.1038/nri1733 · Cited by 5,190 · see citing works
Osteoprotegerin: a novel secreted protein involved in the regulation of bone density.
Simonet, W. S., Lacey, D. L., Dunstan, C. R., Kelley, M., Chang, M.-S., Lüthy, R., Nguyen, H. Q., Wooden, S., Bennett, L., Boone, T., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80209-3 · Cited by 5,130 · see citing works
Yasuda, H., Shima, N., Nakagawa, N., Yamaguchi, K., Kinosaki, M., Mochizuki, S.-I., Tomoyasu, A., Yano, K., Goto, M., Murakami, A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.3597 · Cited by 4,224 · see citing works
Bone Resorption by Osteoclasts
Teitelbaum, S. L. (2000) · Science · doi:10.1126/science.289.5484.1504 · Cited by 3,962 · see citing works
OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph node organogenesis.
Kong, Y.-Y., Yoshida, H., Sarosi, I., Tan, H.-L., Timms, E., Capparelli, C., Morony, S., Oliveira-dos-Santos, A. J., Van, G., Itie, A., et al. (1999) · Nature · doi:10.1038/16852 · Cited by 3,351 · see citing works
Self-citationTakayanagi, H., Kim, S., Koga, T., Nishina, H., Isshiki, M., Yoshida, H., Saiura, A., Isobe, M., Yokochi, T., Inoue, J.-I., et al. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00369-6 · Cited by 2,701 · see citing works
Self-citationCytokines in the pathogenesis of rheumatoid arthritis
McInnes, I. B., & Schett, G. A. (2007) · Nature reviews. Immunology · doi:10.1038/nri2094 · Cited by 2,523 · see citing works
Cellular functions regulated by Src family kinases.
Thomas, S. M., & Brugge, J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.513 · Cited by 2,610 · see citing works
Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification.
Bucay, N., Sarosi, I., Dunstan, C. R., Morony, S., Tarpley, J., Capparelli, C., Scully, S., Tan, H. L., Xu, W., Lacey, D. L., et al. (1998) · Genes & Development · doi:10.1101/gad.12.9.1260 · Cited by 2,483 · see citing works
Suda, T., Takahashi, N., Udagawa, N., Jimi, E., Gillespie, M. T., & Martin, T. J. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0367 · Cited by 2,317 · see citing works
Davies, L. C., Jenkins, S. J., Allen, J. E., & Taylor, P. R. (2013) · Nature Immunology · doi:10.1038/ni.2705 · Cited by 2,096 · see citing works
Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells
Florencio-Silva, R., Sasso, G. R. D. S., Sasso-Cerri, E., Simões, M. J., & Cerri, P. S. (2015) · BioMed Research International · doi:10.1155/2015/421746 · Cited by 2,044 · see citing works
Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice
Soriano, P. M., Montgomery, C. A., Geske, R. S., & Bradley, A. (1991) · Cell · doi:10.1016/0092-8674(91)90499-o · Cited by 1,997 · see citing works
Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems
Takayanagi, H. (2007) · Nature Reviews Immunology · doi:10.1038/nri2062 · Cited by 1,878 · see citing works
Okuda, T., van Deursen, J., Hiebert, S. W., Grosveld, G., & Downing, J. R. (1996) · Cell · doi:10.1016/s0092-8674(00)80986-1 · Cited by 1,856 · see citing works
Functions of RANKL/RANK/OPG in bone modeling and remodeling
Boyce, B. F., & Xing, L. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.03.018 · Cited by 1,844 · see citing works
Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., & Werb, Z. (1998) · Cell · doi:10.1016/s0092-8674(00)81169-1 · Cited by 1,737 · see citing works
Genetic regulation of osteoclast development and function
Teitelbaum, S. L., & Ross, F. (2003) · Nature reviews genetics · doi:10.1038/nrg1122 · Cited by 1,733 · see citing works
Hsu, H., Lacey, D. L., Dunstan, C. R., Solovyev, I., Colombero, A., Timms, E., Tan, H.-L., Elliott, G., Kelley, M. J., Sarosi, I., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3540 · Cited by 1,636 · see citing works
Targeted Disruption of the Mouse Stat1 Gene Results in Compromised Innate Immunity to Viral Disease
Durbin, J. E., Hackenmiller, R., Simon, M. C., & Levy, D. E. (1996) · Cell · doi:10.1016/s0092-8674(00)81289-1 · Cited by 1,522 · see citing works
RANK is essential for osteoclast and lymph node development.
