journal article·2023-09

Differentiation-inducing effect of osteoclast microgrooves for the purpose of three-dimensional design of regenerated bone

Heonuk Jeong, Dain Kim, Kevin Montagne, Takashi Ushida, Katsuko S Furukawa

Acta Biomaterialia· Volume 168
Publisher page

Abstract

In vivo bone remodeling is promoted by the balance between osteoclast and osteoblast activity. Conventional research on bone regeneration has mainly focused on increasing osteoblast activity, with limited studies on the effects of scaffold topography on cell differentiation. Here, we examined the effect of microgroove-patterned substrate with spacings ranging from 1 to 10 μm on the differentiation of rat bone marrow-derived osteoclast precursors. Tartrate-resistant acid phosphatase (TRAP) staining and relative gene expression quantification showed that osteoclast differentiation was enhanced in substrate with 1 µm microgroove spacing compared with that in the other groups. Additionally, the ratio of podosome maturation stages in substrate with 1 μm microgroove spacing exhibited a distinct pattern, which was characterized by an increase in the ratio of belts and rings and a decrease in that of clusters. However, myosin II abolished the effects of topography on osteoclast differentiation. Overall, these showed that the reduction of myosin II tension in the podosome core by an integrin vertical vector increased podosome stability and promoted osteoclast differentiation in substrates with 1 μm microgroove spacing, including that microgroove design plays an important role in scaffolds for bone regeneration. STATEMENT OF SIGNIFICANCE: Reduction of myosin II tension in the podosome core, facilitated by an integrin vertical vector, resulted in an enhanced osteoclast differentiation, concomitant with an increase in podosome stability within 1-μm-spaced microgrooves. These findings are anticipated to serve as valuable indicators for the regulation of osteoclast differentiation through the manipulation of biomaterial surface topography in tissue engineering. Furthermore, this study contributes to the lucidation of the underlying mechanisms governing cellular differentiation by providing insights into the impact of the microtopographical environment.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Bone Tissue Engineering Materials · 3D Printing in Biomedical Research · Bone Metabolism and Diseases

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (59)

