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Review Article

Emperipolesis, entosis and cell cannibalism: Demystifying

the cloud
Nidhi Gupta, Kiran Jadhav, Vandana Shah
Department of Oral Pathology and Microbiology, KM Shah Dental College, Sumandeep Vidyapeeth University, Vadodara, Gujarat, India

Abstract There are intense published data in literature related to cell engulfment phenomena such as emperipolesis,
entosis and cell cannibalism. All these are closely related phenomena with a very fine line of differences.
Its correct identification has a significant diagnostic and prognostic value. After extensive literature search,
a gap of knowledge was found in concept designing and clarity about understanding of aforementioned
terminologies. The authors have attempted to review data of these closely knit terminologies and further
organize its characteristic appearances, pathogenetic aspects and prognostic implications. The data
published in English Language, from 1925 to 2015, were collected using keywords such as emperipolesis,
entosis and cell cannibalism through scientific database systems such as MEDLINE, Science Direct, Cochrane
Library and Google Scholar. Articles were selected which have focused to explain the phenomenon,
presentation and pathogenesis of one or more of this phenomenon. A total of 48 articles were retrieved,
thirty of which were selected. The various cell engulfment phenomena are very similar looking but operate
through entirely different pathways.

Keywords: Cell cannibalism, emperipolesis, entosis, phagocytosis

Address for correspondence:

Dr. Gupta Nidhi, Gokulesh Apartment, Jain Derasar Road, Nizampura, Vadodara ‑ 390 002, Gujarat, India. E‑mail: [email protected]
Received: 15.09.2016, Accepted: 15.12.2016

INTRODUCTION as previously mentioned, are very closely knit but differ in

the variety of the involved host cell and the internalized
Cell engulfment is a well‑known phenomenon. The cells. The molecular events and pathogenesis controlling
interfacial energies of the host cell and the engulfed them also vary considerably. However, following cell
cell play an important role in cell–to‑cell interactions.[1] internalization, it is very difficult to differentiate one from
The phenomenon of a cell harboring an another living the other.[2] With this view in mind, the current review
cell is a very extraordinary finding. Study of cell‑in‑cell attempts to throw light on these related terminologies.
phenomena began with the desire of Lewis to understand Focus has been put on the occurrence, pathogenesis and
his observation of nonphagocytotic process of cell eating a appearance of emperipolesis, entosis and cell cannibalism.
cell.[1] Some such phenomena are such as emperipolesis, cell
cannibalism and entosis. Scarcity of sufficient evidence has EMPERIPOLESIS
lead different researches to propose varying concepts and
hypothesize about their occurrence. These terminologies, Emperipolesis is a condition, wherein hematopoietic cells
in living and intact state are seen in the cytoplasm of host
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DOI: How to cite this article: Gupta N, Jadhav K, Shah V. Emperipolesis,

10.4103/0973-029X.203763 entosis and cell cannibalism: Demystifying the cloud. J Oral Maxillofac
Pathol 2017;21:92-8.

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Gupta, et al.: Emperipolesis, entosis and cell cannibalism

cell without any damage.[3] The cells taken in frequently phagocytosis, there is an active participation of the host cell
are neutrophils, lymphocytes and plasma cells. The host cytoskeleton (actin microfilaments) to form pseudopodia
cells may be a megakaryocyte, monocyte, endothelial cell, or extensions to engulf the dead material. Then, engulfed
fibroblast and a malignant cell.[3,4] In this phenomenon material is then transported inside the cytoplasm with the
with both cells being viable, there is not any physiological help of endoplasmic reticulum and lysosomal complex. The
and morphological consequences to either of them.[5,6] released metabolic breakdown products of the process can
The term was first described by   Humble et al. in 1956 then be further used for synthesis of cellular structures or
as, “the active penetration of one cell by another which released outside the cell.[2]
remains intact.”[3,4] The term comes from the Greek
word, “Emperipolesis,” which means “inside round about Emperipolesis has been detected in bone marrow aspirates,
wandering.”[4] Many physiologic and pathologic conditions tissue cultures, cerebrospinal fluid (CSF), fine‑needle
exhibit this phenomenon [Table 1].[3] aspiration cytology (FNAC) and imprint cytology. Amita
et al. described a case of adult T‑cell lymphoblastic
Phagocytosis differs from emperipolesis in the way that lymphoma (mediastinal type) showing emperipolesis, which
the engulfing cell here does not engulf a living cell, was detected in FNAC and imprint cytology. It has been
rather focuses on dead or dying cells and other materials more commonly seen in non‑Hodgkin’s lymphoma than
floating around the extracellular space. Also that in in Hodgkin’s lymphoma.[3]