Dougall, W. C., Glaccum, M., Charrier, K., Rohrbach, K., Brasel, K., De Smedt, T., Daro, E., Smith, J., Tometsko, M. E., Maliszewski, C. R., et al. (1999) · Genes & Development · doi:10.1101/gad.13.18.2412 · Cited by 1,478 · see citing works
Cellular and molecular mechanisms of bone remodeling
Raggatt, L. J., & Partridge, N. C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.r109.041087 · Cited by 1,402 · see citing works
The molecular understanding of osteoclast differentiation
Asagiri, M., & Takayanagi, H. (2007) · Bone · doi:10.1016/j.bone.2006.09.023 · Cited by 1,363 · see citing works
BIOMECHANICAL AND MOLECULAR REGULATION OF BONE REMODELING
Robling, A. G., Castillo, A. B., & Turner, C. H. (2006) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.8.061505.095721 · Cited by 1,343 · see citing works
Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease
Prinz, M., & Priller, J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3722 · Cited by 1,329 · see citing works
TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signalingPreprint
Lomaga, M. A., Yeh, W., Sarosi, I., Duncan, G. S., Furlonger, C. L., Ho, A. P., Morony, S., Capparelli, C., Van, G. Y., Kaufman, S., et al. (1999) · Genes & Development · doi:10.1101/gad.13.8.1015 · Cited by 1,253 · see citing works
Yasuda, H., Shima, N., Nakagawa, N., Mochizuki, S.-I., Yano, K., Fujise, N., Sato, Y., Goto, M., Yamaguchi, K., Kuriyama, M., et al. (1998) · Endocrinology · doi:10.1210/endo.139.3.5837 · Cited by 1,201 · see citing works
Dai, X.-M., Ryan, G. R., Hapel, A. J., Dominguez, M. G., Russell, R. G., Kapp, S., Sylvestre, V., & Stanley, E. R. (2002) · Blood · doi:10.1182/blood.v99.1.111 · Cited by 1,184 · see citing works
Fantin, A., Vieira, J. M., Gestri, G., Denti, L., Schwarz, Q., Prykhozhij, S., Peri, F., Wilson, S. W., & Ruhrberg, C. (2010) · Blood · doi:10.1182/blood-2009-12-257832 · Cited by 1,153 · see citing works
Embryonic stem cell differentiation: emergence of a new era in biology and medicinePreprint
Keller, G. M. (2005) · Genes & Development · doi:10.1101/gad.1303605 · Cited by 1,144 · see citing works
Udagawa, N., Takahashi, N., Akatsu, T., Tanaka, H., Sasaki, T., Nishihara, T., Koga, T., Martin, T. J., & Suda, T. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.18.7260 · Cited by 1,048 · see citing works
Wang, Y., Szretter, K. J., Vermi, W., Gilfillan, S., Rossini, C., Cella, M., Barrow, A. D., Diamond, M. S., & Colonna, M. (2012) · Nature Immunology · doi:10.1038/ni.2360 · Cited by 1,011 · see citing works
Requirement for NF-κB in osteoclast and B-cell development
Franzoso, G., Carlson, L., Xing, L., Poljak, L., Shores, E. W., Brown, K. D., Leonardi, A., Tran, T., Boyce, B. F., & Siebenlist, U. (1997) · Genes & Development · doi:10.1101/gad.11.24.3482 · Cited by 996 · see citing works
Modulation of Osteoclast Differentiation
Suda, T., Takahashi, N., & Martin, T. J. (1992) · Endocrine Reviews · doi:10.1210/edrv-13-1-66 · Cited by 996 · see citing works
Osteogenesis and angiogenesis: The potential for engineering bone
Kanczler, J. M., & Oreffo, R. (2008) · European Cells and Materials · doi:10.22203/ecm.v015a08 · Cited by 984 · see citing works
Macrophages: Development and Tissue Specialization
Varol, C., Mildner, A., & Jung, S. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112220 · Cited by 962 · see citing works
Lieschke, G. J., Grail, D., HODGSON, G. S., Metcalf, D., Stanley, E. G., Cheers, C., Fowler, K., Basu, S., Zhan, Y., & Dunn, A. (1994) · Blood · doi:10.1182/blood.v84.6.1737.1737 · Cited by 956 · see citing works
Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment
Schett, G., & Gravallese, E. (2012) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2012.153 · Cited by 947 · see citing works
Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice
Säftig, P., Hunziker, E. B., Wehmeyer, O., Jones, S. J., BOYDE, A., Rommerskirch, W., Moritz, J. D., Schu, P. V., & FIGURA, K. V. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.23.13453 · Cited by 909 · see citing works
DC-STAMP is essential for cell–cell fusion in osteoclasts and foreign body giant cells
Yagi, M., Miyamoto, T., Sawatani, Y., Iwamoto, K., Hosogane, N., Fujita, N., Morita, K., Ninomiya, K., Suzuki, T., Miyamoto, K., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050645 · Cited by 890 · see citing works
Selective Ablation of Proliferating Microglial Cells Exacerbates Ischemic Injury in the Brain
Lalancette-Hébert, M., Gowing, G., Simard, A., Weng, Y. C., & Kriz, J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5360-06.2007 · Cited by 874 · see citing works
Generation of Lymphohematopoietic Cells from Embryonic Stem Cells in Culture
Nakano, T., Kodama, H., & Honjo, T. (1994) · Science · doi:10.1126/science.8066449 · Cited by 866 · see citing works
Raivich, G., Bohatschek, M., Kloss, C. U. A., Werner, A., Jones, L. L., & Kreutzberg, G. W. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00007-7 · Cited by 843 · see citing works
CSF-1 regulation of the wandering macrophage: complexity in action
Pixley, F. J., & Stanley, E. R. (2004) · Trends in Cell Biology · doi:10.1016/j.tcb.2004.09.016 · Cited by 807 · see citing works
Isolation of a novel cytokine from human fibroblasts that specifically inhibits osteoclastogenesis.
Tsuda, E., Goto, M., Mochizuki, S.-I., Yano, K., Kobayashi, F., Morinaga, T., & Higashio, K. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6603 · Cited by 787 · see citing works
Hoeffel, G., Wang, Y., Greter, M., See, P., Teo, P., Malleret, B., Leboeuf, M., Low, D., Oller, G., Almeida, F., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20120340 · Cited by 786 · see citing works
Osteoclast–osteoblast communication
Matsuo, K., & Irie, N. (2008) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2008.03.027 · Cited by 780 · see citing works
Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin.
Mizuno, A., Amizuka, N., Irie, K., Murakami, A., Fujise, N., Kanno, T., Sato, Y., Nakagawa, N., Yasuda, H., Mochizuki, S.-I., et al. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.8697 · Cited by 775 · see citing works
Interleukin‐6 deficient mice are protected from bone loss caused by estrogen depletion.
Poli, V., Balena, R. F., Fattori, E., Markatos, A., Yamamoto, M., Tanaka, H., Ciliberto, G., Rodan, G. A., & Costantini, F. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06368.x · Cited by 745 · see citing works
Expression and function of c-kit in hemopoietic progenitor cells.
Ogawa, M., Matsuzaki, Y., Nishikawa, S., Hayashi, S., Kunisada, T., Sudo, T., Kina, T., Nakauchi, H., & Nishikawa, S. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.1.63 · Cited by 744 · see citing works
Self-citationEstrogen, cytokines, and pathogenesis of postmenopausal osteoporosis
Pacifici, R. (1996) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650110802 · Cited by 741 · see citing works
Osteoclast differentiation by RANKL and OPG signaling pathways
Udagawa, N., Koide, M., Nakamura, M., Nakamichi, Y., Yamashita, T., Uehara, S., Kobayashi, Y., Furuya, Y., Yasuda, H., Fukuda, C., et al. (2020) · Journal of Bone and Mineral Metabolism · doi:10.1007/s00774-020-01162-6 · Cited by 732 · see citing works
Osteoclasts: What Do They Do and How Do They Do It?
