The ruffled border and attachment regions of the apposing membrane of resorbing osteoclasts as visualized from the cytoplasmic face of the membrane
Abstract
The aim of our present research was to visualize how the plasma membrane is modified and how the cytoskeleton interacts with the attachment and ruffled border regions of resorbing osteoclasts. In order to view the surface modification of membranes and associated cytoskeleton, we employed the method of cell-shearing combined with quick-freezing and rotary replication to expose and replicate an extensive area of the cytoplasmic face of the surface membrane of osteoclasts in contact with synthetic apatite as a substratum. The membrane apposed to the apatite was composed of three different domains: the attachment zone, ruffled border and the remainder. In the attachment zone, a highly organized actin filament network formed dot-shaped, F-actin rich adhesion sites, so-called podosomes, and the actin ring. The cytoskeletal filament of podosomes and actin ring appeared to be in direct contact with the cytoplasmic surface of the underlying membrane. Within the actin ring, individually recognizable podosomes were well preserved, which indicates that the actin ring was probably derived from the fusion of podosomes. After shearing at the ruffled border region, the ruffled border projections and membrane regions among the projections were left behind. These ruffled border projections contained the cytoskeletal network. These actin networks also appeared to be in direct contact with the inner side of the ruffled border membrane or in contact with it via membrane-associated particles. At the basal portion of the ruffled border, numerous clathrin-coated patches or pits were well preserved. Deeper clathrin-coated pits and vesicles were also found, which indicates an active site for receptor-mediated endocytotic events. Clathrin sheets were also observed in the cell periphery outside of the actin ring. This type of clathrin sheets adhered to the apatite substrate, but was not anchored to the actin microfilaments. Our study thus clearly visualized the interaction between the cytoskeletal filaments and the underlying membrane at the ruffled border, attachment zone and podosome in osteoclasts cultured on apatitepellets.
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?
Mature osteoclasts are polarized cells with an apical membrane facing bone and an opposite basolateral membrane facing plasma; both domains are essential for resorbing osteoclasts.
“Mature osteoclasts are polarized cells with an apical membrane facing bone and an opposite basolateral membrane facing plasma. Both apical and basolateral membrane domains are essential structures for resorbing osteoclasts.185”
From Bone remodeling: an operational process ensuring survival and bone mechanical competence (2022) · cites this paper as [185]
Cites
Osteoclastic Bone Resorption by a Polarized Vacuolar Proton Pump
Blair, H. C., Teitelbaum, S. L., Ghiselli, R. W., & Gluck, S. L. (1989) · Science · doi:10.1126/science.2528207 · Cited by 862 · see citing works
Podosomes: adhesion hot-spots of invasive cells
Linder, S., & Aepfelbacher, M. (2003) · Trends in Cell Biology · doi:10.1016/s0962-8924(03)00128-4 · Cited by 615 · see citing works
Foot and mouth: podosomes, invadopodia and circular dorsal ruffles
Buccione, R., Orth, J. D., & McNiven, M. A. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1436 · Cited by 594 · see citing works
Three-dimensional visualization of coated vesicle formation in fibroblasts.
Heuser, J. E. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.84.3.560 · Cited by 580 · see citing works
Destaing, O., Saltel, F., Géminard, J.-C., Jurdic, P., & Bard, F. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-07-0389 · Cited by 453 · see citing works
Tarone, G., Cirillo, D. M., Giancotti, F. G., Comoglio, P. M., & Marchisio, P. C. (1985) · Experimental Cell Research · doi:10.1016/s0014-4827(85)80044-6 · Cited by 436 · see citing works
Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages
Linder, S., Nelson, D. L., Weiss, M., & Aepfelbacher, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9648 · Cited by 429 · see citing works
Removal of Osteoclast Bone Resorption Products by Transcytosis
Salo, J., Lehenkari, P. P., Mulari, M. T. K., Metsikkö, K., & Väänänen, H. K. (1997) · Science · doi:10.1126/science.276.5310.270 · Cited by 427 · see citing works
Trafficking of Matrix Collagens Through Bone-Resorbing Osteoclasts
Nesbitt, S. A., & Horton, M. A. (1997) · Science · doi:10.1126/science.276.5310.266 · Cited by 378 · see citing works
Marchisio, P. C., Cirillo, D. M., Naldini, L., Primavera, M. V., Teti, A. M., & Zambonin-Zallone, A. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.5.1696 · Cited by 328 · see citing works
Lewis, A. K., & Bridgman, P. C. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.5.1219 · Cited by 312 · see citing works
<b>Apatite-mediated Actin Dynamics in Resorbing Osteoclasts</b>
Saltel, F., Destaing, O., Bard, F., Eichert, D., & Jurdic, P. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-06-0522 · Cited by 267 · see citing works
Kinetics of the osteoclast cytoskeleton during the resorption cycle in vitro
Lakkakorpi, P. T., & Väänänen, K. (1991) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650060806 · Cited by 248 · see citing works
The osteoclast clear zone is a specialized cell-extracellular matrix adhesion structure
Väänänen, H. K., & Horton, M. A. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.8.2729 · Cited by 217 · see citing works
Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts
Sato, T., Ovejero, M. D. C., Hou, P., Heegaard, A.-M., Kumegawa, M., Tækker Foged, N., & Delaissé, J.-M. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.5.589 · Cited by 214 · see citing works
Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages
Linder, S., Hüfner, K., Wintergerst, U., et al. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.23.4165 · Cited by 190 · see citing works
Organization of osteoclast microfilaments during the attachment to bone surface in vitro
Lakkakorpi, P. T., Tuukkanen, J., Hentunen, T. A., Järvelin, K., & Väänänen, K. (1989) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650040605 · Cited by 171 · see citing works
Palokangas, H., Mulari, M. T. K., & Väänänen, H. K. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.15.1767 · Cited by 168 · see citing works
Clear zone in osteoclast function: role of podosomes in regulation of bone-resorbing activity
Teti, A. M., Marchisio, P. C., & Zallone, A. Z. (1991) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1991.261.1.c1 · Cited by 144 · see citing works
Osteoclast Ruffled Border Has Distinct Subdomains for Secretion and Degraded Matrix Uptake
Mulari, M. T. K., Zhao, H., Lakkakorpi, P. T., & Väänänen, H. K. (2003) · Traffic · doi:10.1034/j.1600-0854.2003.40206.x · Cited by 140 · see citing works
Formation and function of the ruffled border in osteoclasts
Stenbeck, G. (2002) · Seminars in Cell and Developmental Biology · doi:10.1016/s1084952102000587 · Cited by 133 · see citing works
Jones, S. J., BOYDE, A., & Ali, N. N. (1984) · Anatomy and Embryology · doi:10.1007/bf00318728 · Cited by 117 · see citing works
Avnur, Z., & Geiger, B. (1981) · Journal of Molecular Biology · doi:10.1016/0022-2836(81)90283-7 · Cited by 110 · see citing works
Intracellular membrane trafficking in bone resorbing osteoclasts
Mulari, M., Vääräniemi, J., & Väänänen, H. K. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10371 · Cited by 104 · see citing works
A new specialized cell-matrix interaction in actively resorbing osteoclasts
Stenbeck, G., & Horton, M. A. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.9.1577 · Cited by 85 · see citing works
Paracrine regulation of osteoclast formation and activity: milestones in discovery.
Martin, T. (2004) · PubMed · Cited by 82 · see citing works
Mostov, K. E., & Werb, Z. (1997) · Science · doi:10.1126/science.276.5310.219 · Cited by 73 · see citing works
Aggeler, J., Takemura, R., & Werb, Z. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.97.5.1452 · Cited by 69 · see citing works
Evidence of coated membranes in the ruffled border of the osteoclast
Kallio, D. M., Garant, P. R., & Minkin, C. (1971) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(71)80048-5 · Cited by 63 · see citing works
Structures linking microfilament bundles to the membrane at focal contacts
Samuelsson, S., Luther, P., Pumplin, D. W., et al. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.2.485 · Cited by 46 · see citing works
The effect of substrate composition and condition on resorption by isolated osteoclasts
Shimizu, H., Sakamoto, S., Sakamoto, M., et al. (1989) · Bone and Mineral · doi:10.1016/0169-6009(89)90033-0 · Cited by 40 · see citing works
Clathrin sheets on the protoplasmic surface of ventral membranes of osteoclasts in culture
Akisaka, T. (2003) · Journal of Electron Microscopy · doi:10.1093/jmicro/52.6.535 · Cited by 31 · see citing works
Self-citationMembrane Traffic in Anaglyph Stereo
Heuser, J. E. (2000) · Traffic · doi:10.1034/j.1600-0854.2000.010106.x · Cited by 31 · see citing works
Stages in specialization of fibroblast adhesion and deposition of extracellular matrix.
Woods, A., Smith, C. G., Rees, D. A., et al. (1983) · PubMed · Cited by 29 · see citing works
Stereoscopic display of atomic force microscope images using anaglyph techniques
Smith, J. R., Smith, Connell, et al. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.00603.x · Cited by 24 · see citing works
Spreading of dentinoclasts on various substrata in vitro
Lindskog, S. F., & PIERCE, A. (1988) · European Journal Of Oral Sciences · doi:10.1111/j.1600-0722.1988.tb01561.x · Cited by 15 · see citing works
Robertson, T. A., & Papadimitriou, J. M. (1986) · Journal of Ultrastructure and Molecular Structure Research · doi:10.1016/0889-1605(86)90013-3 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Luxenburg, C., Geblinger, D., Klein, E., Anderson, K., Hanein, D., Geiger, B., & Addadi, L. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000179 · Cited by 285 · see citing works
- Authors
- Akisaka, T.
- Affiliations
- Asahi University (JP)
- Corresponding author
- Akisaka, T.
- Venue
- Journal of Electron Microscopy
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-05-15
- Volume
- 55
- Issue
- 2
- Pages
- 53-61
- ISSN
- 0022-0744 (ISSN-L)
- 1477-9986
- OpenAlex
- W2150894337
- Cited by
- 24
- References
- 37
- Citations by year
- 2025: 1 · 2022: 1 · 2021: 1 · 2020: 1 · 2019: 2 · 2018: 2 · 2016: 1 · 2015: 1 · 2014: 1 · 2013: 1 · 2012: 1
- FWCI
- 1.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Electron Microscopy (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bone Metabolism and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Rheumatology › Bone and Dental Protein Studies
- Keywords
- osteoclasts, ruffled border, plasma membrane, podosomes, actin rings, actin cytoskeleton, clathrin-coated pits, receptor-mediated endocytosis, membrane surface modification
- MeSH terms
- Animals, Bone Resorption, Cell Fractionation, Cell Membrane, Cells, Cultured, Coated Pits, Cell-Membrane, Cytological Techniques, Cytoskeleton, Microscopy, Electron, Microscopy, Electron, Scanning, Microscopy, Fluorescence, Osteoclasts, Rabbits, Clathrin-Coated Vesicles
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