Table 1: Physiological and pathological conditions exhibiting Rosai–Dorfman disease (RDD) is a benign proliferative
emperipolesis disorder of histiocytes.[1] Here, the involved histiocytes
Physiological Pathological phenomenon exhibit emperipolesis of lymphocytes, plasma cells,
phenomenon exhibiting exhibiting emperipolesis[1,7,9]
emperipolesis[1,5‑9] neutrophils and red blood cells [Figure 1].[7‑10] Emperipolesis
• E mperipolesis of Rosai‑Dorfman disease in a lymph node with mixed inflammatory infiltrate is a
erythroblasts by feature suggestive of RDD [Table 2].[10-12] Even CSF in
megakaryocyte in fetal liver
• Normally, 5% of the Autoimmune hemolytic anemia
patients of RDD is diagnostic of emperipolesis.[11]
circulating megakaryocytes
are seen associated with In neutrophilic emperipolesis seen associated with
emperipolesis engulfing cells fibrosis, the neutrophils interact with megakaryocyte
such as neutrophils and red
blood cells [Figure 1] through abnor mal P‑selectin localization on the
• In bone marrow aspirate Myelosclerosis demarcation membrane system (DMS).[12] In bone marrow,
and tissue culture, the
megakaryocytic emperipolesis has been reported to increase
megakaryocyte exhibits
emperipolesis in incidences of granulocytic or erythropoietic hyperplasia.
• Emperipolesis of Myeloproliferative disorders The emperipoletic activity of erythroblasts in liver has
lymphocytes by human
glial cells in brain
been found to increase in periods of high level of hepatic
• Emperipolesis of Idiopathic thrombocytopenic erythropoietic activity and relatively anemic fetal state.[13]
erythroblasts by purpura
megakaryocyte in fetal Neuroblastoma
liver Multiple myeloma
Giant cell carcinoma of lung
Multiple myeloma
Leukemia
Malignant lymphoma
Breast carcinoma
Emperipolesis of
oligodendrocytes in various
central nervous system
diseases including multiple
sclerosis, cerebral infarcts,
Creutzfeldt‑Jakob disease
Chronic metabolic disorders
Malignant lymphoma (more in
non‑Hodgkin’s lymphoma)
Neutrophilic emperipolesis
after sublethal irradiation, aging
and altered megakaryocytic
maturation associated with the Figure 1: Emperipolesis of different variety of cells (red blood cells and
gunmetal mutation
plasma cells) in a vacuolated space by a megakaryocyte

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Table 2: Immunoreactivity of histiocytes diagnostic for emperipolesis

Disease Cell exhibiting cell engulfment Positive Negative
Rosai‑Dorfman disease Histiocytes S‑100 protein, CD68, HAM56, alpha 1 antitrypsin, alpha 1 CD1a (Leu‑6)
chymotrypsin, lysozyme, Mac387, Ki‑1, CD30, Ber‑H2
Reactive lymphoid cell hyperplasia Histiocytes CD68 (+) S100 protein
CD1a

HISTOPATHOLOGIC CHARACTERISTICS

In emperipolesis, the engulfed cell is enclosed in a

membrane‑bound vacuole in the cytoplasm of host
cell. This gives a rim of clear halo around the engulfed
cell [Figures 1 and 2]. Sometimes, vacuolations are also
seen in the cytoplasm.[3] On occasion, internalized cells
appear to continue living within the host cell for brief
periods of time following the engulfment, sometimes even
dividing within the vacuole, in which they are housed. Some
internalized cells manage to escape from the host cell and
survive to continue life as an individual cell. As opposite to
phagocytosis, the engulfed cell here is not destroyed even
after entering the cytoplasm of the host cell.[3]
Figure 2: Emperipolesis of red blood cells in a vacuolated space by
PATHOGENESIS a megakaryocyte