Teitelbaum, S. L. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.060834 · Cited by 730 · see citing works
Smith, J. D., Trogan, E., Ginsberg, M., Grigaux, C., Tian, J., & Miyata, M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.18.8264 · Cited by 721 · see citing works
Kenkre, J. E., & Bassett, J. H. D. (2018) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563218759371 · Cited by 719 · see citing works
Denosumab and bisphosphonates: Different mechanisms of action and effects
Baron, R., Ferrari, S., & Russell, R. G. G. (2010) · Bone · doi:10.1016/j.bone.2010.11.020 · Cited by 716 · see citing works
Arai, F., Miyamoto, T., Ohneda, O., Inada, T., Sudo, T., Brasel, K., Miyata, T., Anderson, D. M., & Suda, T. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.12.1741 · Cited by 693 · see citing works
Self-citationMacrophage heterogeneity in the context of rheumatoid arthritis
Udalova, I. A., Mantovani, A., & Feldmann, M. (2016) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2016.91 · Cited by 686 · see citing works
Toward a molecular understanding of skeletal development
Erlebacher, A., Filvaroff, E. H., Gitelman, S. E., & Derynck, R. (1995) · Cell · doi:10.1016/0092-8674(95)90487-5 · Cited by 683 · see citing works
Targeting macrophages in cancer immunotherapy
Duan, Z., & Luo, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00506-6 · Cited by 634 · see citing works
Pleiotropic effects of a null mutation in the c-fos proto-oncogene
Johnson, R. S., Spiegelman, B. M., & Papaioannou, V. E. (1992) · Cell · doi:10.1016/0092-8674(92)90592-z · Cited by 630 · see citing works
Naito, A., Azuma, S., Tanaka, S., Miyazaki, T., Takaki, S., Takatsu, K., Nakao, K., Nakamura, K., Katsuki, M., Yamamoto, T. S., et al. (1999) · Genes to Cells · doi:10.1046/j.1365-2443.1999.00265.x · Cited by 626 · see citing works
The cell biology of bone metabolism
Datta, H. K., Ng, W. F., Walker, J. A., Tuck, S. P., & Varanasi, S. S. (2008) · Journal of Clinical Pathology · doi:10.1136/jcp.2007.048868 · Cited by 614 · see citing works
Copeland, N. G., Gilbert, D. J., Cho, B. C., Donovan, P. J., Jenkins, N. A., Cosman, D. J., Anderson, D. M., Lyman, S. D., & Williams, D. E. (1990) · Cell · doi:10.1016/0092-8674(90)90298-s · Cited by 604 · see citing works
Biology of the RANKL–RANK–OPG System in Immunity, Bone, and Beyond
Walsh, M. C., & Choi, Y. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00511 · Cited by 599 · see citing works
A timeline of tumour-associated macrophage biology
Cassetta, L., & Pollard, J. W. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-022-00547-1 · Cited by 601 · see citing works
Engsig, M. T., Chen, Q.-J., Vu, T. H., Pedersen, A.-C., Therkidsen, B., Lund, L. R., Henriksen, K., Lenhard, T., Foged, N. T., Werb, Z., et al. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.4.879 · Cited by 596 · see citing works
Regulatory mechanisms of osteoblast and osteoclast differentiation.
