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Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion

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Abstract

Entamoeba histolytica is the causative agent of amoebiasis, a potentially fatal diarrhoeal disease in the developing world. The parasite was named “histolytica” for its ability to destroy host tissues, which is probably driven by direct killing of human cells. The mechanism of human cell killing has been unclear, although the accepted model was that the parasites use secreted toxic effectors to kill cells before ingestion1. Here we report the discovery that amoebae kill by ingesting distinct pieces of living human cells, resulting in intracellular calcium elevation and eventual cell death. After cell killing, amoebae detach and cease ingestion. Ingestion of human cell fragments is required for cell killing, and also contributes to invasion of intestinal tissue. The internalization of fragments of living human cells is reminiscent of trogocytosis (from Greek trogo, nibble) observed between immune cells2,3,4,5,6, but amoebic trogocytosis differs because it results in death. The ingestion of live cell material and the rejection of corpses illuminate a stark contrast to the established model of dead cell clearance in multicellular organisms7. These findings change the model for tissue destruction in amoebiasis and suggest an ancient origin of trogocytosis as a form of intercellular exchange.

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Figure 1: Amoebae internalize human cell fragments, preceding human cell death.
Figure 2: Amoebic trogocytosis is predominant and specific to live human cells.
Figure 3: Amoebic trogocytosis contributes to human cell killing.
Figure 4: Amoebic trogocytosis occurs with red blood cells, contributes to intestinal invasion, and promotes enhanced cell killing.

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Acknowledgements

We thank J. A. Redick and S. J. Guillot for assistance with sample preparation for electron microscopy and D. A. Zemo of Olympus for assistance with multiphoton microscopy. We thank the University of Virginia Research Histology Core for assistance with preparation of frozen sections. We thank J. E. Casanova, J. D. Castle, J. Lannigan, K. S. Ravichandran and R. P. Taylor for helpful discussions. The artwork (Extended Data Fig. 1) was prepared by A. Impagliazzo. K.S.R. was supported by a Howard Hughes Medical Institute Postdoctoral Fellowship from the Life Sciences Research Foundation, and a Postdoctoral Fellowship from the Hartwell Foundation. N.M.M.-L. was supported by NIH Training Grant AI07046-32. This work was supported by NIH grant 5R01 AI-26649 to W.A.P.

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Authors

Contributions

K.S.R. designed, performed and analysed the experiments. W.A.P. oversaw experimental design and analysis. M.D.S. assisted with Amnis Imagestream experimental design and with collection and analysis of Amnis Imagestream data. N.M.M.-L. assisted with isolation and preparation of mouse tissue for ex vivo imaging. S. and A.B. contributed plasmids and antibodies for the study of EhC2PK and contributed to analysis. K.S.R. and W.A.P. wrote the manuscript.

Corresponding author

Correspondence to William A. Petri Jr.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Models for ingestion and human cell killing.

a, Previous model for cell killing, in which human cell attachment is followed by human cell killing and then ingestion of the killed cell. b, Model for amoebic trogocytosis in cell killing, in which attachment is followed by ingestion of fragments of human cell material, which leads to human cell death. Following cell killing, amoebae dissociate from the dead cells. c, Model for phagocytosis of pre-killed human cells, which are ingested whole.

Extended Data Figure 2 Polymerized actin is detected during amoebic trogocytosis.

a, Electron microscopy with human Jurkat cells pre-labelled with biotin and streptavidin–6 nm gold. Human cells (H) were co-incubated with amoebae (A) for 2 min. Top left, low magnification image. Top right, membrane-bound fragment of gold-labelled (circles) human cell material (arrow) within the amoeba. Bottom left, high magnification image of the amoeba cell membrane, demonstrating the absence of gold labelling. Bottom right, high magnification image demonstrating gold in the human cell membrane but not in the amoeba membrane. Scale bar, 5 µm (top left), 0.5 µm (top right and bottom). Images are representative of two independent experiments. b, Electron microscopy imaging of human Jurkat cells co-incubated with amoebae for one minute. Left, demonstration of human cell material contained within polymerized amoeba cytoskeleton (black arrow); note the distorted shape of the human cell as it is pulled into the amoeba (white arrow). Middle, a fragment of human cell material visible (white arrow) within polymerized amoeba cytoskeleton (black arrow). Right, a fragment of human material (white arrow) distal to the targeted human cell is surrounded by polymerized cytoskeleton (black arrow); N, nucleus. Scale bars, 5 μm. Images are representative of three independent experiments. c, Polymerized actin within the amoebae at the site of human cell attachment. CMFDA-labelled amoebae (green) were co-incubated with human Jurkat cells for 1 min, and post-stained with rhodamine-phalloidin (red). Polymerized actin within the amoebae is indicated with black arrows. A ring of polymerized actin likely surrounding an ingested fragment is indicated with a white arrow. Scale bars, 5 μm. Images are representative of two independent experiments. d, Immunofluorescence microscopy imaging, with human cells co-incubated with amoebae for five minutes. Shown are images acquired at the indicated z-heights, with the amoeba plasma membrane stained with anti-Gal/GalNAc lectin, the human Jurkat cell plasma membrane stained with anti-CD3 and DAPI stained nuclei. Arrows, human cell fragments within amoebae, surrounded by amoebic Gal/GalNAc lectin. Scale bar, 10 μm. Images are representative of two independent experiments.

