Rapid and extensive membrane reorganization by dendritic cells following exposure to bacteria revealed by high-resolution imaging

Salter, Russell D.; Tuma-Warrino, Renee J.; Hu, Paul Q.; Watkins, Simon C.

doi:10.1189/jlb.0703339

Cited by 15 publications

(19 citation statements)

References 14 publications

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“…After receiving a nanotube-mediated calcium signal, dendritic cells were observed to spread membrane veils toward the origin of the signal (13), similar to the response observed toward Ags (14). Thus, signals transmitted via membrane nanotubes between myeloid cells could augment immune responses at sites distal to the triggering Ag.…”

mentioning

confidence: 59%

Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria

Önfelt

Nedvetzki

Benninger³

et al. 2006

The Journal of Immunology

437

520

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We report that two classes of membrane nanotubes between human monocyte-derived macrophages can be distinguished by their cytoskeletal structure and their functional properties. Thin membrane nanotubes contained only F-actin, whereas thicker nanotubes, i.e., those > approximately 0.7 microm in diameter, contained both F-actin and microtubules. Bacteria could be trapped and surf along thin, but not thick, membrane nanotubes toward connected macrophage cell bodies. Once at the cell body, bacteria could then be phagocytosed. The movement of bacteria is aided by a constitutive flow of the nanotube surface because streptavidin-coated beads were similarly able to traffic along nanotubes between surface-biotinylated macrophages. Mitochondria and intracellular vesicles, including late endosomes and lysosomes, could be detected within thick, but not thin, membrane nanotubes. Analysis from kymographs demonstrated that vesicles moved in a stepwise, bidirectional manner at approximately 1 microm/s, consistent with their traffic being mediated by the microtubules found only in thick nanotubes. Vesicular traffic in thick nanotubes and surfing of beads along thin nanotubes were both stopped upon the addition of azide, demonstrating that both processes require ATP. However, microtubule destabilizing agents colchicine or nocodazole abrogated vesicular transport but not the flow of the nanotube surface, confirming that distinct cytoskeletal structures of nanotubes give rise to different functional properties. Thus, membrane nanotubes between macrophages are more complex than unvarying ubiquitous membrane tethers and facilitate several means for distal interactions between immune cells.

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mentioning

confidence: 59%

Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria

Önfelt

Nedvetzki

Benninger³

et al. 2006

The Journal of Immunology

437

520

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“…We recently used live-cell imaging to show that individual DC respond to exposure to E. coli by rapidly extending membrane veils, or lamellipodia, that can bind the bacteria and transport them along the plasma membrane to the central region of the cell where internalization occurs (Salter et al, 2004). In this system, cells were imaged continuously prior to and after introduction of medium containing bacteria.…”

Section: Many Cellular Responses Are Initiated By Engagement Of Surfamentioning

confidence: 98%

Functional Connectivity between Immune Cells Mediated by Tunneling Nanotubules

2005

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Intercellular signals can be transmitted through neuronal synapses or through gap junctions, with the latter mediating transmission of calcium fluxes and small molecules between cells. We show here that a third form of communication between cells can be mediated by tunneling nanotubules (TNT). When myeloid-lineage dendritic cells and monocytes are triggered to flux calcium by chemical or mechanical stimulation, the signal can be propagated within seconds to other cells at distances hundreds of microns away via TNT. A complex and transient network of TNT is seen in live cells, with individual tubules exhibiting substantial variation in length and diameter. In addition to calcium fluxes, microinjected dye tracers can be transferred through these connections. Following TNT-mediated stimulation, spreading of lamellipodia occurs in dendritic cells characteristic of that seen during the phagocytic response to bacteria. These results demonstrate that nonneuronal cells can transmit signals to distant cells through a physically connected network.

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“…Enhanced green fluorescent protein (EGFP)-expressing E. coli (BL21 strain) 34,35 were grown overnight in LuriaBertani broth with 50 g/mL ampicillin at 37°C with continuous shaking. Cultures were refreshed and grown for 2 hours to reach log phase, washed with Dulbecco's PBS without calcium and magnesium, and used for phagocytosis and bacteria killing studies.…”

Section: Culturing Of Bacteriamentioning

confidence: 99%

“…34,35 Cell viability was measured using the CellTiter 96 AQueous Non-Radioactive Assay (Promega Corp., Madison, WI) according to the manufacturer's instructions or by means of visual assessment using trypan blue.…”

Section: Cell Viabilitymentioning

confidence: 99%

Extracellular Superoxide Dismutase in Macrophages Augments Bacterial Killing by Promoting Phagocytosis

Manni

Tomai

Norris

et al. 2011

The American Journal of Pathology

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Extracellular superoxide dismutase (EC-SOD) is abundant in the lung and limits inflammation and injury in response to many pulmonary insults. To test the hypothesis that EC-SOD has an important role in bacterial infections, wild-type and EC-SOD knockout (KO) mice were infected with Escherichia coli to induce pneumonia. Although mice in the EC-SOD KO group demonstrated greater pulmonary inflammation than did wild-type mice, there was less clearance of bacteria from their lungs after infection. Macrophages and neutrophils express EC-SOD; however, its function and subcellular localization in these inflammatory cells is unclear. In the present study, immunogold electron microscopy revealed EC-SOD in membrane-bound vesicles of phagocytes. These findings suggest that inflammatory cell EC-SOD may have a role in antibacterial defense. To test this hypothesis, phagocytes from wild-type and EC-SOD KO mice were evaluated. Although macrophages lacking EC-SOD produced more reactive oxygen species than did cells expressing EC-SOD after stimulation, they demonstrated significantly impaired phagocytosis and killing of bacteria. Overall, this suggests that EC-SOD facilitates clearance of bacteria and limits inflammation in response to infection by promoting bacterial phagocytosis.

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Rapid and extensive membrane reorganization by dendritic cells following exposure to bacteria revealed by high-resolution imaging

Cited by 15 publications

References 14 publications

Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria

Structurally Distinct Membrane Nanotubes between Human Macrophages Support Long-Distance Vesicular Traffic or Surfing of Bacteria

Functional Connectivity between Immune Cells Mediated by Tunneling Nanotubules

Extracellular Superoxide Dismutase in Macrophages Augments Bacterial Killing by Promoting Phagocytosis

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