Katagiri, T., & Takahashi, N. (2002) · Oral Diseases · doi:10.1034/j.1601-0825.2002.01829.x · Cited by 640 · see citing works
Mechanisms of Tooth Eruption and Orthodontic Tooth Movement
Wise, G. E., & King, G. J. (2008) · Journal of Dental Research · doi:10.1177/154405910808700509 · Cited by 581 · see citing works
Han, Y., You, X., Xing, W., Zhang, Z., & Zou, W. (2018) · Bone Research · doi:10.1038/s41413-018-0019-6 · Cited by 582 · see citing works
Mackarehtschian, K., Hardin, J. D., Moore, K., Boast, S., Goff, S. P., & Lemischka, I. R. (1995) · Immunity · doi:10.1016/1074-7613(95)90167-1 · Cited by 575 · see citing works
Tanaka, S., Takahashi, N., Udagawa, N., Tamura, T., Akatsu, T., Stanley, E. R., Kurokawa, T., & Suda, T. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116179 · Cited by 573 · see citing works
Regulation of NFATc1 in Osteoclast Differentiation
Kim, J. H., & Kim, N. (2014) · Journal of Bone Metabolism · doi:10.11005/jbm.2014.21.4.233 · Cited by 570 · see citing works
“[5-8] RANKL mediates biological effects in bone through its sole receptor, RANK.”
BackgroundCell biology of the osteoclast
Roodman, G. D. (1999) · Experimental Hematology · doi:10.1016/s0301-472x(99)00061-2 · Cited by 570 · see citing works
Osteoimmunology: Interactions of the Bone and Immune System
Lorenzo, J., Horowitz, M. C., & Choi, Y. (2008) · Endocrine Reviews · doi:10.1210/er.2007-0038 · Cited by 566 · see citing works
Cecchini, M. G., Dominguez, M. G., Mocci, S., Wetterwald, A., Felix, R., Fleisch, H. A., Chisholm, O., Hofstetter, W., Pollard, J. W., & Stanley, E. R. (1994) · Development · doi:10.1242/dev.120.6.1357 · Cited by 557 · see citing works
Injured sensory neuron–derived CSF1 induces microglial proliferation and DAP12-dependent pain
Guan, Z., Kuhn, J., Wang, X., Colquitt, B. M., Solórzano, C., Vaman, S., Guan, A. K., Evans-Reinsch, Z., Braz, J. M., Devor, M. G., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4189 · Cited by 554 · see citing works
Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice.
Boyce, B. F., Yoneda, T., Lowe, C., Soriano, P. M., & Mundy, G. R. (1992) · Journal of Clinical Investigation · doi:10.1172/jci116032 · Cited by 550 · see citing works
A Genetic Linkage Map of the Mouse: Current Applications and Future Prospects
Copeland, N. G., Jenkins, N. A., Gilbert, D. J., Eppig, J. T., Maltais, L. J., Miller, J. C., Dietrich, W. F., Weaver, A., Lincoln, S. E., Steen, R. G., et al. (1993) · Science · doi:10.1126/science.8211130 · Cited by 546 · see citing works
Immune microenvironment of gliomas
Gieryng, A., Pszczolkowska, D., Walentynowicz, K. A., Rajan, W. D., & Kaminska, B. (2017) · Laboratory Investigation · doi:10.1038/labinvest.2017.19 · Cited by 541 · see citing works
Osteopetrosis in mice lacking haematopoietic transcription factor PU.1
Tondravi, M. M., McKercher, S. R., Anderson, K., Erdmann, J. M., Quiroz, M. E., Maki, R. A., & Teitelbaum, S. L. (1997) · Nature · doi:10.1038/386081a0 · Cited by 537 · see citing works
An overview of the regulation of bone remodelling at the cellular level
Kular, J., Tickner, J. C., Chim, S. M., & Xu, J. (2012) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2012.03.021 · Cited by 536 · see citing works
Metcalf, D. (2008) · Blood · doi:10.1182/blood-2007-03-079681 · Cited by 527 · see citing works
The when and how of Src regulation
Cooper, J. A., & Howell, B. W. (1993) · Cell · doi:10.1016/0092-8674(93)90634-3 · Cited by 527 · see citing works
Manolagas, S. C. (2002) · Recent Progress in Hormone Research · doi:10.1210/rp.57.1.385 · Cited by 523 · see citing works