Extended Data Figure 3 Ingestion of fragments precedes human cell death and ceases after cell death.

a, b, Live microscopy with DiD-labelled human Jurkat cells and with SYTOX blue present during imaging. a, Human cells (H) initially retain membrane integrity while amoebae (A) are extensively internalizing fragments (arrows), demonstrated by the lack of SYTOX blue uptake. Images are representative of three independent experiments. b, Loss of human cell membrane integrity indicative of cell death at T = 15:20, and disassociation between the amoebae and the dead human cell at T = 16:00. White arrows, amoebae; black arrow, human cell. Scale bars, 10 μm. Images are representative of three independent experiments.

Extended Data Figure 4 Permeable human cells are not viable and trogocytosis requires viable human cells.

a, Detection of 3′OH nicked DNA using terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL), in conjunction with detection of cell permeability. Amoebae (A) and human Jurkat cells (H) were co-incubated for 40 min, or control human cells were incubated in the absence of amoebae. Prior to fixation, cells were labelled with live/dead fixable red to allow for the detection of membrane permeability. Following fixation, TUNEL was used to allow for the detection of nicked DNA. As indicated by arrows, confocal imaging demonstrates that most permeable human cells (red) also contain nicked DNA (green). Control human cells are not permeable and lack nicked DNA. Images are representative of three independent experiments. b, Detection of mitochondrial potential and membrane permeability using live confocal microscopy. DiD and JC-1-labelled human Jurkat cells were co-incubated with amoebae with SYTOX blue present during imaging. Mitochondrial potential is detected in living, non-permeable human cells (arrows). In contrast, cells that are permeable, as indicated by SYTOX blue staining (arrowheads), lack mitochondrial potential. Images are representative of six independent experiments. c, d, Killed human Jurkat cells were labelled with CMFDA, whereas live human Jurkat cells were separately labelled with DiD. c, Living and pre-killed human cells were combined at 1:1 and SYTOX blue was present in the media during imaging. SYTOX blue staining confirms that only the pre-killed (green) cells are dead (blue). d, Living and dead human cells were combined with amoebae in the presence of SYTOX blue. DiD-labelled fragments (arrows) of living human cells (asterisks) are internalized, whereas pre-killed cells (arrowheads) are ingested whole, demonstrating that live human cells are required for amoebic trogocytosis. Scale bars, 10 μm. Images in c, d are representative of three independent experiments.

Extended Data Figure 5 Imaging flow cytometry analysis.

Shown is the gating strategy that was used to analyse imaging flow cytometry data, with the percentage of gated events, and number of gated events in parentheses, shown in each case. This example illustrates the gating of the T = 40 min. sample shown in Fig. 2, with CMFDA-labelled amoebae, DiD-labelled human Jurkat cells, and live/dead violet-labelled dead cells; 10,000 events were collected. 1, In-focus events were gated using a gradient of Brightfield. 2, Events gated in 1 were refined to remove events with more than one cell or group of cells not in contact, that is, cases where multiple independent events were captured in flow in the same image. 3, Events gated in 2 were gated according to the intensity and aspect ratio of the CMFDA labelled amoebae. These parameters divided the events into ‘human cells not attached to amoebae’, ‘amoebae,’ and clusters with more than one amoeba. Clusters with more than one amoeba were typically less than 2% of gated events, and were omitted from subsequent analyses due to the difficulty in obtaining independent measurements (that is, the extent of human cell internalization) on each individual amoeba present in a cluster. 4, Events gated in 3 as ‘amoebae’ were further examined to determine if human cells were present; events gated as ‘amoebae with human cells’ contained human cells. 5, Human cell positive events gated in 4 were further examined to determine if the human cells were internalized by using the internalization score feature to quantify the overlap between the DiD image and a mask based on the CMFDA image. An internalization score of 1 was used as the cutoff to gate ‘internalized human cells.’ 6, ‘Internalized human cells’ from 5 were further examined to determine if the DiD label was intact or fragmented, by measuring the bright detail and maximum pixel intensity of the DiD image. Events were gated as ‘High,’ ‘Mid,’ or ‘Low’ according to the extent of fragmentation. 3a, To assess the viability of human cells in events not containing amoebae, ‘human cells not attached to amoebae’ gated in 3 were further examined to measure the intensity of live/dead violet staining and granularity (SSC, side scatter). Dead cells were gated as indicated, to define ‘dead human cells not attached to amoebae.’ 4a, To assess the viability of human cells in events containing amoebae, ‘amoebae with human cells’ gated in 4 were further examined. Dead amoebae were first excluded by measuring the overlap between the live/dead violet image and a mask based on the CMFDA image. ‘Live amoebae’ were gated as indicated. 4b, Events gated in 4a that contained human cells and live amoebae (‘live amoebae’) were further examined to identify dead human cells by measuring the intensity of live/dead violet staining and granularity (SSC). Dead human cells were gated as indicated, to define ‘dead human cells attached to amoebae.’