Show source-provided references
1. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells10.1353/port.2012.0000 ↗
2. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene10.1038/345442a0 ↗
3. Retinoic acid increases proliferation of human osteoclast progenitors and inhibits RANKL-stimulated osteoclast differentiation by suppressing RANK10.1371/journal.pone.0013305 ↗
4. Inhibition of osteoclast differentiation and bone resorption by N-methylpyrrolidone10.1074/jbc.M111.223297 ↗
5. The role of bisphosphonates in breast cancer: Development of bisphosphonates10.1186/bcr414 ↗
6. Mechanical stress directly suppresses osteoclast differentiation in RAW264.7 cells
7. Nano-topography sensing by osteoclasts10.1242/jcs.073411 ↗
8. Nanocrystalline silicon substituted hydroxyapatite effects on osteoclast differentiation and resorptive activity10.1039/c3tb21697g ↗
9. Osteoclastogenic differentiation of human precursor cells over micro- and nanostructured hydroxyapatite topography10.1016/j.bbagen.2016.01.014 ↗
10. Osteoclast differentiation from human blood precursors on biomimetic calcium-phosphate substrates10.1016/j.actbio.2016.12.013 ↗
11. Response of osteoclasts to titanium surfaces with increasing surface roughness: an in vitro study10.1007/s13758-012-0034-x ↗
12. Surface microtopography modulates sealing zone development in osteoclasts cultured on bone
13. Effects of surface microtopography on the assembly of the osteoclast resorption apparatus10.1098/rsif.2011.0659 ↗
14. Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles10.1038/nrm1436 ↗
15. Podosomes: adhesion hot-spots of invasive cells10.1016/S0962-8924(03)00128-4 ↗
16. Integrin-matrix clusters form podosome-like adhesions in the absence of traction forces10.1016/j.celrep.2013.10.040 ↗
17. Geometry sensing by dendritic cells dictates spatial organization and PGE 2-induced dissolution of podosomes10.1007/s00018-011-0908-y ↗
18. Feel the force: podosomes in mechanosensing10.1016/j.yexcr.2015.11.026 ↗
19. Podosome and sealing zone: specificity of the osteoclast model10.1016/j.ejcb.2005.09.008 ↗
20. Podosomes in adhesion, migration, mechanosensing and matrix remodeling10.1002/cm.21119 ↗
21. Regulated proteolysis of nonmuscle myosin IIA stimulates osteoclast fusion10.1074/jbc.M808621200 ↗
22. Differential contributions of nonmuscle myosin II isoforms and functional domains to stress fiber mechanics10.1038/srep13736 ↗
23. The effect of substrate microtopography on focal adhesion maturation and actin organization via the RhoA/ROCK pathway10.1016/j.biomaterials.2011.08.077 ↗
24. The switching of focal adhesion maturation sites and actin filament activation for MSCs by topography of well-defined micropatterned surfaces10.1016/j.biomaterials.2012.11.031 ↗
25. Micropit surfaces designed for accelerating osteogenic differentiation of murine mesenchymal stem cells via enhancing focal adhesion and actin polymerization10.1016/j.biomaterials.2013.11.089 ↗
26. Osteogenic differentiation of murine mesenchymal stem cells by combination of surface topography and uniaxial stress10.1299/jbse.20-00009 ↗
27. A Topographically optimized substrate with well-ordered lattice micropatterns for enhancing the osteogenic differentiation of Murine Mesenchymal stem cells10.1002/mabi.201000477 ↗
28. Bone is not essential for osteoclast activation10.1371/journal.pone.0012837 ↗
29. Fibronectin inhibits osteoclastogenesis while enhancing osteoclast activity via nitric oxide and interleukin-1β-mediated signaling pathways10.1002/jcb.22791 ↗
30. Tartrate-resistant acid phosphate activity as osteoclastic marker: sensitivity of cytochemical assessment and serum assay in comparison with standardized osteoclast histomorphometry10.1007/BF01623458 ↗
31. New roles of filopodia and podosomes in the differentiation and fusion process of osteoclasts10.4238/2014.July.2.7 ↗
32. Mechanism of blebbistatin inhibition of myosin II10.1074/jbc.M405319200 ↗
33. Microfluidic spinning of flat alginate fibers with grooves for cell-aligning scaffolds10.1002/adma.201201232 ↗
34. Orientation of ECM protein deposition, fibroblast cytoskeleton, and attachment complex components on silicone microgrooved surfaces10.1002/(SICI)1097-4636(199805)40:2<291::AID-JBM14>3.0.CO;2-P ↗
35. Surface topography enhances differentiation of mesenchymal stem cells towards osteogenic and adipogenic lineages10.1016/j.biomaterials.2015.05.030 ↗
36. The control of mesenchymal stem cell differentiation using dynamically tunable surface microgrooves10.1002/adhm.201300692 ↗
37. Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit10.1038/bonekey.2013.215 ↗
38. Norisoboldine suppresses osteoclast differentiation through preventing the accumulation of TRAF6-TAK1 complexes and activation of MAPKs/NF-κB/c-Fos/NFATc1 pathways
39. Akt induces osteoclast differentiation through regulating the GSK3 /NFATc1 signaling cascade10.4049/jimmunol.1101254 ↗
40. Combinatorial surface roughness effects on osteoclastogenesis and osteogenesis10.1021/acsami.8b10992 ↗
41. Assessment of the inner surface microstructure of decellularized cortical bone by a scanning electron microscope10.3390/bioengineering6030086 ↗
42. The architecture of the adhesive apparatus of cultured osteoclasts: From podosome formation to sealing zone assembly10.1371/journal.pone.0000179 ↗
43. Surface-induced regulation of podosome organization and dynamics in cultured osteoclasts10.1002/cbic.200800549 ↗
44. Membrane curvature and its generation by BAR proteins10.1016/j.tibs.2012.09.001 ↗
45. Biogenesis of podosome rosettes through fission10.1038/s41598-017-18861-2 ↗
46. Spatiotemporal organization and mechanosensory function of podosomes10.4161/cam.28182 ↗
47. Different micro/nano-scale patterns of surface materials influence osteoclastogenesis and actin structure10.1007/s12274-021-4026-3 ↗
48. Fibronectin inhibited RANKL-induced differentiation into osteoclast
49. Myosins in osteoclast formation and function10.3390/biom8040157 ↗
50. The RhoGAP activity of myosin IXB is critical for osteoclast podosome patterning, motility, and resorptive capacity10.1371/journal.pone.0087402 ↗
51. Differential localization of myosin II isoforms in resting and activated osteoclasts10.1007/s00223-001-1112-0 ↗
52. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts10.1038/35008607 ↗
53. Substrate adhesion regulates sealing zone architecture and dynamics in cultured osteoclasts10.1371/journal.pone.0028583 ↗
54. Phosphoglycerol dihydroceramide, a distinctive ceramide produced by Porphyromonas gingivalis, promotes RANKL-induced osteoclastogenesis by acting on non-muscle myosin II-A (Myh9), an osteoclast cell fusion regulatory factor10.1016/j.bbalip.2017.01.008 ↗
55. Galectin-3 cleavage alters bone remodeling: Different outcomes in breast and prostate cancer skeletal metastasis10.1158/0008-5472.CAN-15-1793 ↗
56. Symmetrical retrograde actin flow in the actin fusion structure is involved in osteoclast fusion10.1242/bio.025460 ↗
57. Dynamics of podosome stiffness revealed by atomic force microscopy10.1073/pnas.1007835107 ↗
58. Protrusion force microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes10.1038/ncomms6343 ↗
59. Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations10.1038/ncomms2402 ↗