CoChat
Sign Up
Cited by 76Bone Metabolism and DiseasesBone health and osteoporosis researchBone and Dental Protein Studies

The osteoclast cytoskeleton – current understanding and therapeutic perspectives for osteoporosis

Open access
Blangy, Anne, Bompard, Guillaume, Guerit, David, Marie, Pauline, Maurin, Justine, Morel, Anne, Vives, Virginie·2020·Journal of Cell Science
DOI 10.1242/jcs.244798
Open this paper in CoChat — free accountOpen PDF

Abstract

Osteoclasts are giant multinucleated myeloid cells specialized for bone resorption, which is essential for the preservation of bone health throughout life. The activity of osteoclasts relies on the typical organization of osteoclast cytoskeleton components into a highly complex structure comprising actin, microtubules and other cytoskeletal proteins that constitutes the backbone of the bone resorption apparatus. The development of methods to differentiate osteoclasts in culture and manipulate them genetically, as well as improvements in cell imaging technologies, has shed light onto the molecular mechanisms that control the structure and dynamics of the osteoclast cytoskeleton, and thus the mechanism of bone resorption. Although essential for normal bone physiology, abnormal osteoclast activity can cause bone defects, in particular their hyper-activation is commonly associated with many pathologies, hormonal imbalance and medical treatments. Increased bone degradation by osteoclasts provokes progressive bone loss, leading to osteoporosis, with the resulting bone frailty leading to fractures, loss of autonomy and premature death. In this context, the osteoclast cytoskeleton has recently proven to be a relevant therapeutic target for controlling pathological bone resorption levels. Here, we review the present knowledge on the regulatory mechanisms of the osteoclast cytoskeleton that control their bone resorption activity in normal and pathological conditions.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1242/jcs.244798

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Osteoclasts adhere to bone by means of the sealing zone, a belt of densely packed microtubule-stabilized podosomes, and podosomes mediate adhesion via integrin αvβ3, the major osteoclast integrin.

    “Osteoclasts adhere to bone by means of the sealing zone, a belt of densely packed microtubule-stabilized podosomes (Figure 6). Podosomes mediate adhesion via integrin αvβ3, the major osteoclast integrin.”

    From Osteoclasts and Microgravity (2020) · cites this paper as [2]

  • The osteoclast cytoskeleton is made of four categories of filamentous structures and fulfills essential functions including cell adhesion, migration, contractility, division, vesicular transport, and bone resorption.

    “The osteoclast cytoskeleton is made of filamentous structures that belong to one of four categories: polarized actin filaments; polarized microtubules; non-polarized intermediate filaments; or non-polarized septin filaments. The cytoskeleton fulfills essential functions including cell adhesion, migration, contractility, division, vesicular transport, and bone resorption [2,3,4,5,6].”

    From Osteoclasts and Microgravity (2020) · cites this paper as [2]

  • In the center of the sealing zone, the osteoclast membrane differentiates into a ruffled border, where it secretes hydrochloric acid and proteases to dissolve hydroxyapatite crystals and bone matrix.

    “In the center of the sealing zone, the osteoclast membrane differentiates into a ruffled border, where it secretes hydrochloric acid and proteases (cathepsin-K, MMP9, and MMP14) to dissolve hydroxyapatite crystals and bone matrix, respectively [2].”

    From Osteoclasts and Microgravity (2020) · cites this paper as [2]

  • A number of physiopathological conditions are characterized by excessive osteoclast activity, including menopause, juvenile Paget's disease of bone, inflammatory joint diseases, bone cancers such as multiple myeloma, and glucocorticoid therapy.

    “a number of physiopathological conditions are characterized by excessive osteoclast activity. These include but are not limited to menopause, juvenile Paget’s disease of bone, inflammatory joint diseases, bone cancers such as multiple myeloma, and glucocorticoid therapy [1,2]”

    From Osteoclasts and Microgravity (2020) · cites this paper as [2]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 141