Extended Data Figure 6 Incubation on ice or treatment with wortmannin inhibits amoebic trogocytosis and human cell killing.

af, Imaging flow cytometry analysis with amoebae and human Jurkat cells that were incubated at 37 °C (control), or with amoebae and human Jurkat cells that were briefly centrifuged and incubated on ice; cells were co-incubated for 40 min. a, Measurement of human cell internalization. b, Measurement of fragmentation of internalized human cellular material, gated from low to high. c, Detection of dead human cells. Shown in df are means and standard deviations for biological replicates at each time point (10,000 events/replicate). gj, Imaging flow cytometry analysis with amoebae treated with wortmannin. Shown are plots from T = 40 min. g, Measurement of fragmentation. h, Detection of dead cells. i, j, Means and standard deviations for biological triplicates (15,000 events/replicate). P values from t-tests: *P < 0.05, **P < 0.01, ***P < 0.001.

Extended Data Figure 7 Treatment with cytochalasin D or anti-Gal/GalNAc lectin blocking antibodies inhibits amoebic trogocytosis and human cell killing.

af, Imaging flow cytometry analysis with amoebae treated with vehicle (control) or treated with cytochalasin D. Shown are plots from T = 40 min. a, Measurement of human cell internalization. b, Measurement of human cell fragmentation. c, Detection of dead human cells. Shown in df are means and standard deviations for biological replicates at each time point (10,000 events/replicate). gl, Imaging flow cytometry analysis with amoebae treated with a control monoclonal antibody16,28 (7F4, control) directed to the amoebic Gal/GalNAc lectin epitope 3 (amino acids 1082–1138) or treated with a blocking monoclonal antibody16,28 (3F4, blocking) directed to the amoebic Gal/GalNAc lectin epitope 1 (amino acids 895–998). Mab 3F4 was previously shown to enhance adhesion to human cells, while inhibiting human cell killing16. Shown are plots from T = 40 min. g, Measurement of human cell internalization. h, Measurement of human cell fragmentation. i, Detection of dead human cells. Shown in jl are means and standard deviations for biological replicates at each time point (10,000 events/replicate). P values from t-tests: *P < 0.05, **P < 0.01, ***P < 0.001.

Extended Data Figure 8 Amoebic trogocytosis occurs with human Caco-2 colonic epithelial cells.

Live confocal microscopy with human Caco-2 cells pre-labelled with DiD and CMFDA. Shown is an amoeba (A) in contact with a human cell (H) at time 0, and fragments (arrows) of DiD- and CMFDA-labelled human material ingested over time. Scale bar, 10 μm. Images are representative of two independent experiments.

Extended Data Figure 9 Amoebic trogocytosis precedes tissue invasion.

Live three dimensional multiphoton microscopy with amoebae interacting with ex vivo mouse intestinal tissue, demonstrating that amoebic trogocytosis occurs before amoebic tissue invasion. Intestinal tissue was from the caecum of a mouse expressing membrane-targeted enhanced EGFP (yellow false colour) and amoebae were pre-labelled with calcein violet (blue). a, Time points from one x–y plane taken from the three dimensional reconstruction of the live three dimensional data. Note that ingestion of fragments (arrows) of mouse cells occurs before amoebic tissue invasion in the z-axis. This is visualized as loss of an amoeba (asterisk) from the x–y plane. b, The same time points as in panel a, shown as three dimensional reconstructions. Shown is a subset of the total collected z-height. The same amoeba (asterisk/arrow) can be seen invading the tissue in the z-axis. Images are representative of three independent experiments.

