The Race to the Pole: How High-Aspect Ratio Shape and Heterogeneous Environments Limit Phagocytosis of Filamentous Escherichia coli Bacteria by Macrophages

Möller, Jens; Luehmann, Tessa; Hall, Heike; Vogel, Viola

doi:10.1021/nl3004896

Cited by 100 publications

(118 citation statements)

References 47 publications

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“…[38][39] Successful phagocytosis of filamentous E. coli bacteria by macrophages only happened when one of the terminal bacterial filament poles was accessible to macrophages. 40 Therefore, the contact between cellular membrane and end-caps of rods may be the key to effective cellular uptake via phagocytosis. However, the uptake of nanometer-sized rods by non-phagocytic cells was found to be affected by particle size and aspect ratio.…”

Section: Length Effect Of Rods On Cellular Uptake By Breast Cancer Cementioning

confidence: 99%

Cellular Uptake and Movement in 2D and 3D Multicellular Breast Cancer Models of Fructose-Based Cylindrical Micelles That Is Dependent on the Rod Length

Zhao

Xiao

et al. 2016

ACS Appl. Mater. Interfaces

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While the shape effect of nanoparticles on cellular uptake has been frequently studied, no consistent conclusions are available currently. The controversy mainly focuses on the cellular uptake of elongated (i.e., filaments or rod-like micelles) as compared to spherical (i.e., micelles and vesicles) nanoparticles. So far, there is no clear trend that proposes the superiority of spherical or nonspherical nanoparticles with conflicting reports available in the literature. One of the reasons is that these few reports available deal with nanoparticles of different shapes, surface chemistries, stabilities, and aspects ratios. Here, we investigated the effect of the aspect ratio of cylindrical micelles on the cellular uptake by breast cancer cell lines MCF-7 and MDA-MB-231. Cylindrical micelles, also coined rod-like micelles, of various length were prepared using fructose-based block copolymers poly(1-O-methacryloyl-β-d-fructopyranose)-b-poly(methyl methacrylate). The critical water content, temperature, and stirring rate that trigger the morphological transition from spheres to rods of various aspect ratios were identified, allowing the generation of different kinetically trapping morphologies. High shear force as they are found with high stirring rates was observed to inhibit the formation of long rods. Rod-like micelles with length of 500-2000 nm were subsequently investigated toward their ability to translocate in breast cancer cells and penetrate into MCF-7 multicellular spheroid models. It was found that shorter rods were taken up at a higher rate than longer rods.

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Section: Length Effect Of Rods On Cellular Uptake By Breast Cancer Cementioning

confidence: 99%

Cellular Uptake and Movement in 2D and 3D Multicellular Breast Cancer Models of Fructose-Based Cylindrical Micelles That Is Dependent on the Rod Length

Zhao

Xiao

et al. 2016

ACS Appl. Mater. Interfaces

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“…This entry is assumed to be caused by tip recognition following rotation initiated by the asymmetric elastic strain at the tube-bilayer interface. To determine whether such shape-and orientation-dependent mechanisms are also manifested by the phagocytosis of bacterial filaments, Mö ller et al [7] experimentally investigated the effects of shape and micro-environments on the phagocytosis of filamentous Escherichia coli bacteria by macrophages. They found that complete uptake occurs only if one of the terminal bacteria filament poles enters the cell first.…”

Section: Introductionmentioning

confidence: 99%

Coupled elasticity–diffusion model for the effects of cytoskeleton deformation on cellular uptake of cylindrical nanoparticles

Wang

2015

J. R. Soc. Interface.

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Molecular dynamic simulations and experiments have recently demonstrated how cylindrical nanoparticles (CNPs) with large aspect ratios penetrate animal cells and inevitably deform cytoskeletons. Thus, a coupled elasticity-diffusion model was adopted to elucidate this interesting biological phenomenon by considering the effects of elastic deformations of cytoskeleton and membrane, ligand -receptor binding and receptor diffusion. The mechanism by which the binding energy drives the CNPs with different orientations to enter host cells was explored. This mechanism involved overcoming the resistance caused by cytoskeleton and membrane deformations and the change in configurational entropy of the ligand -receptor bonds and free receptors. Results showed that deformation of the cytoskeleton significantly influenced the engulfing process by effectively slowing down and even hindering the entry of the CNPs. Additionally, the engulfing depth was determined quantitatively. CNPs preferred or tended to vertically attack target cells until they were stuck in the cytoskeleton as implied by the speed of vertically oriented CNPs that showed much faster initial engulfing speeds than horizontally oriented CNPs. These results elucidated the most recent molecular dynamics simulations and experimental observations on the cellular uptake of carbon nanotubes and phagocytosis of filamentous Escherichia coli bacteria. The most efficient engulfment showed the stiffness-dependent optimal radius of the CNPs. Cytoskeleton stiffness exhibited more significant influence on the optimal sizes of the vertical uptake than the horizontal uptake.

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“…9,10 Rod-like or ellipsoidal particles, for example, mostly enter cells from their tip. 11,12 Oblate particles were found to be internalized more efficiently than spherical or ellipsoidal ones. 13 Surface chemistry of particles has also been shown to impact phagocytosis.…”

mentioning

confidence: 95%

Macrophage Uptake of Janus Particles Depends upon Janus Balance

Gao

2015

Langmuir

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Properties of synthetic particles, such as size and shape, influence how immune cells uptake vaccine and drug carriers. Here, we explore the role of a new property, anisotropic presentation of ligands, in particle uptake by macrophage cells. We use micrometer-sized Janus particles that are partially coated with ligands and investigate how the ligand patch size (Janus balance) affects their uptake by macrophages. Macrophage uptake of both 1.6 and 3 μm Janus particles is enhanced as the size of the ligand patch increases. However, presenting ligands asymmetrically reduces particle phagocytosis; Janus particles with the same amount of ligands as uniformly coated particles are internalized less efficiently. We also show that, because of the asymmetric geometry of Janus particles, the onset of ligand-mediated phagocytosis depends upon the orientation of the particles with respect to the cells. This study demonstrates Janus balance as a new parameter that we can use to manipulate the macrophage uptake of particles.

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The Race to the Pole: How High-Aspect Ratio Shape and Heterogeneous Environments Limit Phagocytosis of Filamentous Escherichia coli Bacteria by Macrophages

Cited by 100 publications

References 47 publications

Cellular Uptake and Movement in 2D and 3D Multicellular Breast Cancer Models of Fructose-Based Cylindrical Micelles That Is Dependent on the Rod Length

Cellular Uptake and Movement in 2D and 3D Multicellular Breast Cancer Models of Fructose-Based Cylindrical Micelles That Is Dependent on the Rod Length

Coupled elasticity–diffusion model for the effects of cytoskeleton deformation on cellular uptake of cylindrical nanoparticles

Macrophage Uptake of Janus Particles Depends upon Janus Balance

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