  1. Akatsu, T., Tamura, T., Takahashi, N., Udagawa, N., Tanaka, S., Sasaki, T., Yamaguchi, A., Nagata, N. and Suda, T. (1992). Preparation and characterization of a mouse osteoclast-like multinucleated cell population. J. Bone Miner. Res. 7, 1297-1306. doi:10.1002/jbmr.5650071109 · DOI
  2. Akisaka, T., Yoshida, H., Suzuki, R. and Takama, K. (2008). Adhesion structures and their cytoskeleton-membrane interactions at podosomes of osteoclasts in culture. Cell Tissue Res. 331, 625-641. doi:10.1007/s00441-007-0552-x · DOI
  3. Akisaka, T., Yoshida, H. and Takigawa, T. (2011). Differential distribution of posttranslationally modified microtubules in osteoclasts. J. Histochem. Cytochem. 59, 630-638. doi:10.1369/0022155411405334 · DOI
  4. Babb, S. G., Matsudaira, P., Sato, M., Correia, I. and Lim, S.-S. (1997). Fimbrin in podosomes of monocyte-derived osteoclasts. Cell Motil. Cytoskeleton 37, 308-325. doi:10.1002/(SICI)1097-0169(1997)37:4<308::AID-CM3>3.0.CO;2-0 · DOI
  5. Bai, X., Bowen, J. R., Knox, T. K., Zhou, K., Pendziwiat, M., Kuhlenbäumer, G., Sindelar, C. V. and Spiliotis, E. T. (2013). Novel septin 9 repeat motifs altered in neuralgic amyotrophy bind and bundle microtubules. J. Cell Biol. 203, 895-905. doi:10.1083/jcb.201308068 · DOI
  6. Batsir, S., Geiger, B. and Kam, Z. (2017). Dynamics of the sealing zone in cultured osteoclasts. Cytoskeleton (Hoboken) 74, 72-81. doi:10.1002/cm.21350 · DOI
  7. Bettis, T., Kim, B.-J. and Hamrick, M. W. (2018). Impact of muscle atrophy on bone metabolism and bone strength: implications for muscle-bone crosstalk with aging and disuse. Osteoporos. Int. 29, 1713-1720. doi:10.1007/s00198-018-4570-1 · DOI
  8. Bhuwania, R., Cornfine, S., Fang, Z., Krüger, M., Luna, E. J. and Linder, S. (2012). Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J. Cell. Sci. 125, 2300-2314. doi:10.1242/jcs.100032 · DOI
  9. Biosse Duplan, M., Zalli, D., Stephens, S., Zenger, S., Neff, L., Oelkers, J. M., Lai, F. P., Horne, W., Rottner, K. and Baron, R. (2014). Microtubule dynamic instability controls podosome patterning in osteoclasts through EB1, cortactin, and Src. Mol. Cell. Biol. 34, 16-29. doi:10.1128/MCB.00578-13 · DOI
  10. Blangy, A., Touaitahuata, H., Cres, G. and Pawlak, G. (2012). Cofilin activation during podosome belt formation in osteoclasts. PLoS ONE 7, e45909. doi:10. 1371/journal.pone.0045909 · DOI
  11. Brazier, H., Stephens, S., Ory, S., Fort, P., Morrison, N. and Blangy, A. (2006). Expression profile of RhoGTPases and RhoGEFs during RANKL-stimulated osteoclastogenesis: identification of essential genes in osteoclasts. J. Bone Miner. Res. 21, 1387-1398. doi:10.1359/jbmr.060613 · DOI
  12. Buckley, L. and Humphrey, M. B. (2018). Glucocorticoid-induced osteoporosis. N. Engl. J. Med. 379, 2547-2556. doi:10.1056/NEJMcp1800214 · DOI · Paper page
  13. Cervero, P., Wiesner, C., Bouissou, A., Poincloux, R. and Linder, S. (2018). Lymphocyte-specific protein 1 regulates mechanosensory oscillation of podosomes and actin isoform-based actomyosin symmetry breaking. Nat. Commun. 9, 515. doi:10.1038/s41467-018-02904-x · DOI
  14. Chellaiah, M. A., Soga, N., Swanson, S., McAllister, S., Alvarez, U., Wang, D., Dowdy, S. F. and Hruska, K. A. (2000). Rho-A is critical for osteoclast podosome organization, motility, and bone resorption. J. Biol. Chem. 275, 11993-12002. doi:10.1074/jbc.275.16.11993 · DOI
  15. Chellaiah, M. A., Ma, T. and Majumdar, S. (2018). L-plastin phosphorylation regulates the early phase of sealing ring formation by actin bundling process in mouse osteoclasts. Exp. Cell Res. 372, 73-82. doi:10.1016/j.yexcr.2018.09.014 · DOI
  16. Chellaiah, M. A., Moorer, M. C., Majumdar, S., Aljohani, H., Morley, S. C., Yingling, V. and Stains, J. P. (2020). L-Plastin deficiency produces increased trabecular bone due to attenuation of sealing ring formation and osteoclast dysfunction. Bone Res 8, 3. doi:10.1038/s41413-019-0079-2 · DOI
  17. Compston, J. E., McClung, M. R. and Leslie, W. D. (2019). Osteoporosis. Lancet 393, 364-376. doi:10.1016/S0140-6736(18)32112-3 · DOI · Paper page
  18. Coury, F., Peyruchaud, O. and Machuca-Gayet, I. (2019). Osteoimmunology of bone loss in inflammatory rheumatic diseases. Front Immunol 10, 679. doi:10. 3389/fimmu.2019.00679 · DOI
  19. Cremers, S., Drake, M. T., Ebetino, F. H., Bilezikian, J. P. and Russell, R. G. G. (2019). Pharmacology of bisphosphonates. Br. J. Clin. Pharmacol. 85, 1052-1062. doi:10.1111/bcp.13867 · DOI
  20. Croke, M., Ross, F. P., Korhonen, M., Williams, D. A., Zou, W. and Teitelbaum, S. L. (2011). Rac deletion in osteoclasts causes severe osteopetrosis. J. Cell Sci. 124, 3811-3821. doi:10.1242/jcs.086280 · DOI
  21. Croucher, P. I., McDonald, M. M. and Martin, T. J. (2016). Bone metastasis: the importance of the neighbourhood. Nat. Rev. Cancer 16, 373-386. doi:10.1038/ nrc.2016. · DOI
  22. Dent, E. W. (2020). Dynamic microtubules at the synapse. Curr. Opin. Neurobiol. 63, 9-14. doi:10.1016/j.conb.2020.01.003 · DOI
  23. Destaing, O., Saltel, F., Geḿinard, J.-C., Jurdic, P. and Bard, F. (2003). Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actin-green fluorescent protein. Mol. Biol. Cell 14, 407-416. doi:10. 1091/mbc.e02-07-0389 · DOI
  24. Destaing, O., Saltel, F., Gilquin, B., Chabadel, A., Khochbin, S., Ory, S. and Jurdic, P. (2005). A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 118, 2901-2911. doi:10.1242/jcs.02425 · DOI
  25. Destaing, O., Sanjay, A., Itzstein, C., Horne, W. C., Toomre, D., De Camilli, P. and Baron, R. (2008). The tyrosine kinase activity of c-Src regulates actin dynamics and organization of podosomes in osteoclasts. Mol. Biol. Cell 19, 394-404. doi:10.1091/mbc.e07-03-0227 · DOI