Since the term “emperipolesis” was coined, several attempts natural killer cell‑mediated tumor cell death. Target cell
have been made to understand how a cell inhabits the other, membrane fluidity is essential for this interaction. This
and the biological relevance of this co-habitation with their process requires free calcium, adhesion molecules and
final respective fates. Emperipolesis is now understood as actin‑based cytoskeleton.[15] Occasionally, mitotic activity
a mechanism to improve cell survival and help prevent was also observed in the invaded natural killer cells inside
apoptosis of cells within the host cell or control cells that the host tumor cells after emperipolesis, similar to those
could be cytotoxic to the host cells.[13] observed in Overholtzer’s report, suggesting an attempt
to cell division within the host cell.[15,16]
Occurrence of emperipolesis in lymphomas is correlated
with the role of cytokines released by lymphoma cells. In the bone marrow, erythroblastic emperipolesis is
Some investigators opine that the phenomenon is a result believed to be due to binding of the erythroblasts to the
of active adherence of lymphocytes to tumor cells or ED2 antigen or to the 30 kDa heparin‑binding protein of
macrophages with a subsequent inclusion in vacuoles inside the macrophages.[13] No such obvious cell‑to‑cell binding
the cytoplasm of this cells.[8,14] and/or communication has been noted in the occurrence
of emperipolesis of erythroblasts by Kupffer cells in fetal
Wang and Li attempted to propose the mechanism behind liver.[13]
emperipolesis. They described this as a mechanism of the
natural killer cell to mediate tumor cell death. For this, the Emperipolesis of neutrophils in marrow fibrosis has been
membranes of both the target cell and the natural killer proposed to be a result of detection of P‑selectin on the
cell should be fluid enough to make this heterogeneous DMS of neutrophils. This is believed to be due to the
interaction successful enough, for its engagement with release of neutrophil enzymes, in close proximity to the
natural killer cells. They demonstrated at ultrastructural atypical granules within the cytoplasm of megakaryocyte,
level the disintegration of host tumor cells following causing the granules themselves to release their content
emperipolesis of natural killer through a lysosome‑mediated including growth factors such as transforming growth factor
degradation pathway. However, unexpectedly, few years in the microenvironment through the DMS.[12] Abnormal
later, they also discovered that some natural killer cells were P‑selectin localization on the DMS triggers therefore
disintegrated by tumor cells through a lysosome‑mediated might mechanism of pathologic neutrophil emperipolesis
mechanism, similar to what was observed in entosis. The within the MK, which may cause marrow fibrosis and also
authors suggested emperipolesis is a pathway to mediate extramedullary hemopoiesis in these mutants.

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Gupta, et al.: Emperipolesis, entosis and cell cannibalism