Extended Data Figure 10 Cell death occurs during tissue invasion.

a, Live confocal microscopy with amoebae interacting ex vivo mouse intestinal tissue, demonstrating that cell death occurs during tissue invasion. Amoebae were pre-labelled with calcein violet (blue) and incubated with mouse intestinal tissue from the caecum of a mouse expressing membrane-targeted enhanced EGFP (green), in the presence of SYTOX Orange. Dead cells are predominantly found adjacent to amoebae, which are undergoing amoebic trogocytosis. Images are representative of three independent experiments. b, Live multiphoton microscopy with amoebae interacting with ex vivo mouse intestinal tissue, demonstrating that the parasites traverse the intestinal crypts, as has been demonstrated in studies using ex vivo human intestine18. Intestinal tissue was from the caecum of a mouse expressing membrane-targeted GFP (green) and amoebae were pre-labelled with calcein violet (blue). Parasites can be seen localized to the centre of crypts, shown in cross-section (brackets). Scale bars, 20 μm. Images are representative of three independent experiments.

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Supplementary information

Live confocal microscopy time lapse demonstrating that bites of human cell material are internalized by the amoebae

Ingestion of bites occurs while human Jurkat cells are viable and ceases once they are dead. Human cells were pre-labeled with DiI (red; cell membrane), Flou4 (green; intracellular Ca2+); and SYTOX blue (blue; nucleic acid in permeable cells) was present in the media during imaging. Images were collected every 30 seconds are played back at 1 frame per second. (MOV 10109 kb)

Live confocal microscopy time lapse demonstrating that human cell intracellular calcium elevation follows the ingestion of bites

Human Jurkat cells were pre-labeled with DiD (pink; cell membrane), and Flou4 (green; intracellular Ca2+). Images were collected every 20 seconds and are played back at 1 frame per second. (MOV 7735 kb)

3-D reconstruction of live 4-D confocal microscopy demonstrating that amoebic trogocytosis occurs with human red blood cells and that they are not fully internalized by the amoebae

Human red blood cells were pre-labeled with DiD (pink; cell membrane) and amoebae were pre-labeled with CMFDA (green). Z-stacks were collected continuously. The Video is played back at 1 frame per second. (MOV 160 kb)

Surface rendered version of Video 3 demonstrating that amoebic trogocytosis occurs with human red blood cells and that they are not fully internalized

Red blood cells are shown in pink and the amoeba in green. (MOV 581 kb)

Live 4-D multiphoton microscopy with amoebae interacting with ex vivo mouse intestinal tissue, demonstrating that amoebic trogocytosis occurs during amoebic tissue invasion

Intestinal tissue was from the cecum of a mouse expressing membrane-targeted enhanced green fluorescent protein (EGFP) and amoebae were pre-labeled with calcein violet (blue; intracellular esterase activity). Shown is one X-Y plane from the 3-D reconstruction of the 4-D data. Z-stacks were collected continuously. The Video is played back at 1 frame per second. (MOV 16521 kb)

3-D reconstruction of the live 4-D multiphoton microscopy dataset from Video 5

Shown is a subset of the total collected Z-height, as a 3-D reconstruction with membrane targeted EGFP shown false-colored in yellow and amoebae in blue. (MOV 3733 kb)

Live 4-D multiphoton microscopy with amoebae interacting with ex vivo mouse intestinal tissue, demonstrating that amoebic trogocytosis occurs during amoebic tissue invasion

Shown is one X-Y plane from the 3-D reconstruction of the 4-D data. Note that ingestion of bites of mouse cells occurs prior to amoebic tissue invasion in the Z-axis (visualized as loss of the amoeba from the X-Y plane). Intestinal tissue was from the cecum of a mouse expressing membrane-targeted EGFP (yellow false color) and amoebae were pre-labeled with calcein violet (blue; intracellular esterase activity). Z-stacks were collected continuously. The Video is played back at 1 frame per second. (MOV 13105 kb)

3-D reconstruction of the live 4-D multiphoton microscopy dataset from Video 7

Shown is a subset of the total collected Z-height, as a 3-D reconstruction with membrane targeted EGFP shown false-colored in yellow and amoebae in blue. An amoeba can be seen invading the tissue in the Z-axis. (MOV 13234 kb)

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Ralston, K., Solga, M., Mackey-Lawrence, N. et al. Trogocytosis by Entamoeba histolytica contributes to cell killing and tissue invasion. Nature 508, 526–530 (2014). https://doi.org/10.1038/nature13242

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