  26. Di Ceglie, I., van den Akker, G. G. H., Ascone, G., Ten Harkel, B., Häcker, H., van de Loo, F. A. J., Koenders, M. I., van der Kraan, P. M., de Vries, T. J., Vogl, T. et al. (2017). Genetic modification of ER-Hoxb8 osteoclast precursors using CRISPR/Cas9 as a novel way to allow studies on osteoclast biology. J. Leukoc. Biol. 101, 957-966. doi:10.1189/jlb.1AB0416-180RR · DOI
  27. Dogterom, M. and Koenderink, G. H. (2019). Actin-microtubule crosstalk in cell biology. Nat. Rev. Mol. Cell Biol. 20, 38-54. doi:10.1038/s41580-018-0067-1 · DOI
  28. Drissi, H. and Sanjay, A. (2016). The multifaceted osteoclast; far and beyond bone resorption. J. Cell. Biochem. 117, 1753-1756. doi:10.1002/jcb.25560 · DOI
  29. Eleniste, P. P. and Bruzzaniti, A. (2012). Focal adhesion kinases in adhesion structures and disease. J Signal Transduct 2012, 296450. doi:10.1155/2012/ 296450 · DOI
  30. Faccio, R., Teitelbaum, S. L., Fujikawa, K., Chappel, J., Zallone, A., Tybulewicz, V. L., Ross, F. P. and Swat, W. (2005). Vav3 regulates osteoclast function and bone mass. Nat. Med. 11, 284-290. doi:10.1038/nm1194 · DOI
  31. Ferrandez, Y., Zhang, W., Peurois, F., Akendengue, L., Blangy, A., Zeghouf, M. and Cherfils, J. (2017). Allosteric inhibition of the guanine nucleotide exchange factor DOCK5 by a small molecule. Sci. Rep. 7, 14409. doi:10.1038/s41598-017- 13619-2 · DOI · Paper page
  32. Florencio-Silva, R., Sasso, G. R., Sasso-Cerri, E., Simões, M. J. and Cerri, P. S. (2015). Biology of bone tissue: structure, function, and factors that influence bone cells. BioMed. Res. Int.2015, 1-17. doi:10.1155/2015/421746 · DOI · Paper page
  33. Fort, P. and Blangy, A. (2017). The evolutionary landscape of Dbl-like RhoGEF families: adapting eukaryotic cells to environmental signals. Genome Biol. Evol. 9, 1471-1486. doi:10.1093/gbe/evx100 · DOI
  34. Fuller, K., Ross, J. L., Szewczyk, K. A., Moss, R. and Chambers, T. J. (2010). Bone is not essential for osteoclast activation. PLoS ONE 5, e12837. doi:10.1371/ journal.pone.0012837 · DOI
  35. Gad, A., Lach, S., Crimaldi, L. and Gimona, M. (2008). Plectin deposition at podosome rings requires myosin contractility. Cell Motil. Cytoskeleton 65, 614-625. doi:10.1002/cm.20287 · DOI
  36. Georgess, D., Machuca-Gayet, I., Blangy, A. and Jurdic, P. (2014a). Podosome organization drives osteoclast-mediated bone resorption. Cell Adh Migr. 8, 191-204. doi:10.4161/cam.27840 · DOI
  37. Georgess, D., Mazzorana, M., Terrado, J., Delprat, C., Chamot, C., Guasch, R. M., Peŕez-Roger, I., Jurdic, P. and Machuca-Gayet, I. (2014b). Comparative transcriptomics reveals RhoE as a novel regulator of actin dynamics in bone- resorbing osteoclasts. Mol. Biol. Cell 25, 380-396. doi:10.1091/mbc.e13-07-0363 · DOI
  38. Gil-Henn, H., Destaing, O., Sims, N. A., Aoki, K., Alles, N., Neff, L., Sanjay, A., Bruzzaniti, A., De Camilli, P., Baron, R. et al. (2007). Defective microtubule- dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J. Cell Biol. 178, 1053-1064. doi:10.1083/jcb.200701148 · DOI
  39. Goldmann, W. H. (2018). Intermediate filaments and cellular mechanics: Intermediate filaments influence cell mechanics. Cell Biol. Int. 42, 132-138. doi:10.1002/cbin. 10879 · DOI
  40. Guerit, D., Marie, P., Morel, A., Maurin, J., Verollet, C., Raynaud-Messina, B., Urbach, S. and Blangy, A. (2019). Primary myeloid cell proteomics and transcriptomics: importance of β-tubulin isotypes for osteoclast function. J. Cell Sci. 133, jcs239772. doi:10.1242/jcs.239772 · DOI
  41. Guimbal, S., Morel, A., Gueŕit, D., Chardon, M., Blangy, A. and Vives, V. (2019). Dock5 is a new regulator of microtubule dynamic instability in osteoclasts. Biol. Cell 111, 271-283. doi:10.1111/boc.201900014 · DOI
  42. Guo, L., Chen, K., Yuan, J., Huang, P., Xu, X., Li, C., Qian, N., Qi, J., Shao, Z., Deng, L. et al. (2018). Estrogen inhibits osteoclasts formation and bone resorption via microRNA-27a targeting PPARγ and APC. J. Cell. Physiol. 234, 581-594. doi:10.1002/jcp.26788 · DOI
  43. Heimsath, E. G., Yim, Y.-I., Mustapha, M., Hammer, J. A. and Cheney, R. E. (2017). Myosin-X knockout is semi-lethal and demonstrates that myosin-X functions in neural tube closure, pigmentation, hyaloid vasculature regression, and filopodia formation. Sci. Rep. 7, 17354. doi:10.1038/s41598-017-17638-x · DOI
  44. Henderson, C. A., Gomez, C. G., Novak, S. M., Mi-Mi, L. and Gregorio, C. C. (2017). Overview of the Muscle Cytoskeleton. In Comprehensive Physiology (ed. R. Terjung), pp. 891-944.
  45. Horne, W. C., Neff, L., Chatterjee, D., Lomri, A., Levy, J. B. and Baron, R. (1992). Osteoclasts express high levels of pp6°c-src in association with intracellular membranes. J. Cell Biol. 119, 1003-1013. doi:10.1083/jcb.119.4.1003 · DOI
  46. 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). Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. USA 96, 3540-3545. doi:10.1073/pnas.96.7.3540 · DOI · Paper page
  47. Hussein, N. J., Mbimba, T., Al-Adlaan, A. A., Ansari, M. Y., Jaber, F. A., McDermott, S., Kasumov, T. and Safadi, F. F. (2019). A novel regulatory role of TRAPPC9 in L-plastin-mediated osteoclast actin ring formation. J. Cell. Biochem. 121, 284-298. doi:10.1002/jcb.29168 · DOI
  48. Ito, Y., Teitelbaum, S. L., Zou, W., Zheng, Y., Johnson, J. F., Chappel, J., Ross, F. P. and Zhao, H. (2010). Cdc42 regulates bone modeling and remodeling in mice by modulating RANKL/M-CSF signaling and osteoclast polarization. J. Clin. Invest. 120, 1981-1993. doi:10.1172/JCI39650 · DOI