ENTOSIS Entosis also has been found to be leading to lysosomal

cell death [Figure 3].[19]
Overholtzer et al. observed a homogeneous cell‑in‑cell
phenomenon similar to emperipolesis and gave the term In this event, some invading cells try to escape through a
“entosis” to it (from the Greek word “entos” for “inside” transcytosis‑like movement, whereas a small percentage of
or “into”).[16] Here, a cell engulfs a cell of same type. While invading cells undergo cell division within the host cells.[6]
cells that are internalized by this mechanism are initially This suggests that emperipolesis and entosis primarily
viable, with the majority of them eventually undergoing a differ in the mechanism though the outcomes of both
nonapoptotic form of cell death that requires autophagy processes may vary from existence of the engulfed cell, to
proteins.[17] This was proposed as a process of cell‑in‑cell cell division, to escape through transcytosis.
invasion, which plays a physiological role in the elimination
of cells detached from a surface.[18] Previous literature supports the stimulation of entosis by
oncogene Kras, as one class of tumor suppressors. This
PATHOGENESIS involves the regulation of epithelial cadherins E and P.[19]
This oncogenic transformation in a cell leads to its capability
Entotic cell engulfment is induced by detachment of a cell to engulf the other cells [Figure 4]. This leads to physical
from the extracellular matrices and further potentiated elimination of the “loser” cells, which usually succumb to
by imbalances in actomyosin contraction between nonapoptotic cell death when the phagosome envelopes
the neighboring cells. Entosis is driven by imbalances the engulfed cell. This phagosome has membrane surface
in actomyosin contraction between the neighboring LC3 which then fuses with lysosomes. Entosis exhibits
cells.[17] This similar cell–to‑cell engulfment is mediated β‑catenin localization patterns that are indicative of a
by adherens junction molecules such as E‑cadherins, Rho cell junction‑mediated mechanism of engulfment.[19] The
GTPase and Rho‑kinase (ROCK)‑mediated actomyosin prognostic implications of entosis are varying in various
contraction within engulfing cells.[17] There is absence of studies. High number of cancer‑initiating cells (CICs) in
integrin signaling and force‑driven invasion of one cell high‑grade, aggressive breast cancers has been found to
into another cell. Cell engulfment requires actin, myosin be indicative of poor prognosis. In contrast, high levels
II, Rho and ROCK activity of the invading cell and of CICs correlated with a lower incidence of metastases
myosin‑based contractile force from the recipient cell. in pancreatic adenocarcinomas.[19]

Figure 3: Pathogenesis of entosis Figure 4: Schematic presentation of phenomenon of entosis

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Sun et al. proposed that the mechanic deformability of been engulfed, and heterotypic cell engulfment, wherein
the engulfing cell makes its function easier. As tumors are dissimilar cell is engulfed [Table 3].[22] Homotypic live cell
more mechanically heterogeneous than normal tissues, engulfment (among cells of the same type) mostly occurs
the tendency for tumor progression is further increased in cancers, probably reflecting major alterations in cellular
with an elevated mechanically deformable tendency of physiology, which are associated with oncogenesis and
the cancer cells. This increases motility, entotic activity tumor progression. Heterotypic live cell engulfment usually
and the metastatic potential of the tumor.[20] Transfection involves the ingestion of leukocytes by nonleukocytes (such
enforced expression of active KrasV12 further increases as epithelial cells or fibroblasts).[19]
this mechanical tendency to deformation. The effect of
KrasV12 relies on Rac1.[20] Knockdown of Rac1 suppresses OCCURRENCE
engulfment tendency (so‑called “winner” phenotype status)
conferred by KrasV12. On the other hand, expression of The earliest report of a cell–in‑cell phenomenon in
active Rac1 induces a “loser” status [Figure 3]. Entosis carried tumors was reported by Steinhans in 1891. The engulfed
out by “winner” cells constitutes a competitive advantage cell still remains alive when internalized, but the process
to the aggressive tumor cells by giving the capability to the implies its death.[18] The process of cannibalism has been
“winner cells” to retrieve amino acids and other building reported in breast carcinoma, giant cell carcinoma of lungs,
blocks from the engulfed cell or increasing their genomic gallbladder carcinoma, endometrial stromal carcinoma,
instability subsequent to mitotic aberrations.[21] malignant thymoma, malignant lymphoma, etc., In the
literature, cancer cannibalism has been used to differentiate
CELLULAR CANNIBALISM between benign tumors from malignant, but few studies
recently have reported its occurrence in giant cell tumor
A much related phenomenon is cellular cannibalism, which of tendon sheath and central and peripheral giant cell
is the ability of a cell to engulf another living cell of its granuloma (PGCG) of the oral cavity.[18]
own type or another. Leyden used the term, “birds” eye
cells for cells exhibiting this phenomenon.[22] Other terms In cannibalism, the tumor cells are seen engulfing cells
used in the literature to describe this phenomenon are such as other tumor cells, neutrophils and erythrocytes.
“cellular phagocytosis,” “cell phagocytosis,” “cell–in‑cell Sachin et al. have noted and studied the phenomenon of
appearance,” “cell‑in‑cell pattern,” “one cell delicately neutrophil‑tumor cell cannibalism (NTCC) in 500 cases of
wrapped around the next,” “tumor cell within a tumor cell,”
“phagocytosis of tumor cell by tumor cell” and “tumor cell
embraced by another tumor cell.”[23]

