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Cited by 65Cellular Mechanics and InteractionsNeuroinflammation and Neurodegeneration MechanismsCell Adhesion Molecules Research

Podosomes in migrating microglia: components and matrix degradation

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Vincent, Catherine, Siddiqui, Tamjeed A, Schlichter, Lyanne C·2012·Journal of Neuroinflammation
DOI 10.1186/1742-2094-9-190PMC PMC3423073
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Abstract

Background: To perform their functions during development and after central nervous system injury, the brain’s immune cells (microglia) must migrate through dense neuropil and extracellular matrix (ECM), but it is not known how they degrade the ECM. In several cancer cell lines and peripheral cells, small multi-molecular complexes (invadopodia in cancer cells, podosomes in nontumor cells) can both adhere to and dissolve the ECM. Podosomes are tiny multi-molecular structures (0.4 to 1 μm) with a core, rich in F-actin and its regulatory molecules, surrounded by a ring containing adhesion and structural proteins. Methods: Using rat microglia, we performed several functional assays: live cell imaging for chemokinesis, degradation of the ECM component, fibronectin, and chemotactic invasion through Matrigel™, a basement membrane type of ECM. Fluorescent markers were used with high-resolution microscopy to identify podosomes and their components. Results: The fan-shaped lamella at the leading edge of migrating microglia contained a large F-actin-rich superstructure composed of many tiny (<1 μm) punctae that were adjacent to the substrate, as expected for cell–matrix contact points. This superstructure (which we call a podonut) was restricted to cells with lamellae, and conversely almost every lamella contained a podonut. Each podonut comprised hundreds of podosomes, which could also be seen individually adjacent to the podonut. Microglial podosomes contained hallmark components of these structures previously seen in several cell types: the plaque protein talin in the ring, and F-actin and actin-related protein (Arp) 2 in the core. In microglia, podosomes were also enriched in phosphotyrosine residues and three tyrosine-kinase-regulated proteins: tyrosine kinase substrate with five Src homology 3 domains (Tks5), phosphorylated caveolin-1, and Nox1 (nicotinamide adenine dinucleotide phosphate oxidase 1). When microglia expressed podonuts, they were able to degrade the ECM components, fibronectin, and Matrigel™. Conclusion: The discovery of functional podosomes in microglia has broad implications, because migration of these innate immune cells is crucial in the developing brain, after damage, and in disease states involving inflammation and matrix remodeling. Based on the roles of invadosomes in peripheral tissues, we propose that microglia use these complex structures to adhere to and degrade the ECM for efficient migration.

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  • Microglia, along with macrophages, are capable of producing podosomes, a matrix-degrading ventral cell surface structure similar to invadopodia.

    “Microglia, along with macrophages, are capable of producing podosomes, a matrix-degrading ventral cell surface structure similar to invadopodia (24).”

    From Microglia express ABI3 in the brains of Alzheimer's disease and Nasu-Hakola disease (2017) · cites this paper as [24]

  • TLN1, PFN1, and VASP are less abundant in microglia isolated from older donors.

    “For instance, talin-1 (TLN1), a protein involved in actin remodeling and cell motility; profilin (PFN1), a protein directly involved in actin binding and polymerization; and VASP, a protein involved in actin filaments elongation, are less abundant in microglia isolated from older donors 47 .”

    From Transcriptomic analysis of purified human cortical microglia reveals age-associated changes (2017) · cites this paper as [47]

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Authors
Vincent, C., Siddiqui, T. A., & Schlichter, L. C.
Affiliations
University of Toronto (CA)
Corresponding author
Schlichter, Lyanne C
ORCID
Schlichter, Lyanne C
Venue
Journal of Neuroinflammation
Publisher
Springer Science and Business Media LLC
Published
2012-08-08
Volume
9
Issue
1
Pages
190-190
ISSN
1742-2094 (ISSN-L)
DOI
10.1186/1742-2094-9-190
PMC
PMC3423073
OpenAlex
W2001913172
Cited by
65
References
0
Citations by year
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FWCI
1.83
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroinflammation (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • TSpace (University of Toronto) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
Heart and Stroke Foundation of Canada
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Keywords
podosomes, microglial migration, extracellular matrix degradation, F-actin, talin, Arp2, fibronectin, Matrigel, caveolin-1, NOX1, Tks5, tyrosine kinase signaling, chemotaxis, chemokinesis, matrix remodeling, lamellae, invadopodia
MeSH terms
Animals, Cell Movement, Cells, Cultured, Chemotaxis, Extracellular Matrix, Rats, Sprague-Dawley, Microglia, Cell Surface Extensions, Rats

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