  49. Itokowa, T., Zhu, M., Troiano, N., Bian, J., Kawano, T. and Insogna, K. (2011). Osteoclasts lacking Rac2 have defective chemotaxis and resorptive activity. Calcif. Tissue Int. 88, 75-86. doi:10.1007/s00223-010-9435-3 · DOI
  50. 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). Developmental origin, functional maintenance and genetic rescue of osteoclasts. Nature 568, 541-545. doi:10.1038/s41586-019-1105-7 · DOI · Paper page
  51. Janke, C. and Magiera, M. M. (2020). The tubulin code and its role in controlling microtubule properties and functions. Nat. Rev. Mol. Cell Biol. 21, 307-326. doi:10. 1038/s41580-020-0214-3 · DOI · Paper page
  52. Juanes, M. A., Isnardon, D., Badache, A., Brasselet, S., Mavrakis, M. and Goode, B. L. (2019). The role of APC-mediated actin assembly in microtubule capture and focal adhesion turnover. J. Cell Biol. 218, 3415-3435. doi:10.1083/ jcb.201904165 · DOI
  53. Kerber, M. L. and Cheney, R. E. (2011). Myosin-X: a MyTH-FERM myosin at the tips of filopodia. J. Cell Sci. 124, 3733-3741. doi:10.1242/jcs.023549 · DOI
  54. Klapproth, S., Bromberger, T., Tu ̈rk, C., Krüger, M. and Moser, M. (2019). A kindlin-3-leupaxin-paxillin signaling pathway regulates podosome stability. J. Cell Biol. 218, 3436-3454. doi:10.1083/jcb.201903109 · DOI
  55. Kobayakawa, M., Matsubara, T., Mizokami, A., Hiura, F., Takakura, N., Kokabu, S., Matsuda, M., Yasuda, H., Nakamura, I., Takei, Y. et al. (2019). Kif1c regulates osteoclastic bone resorption as a downstream molecule of p130Cas. Cell Biochem. Funct. 38, 300-308. doi:10.1002/cbf.3476 · DOI
  56. Lacey, D. L., Timms, E., Tan, H.-L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S. et al. (1998). Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165-176. doi:10.1016/S0092-8674(00)81569-X · DOI · Paper page
  57. Latorre, E., Kale, S., Casares, L., Gómez-Gonzaĺez, M., Uroz, M., Valon, L., Nair, R. V., Garreta, E., Montserrat, N., del Campo, A. et al. (2018). Active superelasticity in three-dimensional epithelia of controlled shape. Nature 563, 203-208. doi:10.1038/s41586-018-0671-4 · DOI
  58. Leduc, C. and Etienne-Manneville, S. (2015). Intermediate filaments in cell migration and invasion: the unusual suspects. Curr. Opin. Cell Biol. 32, 102-112. doi:10.1016/j.ceb.2015.01.005 · DOI
  59. Lee, B. S. (2018). Myosins in osteoclast formation and function. Biomolecules 8, 157. doi:10.3390/biom8040157 · DOI
  60. Li, J., Fukase, Y., Shang, Y., Zou, W., Mun ̃oz-Feĺix, J. M., Buitrago, L., van Agthoven, J., Zhang, Y., Hara, R., Tanaka, Y. et al. (2019). Novel pure αVβ3 integrin antagonists that do not induce receptor extension, prime the receptor, or enhance angiogenesis at low concentrations. ACS Pharmacol. Transl. Sci. 2, 387-401. doi:10.1021/acsptsci. · DOI
  61. 9b00041 · DOI
  62. Lin, T.-H., Yang, R.-S., Tu, H.-J., Liou, H.-C., Lin, Y.-M., Chuang, W.-J. and Fu, W.-M. (2017). Inhibition of osteoporosis by the αvβ3 integrin antagonist of rhodostomin variants. Eur. J. Pharmacol. 804, 94-101. doi:10.1016/j.ejphar.2017. 03.019 · DOI
  63. Linder, S. (2007). The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117. doi:10.1016/j.tcb.2007.01.002 · DOI
  64. Linder, S. and Wiesner, C. (2015). Tools of the trade: podosomes as multipurpose organelles of monocytic cells. Cell. Mol. Life Sci. 72, 121-135. doi:10.1007/ s00018-014-1731-z · DOI
  65. Lowell, C. A. and Soriano, P. (1996). Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev. 10, 1845-1857. doi:10.1101/gad. 10.15.1845 · DOI
  66. Madel, M.-B., Ibań ̃ez, L., Wakkach, A., de Vries, T. J., Teti, A., Apparailly, F. and Blin-Wakkach, C. (2019). Immune function and diversity of osteoclasts in normal and pathological conditions. Front. Immunol. 10, 1408. doi:10.3389/fimmu.2019. 01408 · DOI
  67. Magalhaes, J. K. R. S., Grynpas, M. D., Willett, T. L. and Glogauer, M. (2011). Deleting Rac1 improves vertebral bone quality and resistance to fracture in a murine ovariectomy model. Osteoporos. Int. 22, 1481-1492. doi:10.1007/s00198- 010-1355-6 · DOI
  68. Masi, L., Agnusdei, D., Bilezikian, J., Chappard, D., Chapurlat, R., Cianferotti, L., Devolgelaer, J.-P., El Maghraoui, A., Ferrari, S., Javaid, M. K. et al. (2015). Taxonomy of rare genetic metabolic bone disorders. Osteoporos. Int. 26, 2529-2558. doi:10.1007/s00198-015-3188-9 · DOI
  69. Matsubara, T., Kinbara, M., Maeda, T., Yoshizawa, M., Kokabu, S. and Takano Yamamoto, T. (2017). Regulation of osteoclast differentiation and actin ring formation by the cytolinker protein plectin. Biochem. Biophys. Res. Commun. 489, 472-476. doi:10.1016/j.bbrc.2017.05.174 · DOI
  70. Matsubara, T., Yaginuma, T., Addison, W. N., Fujita, Y., Watanabe, K., Yoshioka, I., Hikiji, H., Maki, K., Baron, R. and Kokabu, S. (2020). Plectin stabilizes microtubules during osteoclastic bone resorption by acting as a scaffold for Src and Pyk2. Bone 132, 115209. doi:10.1016/j.bone.2019.115209 · DOI
  71. Matsumoto, T., Nagase, Y., Hirose, J., Tokuyama, N., Yasui, T., Kadono, Y., Ueki, K., Kadowaki, T., Nakamura, K. and Tanaka, S. (2013). Regulation of bone resorption and sealing zone formation in osteoclasts occurs through protein kinase B-mediated microtubule stabilization. J. Bone Miner. Res. 28, 1191-1202. doi:10.1002/jbmr.1844 · DOI
  72. Maurin, J., Morel, A., Hassen-Khodja, C., Vives, V., Jurdic, P., Machuca-Gayet, I. and Blangy, A. (2018). Combined strategy of siRNA and osteoclast actin cytoskeleton automated imaging to identify novel regulators of bone resorption shows a non-mitotic function for anillin. Eur. J. Cell Biol. 97, 568-579. doi:10.1016/ j.ejcb.2018.10.002 · DOI