Self‑cannibalism (macroautophagy) has been described as

a process of cell repair, wherein there is a molecule and
organelle recycling of the engulfed cell, allowing it to survive.
In contrast to this term, xeno‑cannibalism signifies a process
where the engulfed cell is completely digested to death.[22]

The cannibalistic cell can engulf similar or dissimilar cell

types. Most of the times an inactive lying cell becomes a
favorite target of the cannibalistic cell. “Homotypic cell
engulfment” is a term used when similar cell types have
Table 3: Types of cell cannibalism
Homotypic cell engulfment Heterotypic cell engulfment
Cannibalistic Engulfed (seen in tumor cells of)
cell cell
Epithelial cells White blood Breast carcinoma Gall bladder
cells carcinoma
Fibroblasts White blood Lung carcinoma Endometrial
cells stromal carcinoma
Neural cells White blood Gastric carcinoma Malignant
cells thymoma
Giant cell Malignant
carcinoma of lung melanoma
Figure 5: Schematic presentation of cellular cannibalism

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Gupta, et al.: Emperipolesis, entosis and cell cannibalism

oral squamous cell carcinoma (OSCC). They found NTCC encourages cannibalization of these cells within other similar
in 1.4% of cases of OSCC. The internalized neutrophil tumor cells, in adverse conditions of hypoxia, decreased
showed different stages of degeneration. They concluded nutritional state and acidic states [Figure 6]. This leads to the
that NTCC can predict the biological behavior and could selection of certain resistant cell phenotypes over others in
be a useful prognostic marker for OSCC. The authors caustic environment. These malignant cells are highly virulent
have proposed NTCC as an important histopathological and cannibalize other malignant cells and help them survive
prognostic indicator in OSCC.[24] and progress in such difficult conditions. However, this
pathogenesis cannot be considered for the giant cells as seen
NTCC has also been reported in carcinoma arising in PGCG and central giant cell granuloma, as they possess
from gallbladder (anaplastic carcinoma), small intestine an inherent property of engulfment.[18]
(adenocarcinoma), pancreatic adenocarcinoma, infiltrating
duct carcinoma of breast, squamous cell carcinoma of larynx Krajcovic et al. suggested that cannibalistic cell engulfment
and pleomorphic giant cell carcinoma of lung, gallbladder, leads to polyploidy, as internalized cells disrupt the
pancreas and intestine. This neutrophilic engulfment helps cytokinesis of the engulfing cell. This behavior can
in immune evasion and tumor survival.[25‑29] promote tumor progression by inducing aneuploidy.
Cannibalism‑mediated chromosomal instability and
HISTOPATHOLOGIC CHARACTERISTICS aneuploidy may be one of the reasons for aggressive
behavior of any cancer.[18]
In cellular cannibalism, a cell gets entrapped within
another cell and is present in a vacuolated space. This At times, a malignant cell which has engulfed another
pushes the nucleus to the periphery. This mechanism has malignant cell might, in turn, get engulfed by a third
been proposed to create a favorable stay house for the malignant cell. The process is referred to as complex
tumor cells within the host immune cells, thereby escaping cannibalism [Figure 7]. Cannibalistic giant cells as well as
destruction [Figure 5].[22] stromal cells express histiocytic markers. The internalized
cells do not express bcl2, suggesting that this internalization
PATHOGENESIS OF CELL CANNIBALISM
induces apoptotic cell death.[22]
The mechanism of cannibalism has been attributed to the
The hidden state holds great possibility of the escape of
metabolic alterations in the malignant tumor cells, which
tumor cells from host immune system (immune escape).
The number of cannibalistic cells directly correlates
with the poor prognosis of the tumor. Cannibalistic
cells are thus well related to aggressive behavior,
anaplasia, invasiveness and metastatic potential of the
malignancy.[22,23] This opens a new arena of research to
definitely target such cells in tumor immunotherapy.
Studying the degree and extent of cannibalistic cells

Figure 7: Schematic presentation of malignant tumor cell cannibalism

Figure 6: Pathogenesis of cell cannibalism and complex cannibalism

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