Lyman, S. D., James, L., Bos, T. V., de Vries, P., Brasel, K., Gliniak, B., Hollingsworth, L. T., Picha, K. S., McKenna, H. J., Splett, R. R., et al. (1993) · Cell · doi:10.1016/0092-8674(93)90325-k · Cited by 521 · see citing works
Regulation of Osteoclast Differentiation by Cytokine Networks
Amarasekara, D. S., Yun, H., Kim, S., Lee, N., Kim, H., & Rho, J. (2018) · Immune Network · doi:10.4110/in.2018.18.e8 · Cited by 518 · see citing works
Compston, J. E. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.419 · Cited by 515 · see citing works
Tolar, J., Teitelbaum, S. L., & Orchard, P. J. (2004) · New England Journal of Medicine · doi:10.1056/nejmra040952 · Cited by 496 · see citing works
Palmqvist, P., Persson, E., Conaway, H. H., & Lerner, U. H. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.6.3353 · Cited by 484 · see citing works
Developmental origin, functional maintenance and genetic rescue of osteoclasts
Jacome-Galarza, C. E., Percin, G. I., Muller, J. T., Mass, E., Lazarov, T., Eitler, J., Rauner, M., Yadav, V. K., Crozet, L., Bohm, M., et al. (2019) · Nature · doi:10.1038/s41586-019-1105-7 · Cited by 475 · see citing works
Postnatal mammary gland development requires macrophages and eosinophils
Gouon–Evans, V., Rothenberg, M. E., & Pollard, J. W. (2000) · Development · doi:10.1242/dev.127.11.2269 · Cited by 463 · see citing works
Stark, Z., & Savarirayan, R. (2009) · Orphanet Journal of Rare Diseases · doi:10.1186/1750-1172-4-5 · Cited by 463 · see citing works
Takahashi, N., Udagawa, N., & Suda, T. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0252 · Cited by 461 · see citing works
Peacock, M., Turner, C. H., Econs, M. J., & Foroud, T. (2002) · Endocrine Reviews · doi:10.1210/edrv.23.3.0464 · Cited by 461 · see citing works
The hematopoietic stem cell in its place
Adams, G. B., & Scadden, D. T. (2006) · Nature Immunology · doi:10.1038/ni1331 · Cited by 450 · see citing works
Hematopoietic regulators: redundancy or subtlety?
Metcalf, D. (1993) · Blood · doi:10.1182/blood.v82.12.3515.3515 · Cited by 450 · see citing works
Origin of microglia: current concepts and past controversies
Ginhoux, F., & Prinz, M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020537 · Cited by 446 · see citing works
Niida, S., Kaku, M., Amano, H., Yoshida, H., Kataoka, H., Nishikawa, S., Tanne, K., Maeda, N., Nishikawa, S., & Kodama, H. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.2.293 · Cited by 441 · see citing works
Self-citation
- Authors
- Yoshida, H., Hayashi, S.-I., Kunisada, T., Ogawa, M., Nishikawa, S., Okamura, H., Sudo, T., Shultz, L. D., & Nishikawa, S.-I.
- Affiliations
- Kumamoto University (JP)
- Jackson Laboratory (US)
- Venue
- Nature
- Published
- 1990-05
- Volume
- 345
- Issue
- 6274
- Pages
- 442-444
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2041138285
- Cited by
- 1,789
- References
- 19
- Citations by year
- 2026: 10 · 2025: 20 · 2024: 14 · 2023: 24 · 2022: 46 · 2021: 27 · 2020: 38 · 2019: 44 · 2018: 25 · 2017: 56 · 2016: 39 · 2015: 45 · 2014: 56 · 2013: 63 · 2012: 63
- FWCI
- 18.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Health Sciences › Medicine › Rheumatology › Osteomyelitis and Bone Disorders Research
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- osteopetrosis, macrophage colony-stimulating factor, mouse chromosome 3, macrophage deficiency, bone remodeling, stop codon, gene mapping
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Colony-Stimulating Factors, Genes, Mice, Mutant Strains, Molecular Sequence Data, Osteopetrosis, RNA, Messenger, Polymerase Chain Reaction, Macrophage Colony-Stimulating Factor, Mice
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