  73. McMichael, B. K., Kotadiya, P., Singh, T., Holliday, L. S. and Lee, B. S. (2006). Tropomyosin isoforms localize to distinct microfilament populations in osteoclasts. Bone 39, 694-705. doi:10.1016/j.bone.2006.04.031 · DOI
  74. McMichael, B. K., Cheney, R. E. and Lee, B. S. (2010). Myosin X regulates sealing zone patterning in osteoclasts through linkage of podosomes and microtubules. J. Biol. Chem. 285, 9506-9515. doi:10.1074/jbc.M109.017269 · DOI
  75. McMichael, B. K., Scherer, K. F., Franklin, N. C. and Lee, B. S. (2014). The RhoGAP activity of myosin IXB is critical for osteoclast podosome patterning, motility, and resorptive capacity. PLoS ONE 9, e87402. doi:10.1371/journal.pone. 0087402 · DOI
  76. Mersich, A. T., Miller, M. R., Chkourko, H. and Blystone, S. D. (2010). The formin FRL1 (FMNL1) is an essential component of macrophage podosomes. Cytoskeleton (Hoboken) 67, 573-585. doi:10.1002/cm.20468 · DOI
  77. Miryounesi, M., Nikfar, A., Changi-Ashtiani, M., Shahrooei, M., Dinmohammadi, H., Shahani, T., Zarvandi, S., Bahrami, T., Momenilandi, M. and Rokni-Zadeh, H. (2019). A novel homozygous LRRK1 stop gain mutation in a patient suspected with osteosclerotic metaphyseal dysplasia. Ann. Hum. Genet. 84, 102-106. doi:10.1111/ahg.12352 · DOI
  78. Miura, K., Jacques, K. M., Stauffer, S., Kubosaki, A., Zhu, K., Hirsch, D. S., Resau, J., Zheng, Y. and Randazzo, P. A. (2002). ARAP1. Mol. Cell 9, 109-119. doi:10.1016/S1097-2765(02)00428-8 · DOI
  79. Møller, A. M. J., Füchtbauer, E.-M., Brüel, A., Andersen, T. L., Borggaard, X. G., Pavlos, N. J., Thomsen, J. S., Pedersen, F. S., Delaisse, J.-M. and Søe, K. (2018). Septins are critical regulators of osteoclastic bone resorption. Sci. Rep. 8, 13016. doi:10.1038/s41598-018-31159-1 · DOI
  80. Mulari, M. T. K., Patrikainen, L., Kaisto, T., Metsikkö, K., Salo, J. J. and Väänänen, H. K. (2003). The architecture of microtubular network and Golgi orientation in osteoclasts-major differences between avian and mammalian species. Exp. Cell Res. 285, 221-235. doi:10.1016/S0014-4827(03)00033-8 · DOI
  81. Murphy, M. G., Cerchio, K., Stoch, S. A., Gottesdiener, K., Wu, M. and Recker, R. (2005). Effect of L-000845704, an alphaVbeta3 integrin antagonist, on markers of bone turnover and bone mineral density in postmenopausal osteoporotic women. J. Clin. Endocrinol. Metab. 90, 2022-2028. doi:10.1210/jc.2004-2126 · DOI
  82. Nagai, Y., Osawa, K., Fukushima, H., Tamura, Y., Aoki, K., Ohya, K., Yasuda, H., Hikiji, H., Takahashi, M., Seta, Y. et al. (2013). p130Cas, Crk-associated substrate, plays important roles in osteoclastic bone resorption: P130CAS REGULATES OSTEOCLASTIC BONE RESORPTION. J. Bone Miner. Res. 28, 2449-2462. doi:10.1002/jbmr.1936 · DOI
  83. Nakos, K., Rosenberg, M. and Spiliotis, E. T. (2019). Regulation of microtubule plus end dynamics by septin 9. Cytoskeleton (Hoboken) 76, 83-91. doi:10.1002/ cm.21488 · DOI
  84. Neugebauer, J., Heilig, J., Hosseinibarkooie, S., Ross, B. C., Mendoza-Ferreira, N., Nolte, F., Peters, M., Ho ̈lker, I., Hupperich, K., Tschanz, T. et al. (2018). Plastin 3 influences bone homeostasis through regulation of osteoclast activity. Hum. Mol. Genet. 27, 4249-4262. doi:10.1093/hmg/ddy318 · DOI
  85. Ng, P. Y., Brigitte Patricia Ribet, A. and Pavlos, N. J. (2019). Membrane trafficking in osteoclasts and implications for osteoporosis. Biochem. Soc. Trans. 47, 639-650. doi:10.1042/BST20180445 · DOI
  86. Oinuma, I., Kawada, K., Tsukagoshi, K. and Negishi, M. (2012). Rnd1 and Rnd3 targeting to lipid raft is required for p190 RhoGAP activation. Mol. Biol. Cell 23, 1593-1604. doi:10.1091/mbc.e11-11-0900 · DOI
  87. Okumura, S., Mizoguchi, T., Sato, N., Yamaki, M., Kobayashi, Y., Yamauchi, H., Ozawa, H., Udagawa, N. and Takahashi, N. (2006). Coordination of microtubules and the actin cytoskeleton is important in osteoclast function, but calcitonin disrupts sealing zones without affecting microtubule networks. Bone 39, 684-693. doi:10.1016/j.bone.2006.04.010 · DOI
  88. Ory, S., Brazier, H., Pawlak, G. and Blangy, A. (2008). Rho GTPases in osteoclasts: orchestrators of podosome arrangement. Eur. J. Cell Biol. 87, 469-477. doi:10.1016/j.ejcb.2008.03.002 · DOI
  89. Palagano, E., Menale, C., Sobacchi, C. and Villa, A. (2018). Genetics of osteopetrosis. Curr. Osteoporos Rep. 16, 13-25. doi:10.1007/s11914-018-0415-2 · DOI
  90. Panzer, L., Tru ̈be, L., Klose, M., Joosten, B., Slotman, J., Cambi, A. and Linder, S. (2016). The formins FHOD1 and INF2 regulate inter-and intra-structural contractility of podosomes. J. Cell. Sci. 129, 298-313. doi:10.1242/jcs.177691 · DOI
  91. Paterson, E. K. and Courtneidge, S. A. (2018). Invadosomes are coming: new insights into function and disease relevance. FEBS J. 285, 8-27. doi:10.1111/ febs.14123 · DOI
  92. Pickarski, M., Gleason, A., Bednar, B. and Duong, L. T. (2015). Orally active αvβ3 integrin inhibitor MK-0429 reduces melanoma metastasis. Oncol. Rep. 33, 2737-2745. doi:10.3892/or.2015.3910 · DOI
  93. Purev, E., Neff, L., Horne, W. C. and Baron, R. (2009). c-Cbl and Cbl-b act redundantly to protect osteoclasts from apoptosis and to displace HDAC6 from beta-tubulin, stabilizing microtubules and podosomes. Mol. Biol. Cell 20, 4021-4030. doi:10.1091/mbc.e09-03-0248 · DOI
  94. Rafiq, N. B. M., Nishimura, Y., Plotnikov, S. V., Thiagarajan, V., Zhang, Z., Shi, S., Natarajan, M., Viasnoff, V., Kanchanawong, P., Jones, G. E. et al. (2019). A mechano-signalling network linking microtubules, myosin IIA filaments and integrin-based adhesions. Nat. Mater. 18, 638-649. doi:10.1038/s41563-019- 0371-y · DOI
  95. Raynaud-Messina, B., Bracq, L., Dupont, M., Souriant, S., Usmani, S. M., Proag, A., Pingris, K., Soldan, V., Thibault, C., Capilla, F. et al. (2018). Bone degradation machinery of osteoclasts: An HIV-1 target that contributes to bone loss. Proc. Natl. Acad. Sci. USA 115, E2556-E2565. doi:10.1073/pnas.1713370115 · DOI
  96. Raynaud-Messina, B., Verollet, C. and Maridonneau-Parini, I. (2019). The osteoclast, a target cell for microorganisms. Bone 127, 315-323. doi:10.1016/j. bone.2019.06.023 · DOI
  97. Reznikov, N., Shahar, R. and Weiner, S. (2014). Bone hierarchical structure in three dimensions. Acta Biomater. 10, 3815-3826. doi:10.1016/j.actbio.2014.05.024 · DOI
  98. Rougerie, P., Miskolci, V. and Cox, D. (2013). Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton. Immunol. Rev. 256, 222-239. doi:10.1111/imr.12118 · DOI · Paper page
  99. Sakai, H., Chen, Y., Itokawa, T., Yu, K.-P., Zhu, M. L. and Insogna, K. (2006). Activated c-Fms recruits Vav and Rac during CSF-1-induced cytoskeletal remodeling and spreading in osteoclasts. Bone 39, 1290-1301. doi:10.1016/j. bone.2006.06.012 · DOI
  100. Saltel, F., Destaing, O., Bard, F., Eichert, D. and Jurdic, P. (2004). Apatite- mediated actin dynamics in resorbing osteoclasts. Mol. Biol. Cell 15, 5231-5241. doi:10.1091/mbc.e04-06-0522 · DOI · Paper page
  101. Sanjay, A., Houghton, A., Neff, L., DiDomenico, E., Bardelay, C., Antoine, E., Levy, J., Gailit, J., Bowtell, D., Horne, W. C. et al. (2001). Cbl associates with Pyk2 and Src to regulate Src kinase activity, alpha(v)beta(3) integrin-mediated signaling, cell adhesion, and osteoclast motility. J. Cell Biol. 152, 181-195. doi:10. 1083/jcb.152.1.181 · DOI
  102. Schmidt, S., Nakchbandi, I., Ruppert, R., Kawelke, N., Hess, M. W., Pfaller, K., Jurdic, P., Fassler, R. and Moser, M. (2011). Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J. Cell Biol. 192, 883-897. doi:10.1083/jcb.201007141 · DOI
  103. Seetharaman, S. and Etienne-Manneville, S. (2019). Microtubules at focal adhesions -a double-edged sword. J. Cell. Sci. 132, jcs232843. doi:10.1242/ jcs.232843 · DOI
  104. Segeletz, S., Danglot, L., Galli, T. and Hoflack, B. (2018). ARAP1 bridges actin dynamics and AP-3-dependent membrane traffic in bone-digesting osteoclasts. iScience 6, 199-211. doi:10.1016/j.isci.2018.07.019 · DOI
  105. Shemesh, M., Addadi, L. and Geiger, B. (2017). Surface microtopography modulates sealing zone development in osteoclasts cultured on bone. J. R. Soc. Interface 14, 20160958. doi:10.1098/rsif.2016.0958 · DOI
  106. Si, M., Goodluck, H., Zeng, C., Pan, S., Todd, E. M., Morley, S. C., Qin, X., Mohan, S. and Xing, W. (2018). LRRK1 regulation of actin assembly in osteoclasts involves serine 5 phosphorylation of L-plastin. J. Cell. Biochem. 119, 10351-10357. doi:10.1002/jcb.27377 · DOI
  107. Silver, I. A., Murrills, R. J. and Etherington, D. J. (1988). Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp. Cell Res. 175, 266-276. doi:10.1016/0014-4827(88)90191-7 · DOI
  108. Smith, C., Dolat, L., Angelis, D., Forgacs, E., Spiliotis, E. T. and Galkin, V. E. (2015). Septin 9 exhibits polymorphic binding to F-actin and inhibits myosin and cofilin activity. J. Mol. Biol. 427, 3273-3284. doi:10.1016/j.jmb.2015.07.026 · DOI
  109. Søe, K. and Delaisse, J.-M. (2017). Time-lapse reveals that osteoclasts can move across the bone surface while resorbing. J. Cell. Sci. 130, 2026-2035. doi:10. 1242/jcs.202036 · DOI
  110. Soriano, P., Montgomery, C., Geske, R. and Bradley, A. (1991). Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702. doi:10.1016/0092-8674(91)90499-O Spiliotis, E. T. (2018). Spatial effects-site-specific regulation of actin and microtubule organization by septin GTPases. J. Cell Sci. 131, jcs207555. doi:10.1242/jcs.207555 · DOI
  111. Steenblock, C., Heckel, T., Czupalla, C., Espıŕito Santo, A. I., Niehage, C., Sztacho, M. and Hoflack, B. (2014). The Cdc42 guanine nucleotide exchange factor FGD6 coordinates cell polarity and endosomal membrane recycling in osteoclasts. J. Biol. Chem. 289, 18347-18359. doi:10.1074/jbc.M113.504894 · DOI
  112. Stone, J. A., McCrea, J. B., Witter, R., Zajic, S. and Stoch, S. A. (2019). Clinical and translational pharmacology of the cathepsin K inhibitor odanacatib studied for osteoporosis. Br. J. Clin. Pharmacol. 85, 1072-1083. doi:10.1111/bcp.13869 · DOI · Paper page
  113. Sztul, E., Chen, P.-W., Casanova, J. E., Cherfils, J., Dacks, J. B., Lambright, D. G., Lee, F.-J. S., Randazzo, P. A., Santy, L. C., Schürmann, A. et al. (2019). ARF GTPases and their GEFs and GAPs: concepts and challenges. MBoC 30, 1249-1271. doi:10.1091/mbc.E18-12-0820 · DOI
  114. Takegahara, N., Kang, S., Nojima, S., Takamatsu, H., Okuno, T., Kikutani, H., Toyofuku, T. and Kumanogoh, A. (2010). Integral roles of a guanine nucleotide exchange factor, FARP2, in osteoclast podosome rearrangements. FASEB J.. 24, 4782-4792. doi:10.1096/fj.10.158212 · DOI
  115. Takito, J., Inoue, S. and Nakamura, M. (2018). The sealing zone in osteoclasts: a self-organized structure on the bone. Int. J. Mol. Sci. 19, 984. doi:10.3390/ ijms19040984 · DOI
  116. Tasca, A., Astleford, K., Lederman, A., Jensen, E. D., Lee, B. S., Gopalakrishnan, R. and Mansky, K. C. (2017). Regulation of osteoclast differentiation by myosin X. Sci. Rep. 7, 7603. doi:10.1038/s41598-017-07855-9 · DOI
  117. Tcherkezian, J. and Lamarche-Vane, N. (2007). Current knowledge of the large RhoGAP family of proteins. Biol. Cell 99, 67-86. doi:10.1042/BC20060086 · DOI
  118. Tehrani, S., Faccio, R., Chandrasekar, I., Ross, F. P. and Cooper, J. A. (2006). Cortactin has an essential and specific role in osteoclast actin assembly. MBoC 17, 2882-2895. doi:10.1091/mbc.e06-03-0187 · DOI
  119. Teitelbaum, S. L. (2016). Therapeutic implications of suppressing osteoclast formation versus function. Rheumatology (Oxf.) 55, ii61-ii63. doi:10.1093/ rheumatology/kew350 · DOI
  120. Terman, J. R. and Kashina, A. (2013). Post-translational modification and regulation of actin. Curr. Opin. Cell Biol. 25, 30-38. doi:10.1016/j.ceb.2012.10.009 · DOI
  121. Teti, A., Marchisio, P. C. and Zallone, A. Z. (1991). Clear zone in osteoclast function: role of podosomes in regulation of bone-resorbing activity. Am. J. Physiol. 261, C1-C7. doi:10.1152/ajpcell.1991.261. · DOI
  122. C1 Touaitahuata, H., Blangy, A. and Vives, V. (2014). Modulation of osteoclast differentiation and bone resorption by Rho GTPases. Small GTPases 5, e28119. doi:10.4161/sgtp.28119 · DOI
  123. Touaitahuata, H., Morel, A., Urbach, S., Mateos-Langerak, J., de Rossi, S. and Blangy, A. (2016). Tensin 3 is a new partner of Dock5 that controls osteoclast podosome organization and activity. J. Cell. Sci. 129, 3449-3461. doi:10.1242/jcs.184622 · DOI
  124. Tresguerres, F. G. F., Torres, J., López-Quiles, J., Hernańdez, G., Vega, J. A. and Tresguerres, I. F. (2020). The osteocyte: a multifunctional cell within the bone. Ann. Anat. 227, 151422. doi:10.1016/j.aanat.2019.151422 · DOI
  125. Valadares, N. F., d' Muniz Pereira, H., Ulian Araujo, A. P. and Garratt, R. C. (2017). Septin structure and filament assembly. Biophys Rev 9, 481-500. doi:10. 1007/s12551-017-0320-4 · DOI
  126. van den Dries, K., Nahidiazar, L., Slotman, J. A., Meddens, M. B. M., Pandzic, E., Joosten, B., Ansems, M., Schouwstra, J., Meijer, A., Steen, R. et al. (2019a). Modular actin nano-architecture enables podosome protrusion and mechanosensing. Nat. Commun. 10, 5171. doi:10.1038/s41467-019-13123-3 · DOI
  127. van den Dries, K., Linder, S., Maridonneau-Parini, I. and Poincloux, R. (2019b). Probing the mechanical landscape -new insights into podosome architecture and mechanics. J. Cell. Sci. 132, jcs236828. doi:10.1242/jcs.236828 · DOI
  128. van Dijk, F. S., Zillikens, M. C., Micha, D., Riessland, M., Marcelis, C. L. M., de Die-Smulders, C. E., Milbradt, J., Franken, A. A., Harsevoort, A. J., Lichtenbelt, K. D. et al. (2013). PLS3 mutations in X-linked osteoporosis with fractures. N. Engl. J. Med. 369, 1529-1536. doi:10.1056/NEJMoa1308223 · DOI
  129. Vargas-Franco, J. W., Castaneda, B., Redinı, F., Gómez, D. F., Heymann, D. and Leźot, F. (2018). Paradoxical side effects of bisphosphonates on the skeleton: what do we know and what can we do? J. Cell. Physiol. 233, 5696-5715. doi:10. 1002/jcp.26465 · DOI · Paper page
  130. Vedula, P. and Kashina, A. (2018). The makings of the "actin code": regulation of actin's biological function at the amino acid and nucleotide level. J. Cell. Sci. 131, jcs215509. doi:10.1242/jcs.215509 · DOI
  131. Vives, V., Laurin, M., Cres, G., Larrousse, P., Morichaud, Z., Noel, D., Co ̂te, J.-F. and Blangy, A. (2011). The Rac1 exchange factor Dock5 is essential for bone resorption by osteoclasts. J. Bone Miner. Res. 26, 1099-1110. doi:10.1002/jbmr.282 · DOI
  132. Vives, V., Cres, G., Richard, C., Busson, M., Ferrandez, Y., Planson, A.-G., Zeghouf, M., Cherfils, J., Malaval, L. and Blangy, A. (2015). Pharmacological inhibition of Dock5 prevents osteolysis by affecting osteoclast podosome organization while preserving bone formation. Nat. Commun. 6, 6218. doi:10.1038/ncomms7218 · DOI
  133. Wang, Y., Lebowitz, D., Sun, C., Thang, H., Grynpas, M. D. and Glogauer, M. (2008). Identifying the relative contributions of rac1 and rac2 to osteoclastogenesis. J. Bone Miner. Res. 23, 260-270. doi:10.1359/jbmr.071013 · DOI
  134. Wang, B., Pan, J., Yu, H., Xiong, L., Zhao, K., Xiong, S., Guo, J., Lin, S., Sun, D., Zhao, L. et al. (2019). Lack of myosin X enhances osteoclastogenesis and increases cell surface Unc5b in osteoclast-lineage cells. J. Bone Miner. Res. 34, 939-954. doi:10.1002/jbmr.3667 · DOI
  135. Wennerberg, K., Forget, M.-A., Ellerbroek, S. M., Arthur, W. T., Burridge, K., Settleman, J., Der, C. J. and Hansen, S. H. (2003). Rnd proteins function as RhoA antagonists by activating p190 RhoGAP. Curr. Biol. 13, 1106-1115. doi:10. 1016/S0960-9822(03)00418-4 · DOI
  136. Xing, W., Liu, J., Cheng, S., Vogel, P., Mohan, S. and Brommage, R. (2013). Targeted disruption of leucine-rich repeat kinase 1 but not leucine-rich repeat kinase 2 in mice causes severe osteopetrosis. J. Bone Miner. Res. 28, 1962-1974. doi:10.1002/jbmr.1935 · DOI
  137. Yamamoto, T., Hasegawa, T., Hongo, H. and Amizuka, N. (2019). Three- dimensional morphology of the Golgi apparatus in osteoclasts: NADPase and arylsulfatase cytochemistry, and scanning electron microscopy using osmium maceration. Microscopy (Oxf ) 68, 243-253. doi:10.1093/jmicro/dfz003 · DOI
  138. Zalli, D., Neff, L., Nagano, K., Shin, N. Y., Witke, W., Gori, F. and Baron, R. (2016). The actin-binding protein cofilin and its interaction with cortactin are required for podosome patterning in osteoclasts and bone resorption in vivo and in vitro. J. Bone Miner. Res. 31, 1701-1712. doi:10.1002/jbmr.2851 · DOI
  139. aaw6143 · DOI · Paper page
  140. Zou, W., Kitaura, H., Reeve, J., Long, F., Tybulewicz, V. L., Shattil, S. J., Ginsberg, M. H., Ross, F. P. and Teitelbaum, S. L. (2007). Syk, c-Src, the αvβ3 integrin, and ITAM immunoreceptors, in concert, regulate osteoclastic bone resorption. J. Cell Biol. 176, 877-888. doi:10.1083/jcb.200611083 · DOI
  141. Zumbrunn, J., Kinoshita, K., Hyman, A. A. and Näthke, I. S. (2001). Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3β phosphorylation. Curr. Biol. 11, 44-49. doi:10.1016/S0960-9822(01)00002-1 · DOI

Cited by

Sorted by citations

Authors
Blangy, A., Bompard, G., Guerit, D., Marie, P., Maurin, J., Morel, A., & Vives, V.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Centre de Recherche de Biologie Cellulaire de Montpellier (CRBM), Montpellier Univ. , CNRS, 34000 Montpellier , France
Corresponding author
Blangy, Anne
ORCID
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2020-07-01
Volume
133
Issue
13
Pages
jcs244798
ISSN
  • 0021-9533 (ISSN-L)
  • 1477-9137
DOI
10.1242/jcs.244798
OpenAlex
W3039146981
Cited by
76
References
3
Citations by year
2026: 11 · 2025: 18 · 2024: 9 · 2023: 16 · 2022: 10 · 2021: 10 · 2020: 2
FWCI
0.93
Type
journal article
Language
en
Open access
Licence
www.biologists.com/user-licence-1-1 (vor)
Locations
  • Journal of Cell Science (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • HighWire Press Open Archive (submittedVersion)
Funders
  • Centre National de la Recherche Scientifique
  • Montpellier University
  • Fondation pour la Recherche Médicale (DEQ20160334933)
  • Fondation ARC pour la Recherche sur le Cancer (PJA2019-1209321, PDF2016-1205179)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
  • Health Sciences › Medicine › Rheumatology › Bone and Dental Protein Studies
Keywords
osteoclasts, cytoskeleton, bone resorption, osteoporosis, actin, microtubules, osteoclastogenesis, bone loss, therapeutic target, bone fragility
MeSH terms
Bone Resorption, Cell Differentiation, Cytoskeleton, Humans, Microtubules, Osteoclasts, Osteoporosis

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