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The engulfment of living blood cells by others of the same type.

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Departsteat of Enibr.uology, Cariic.Uk Imtihtiosr
Baltimore, .Varyleiid
In the course of our iiivestigations on the behavior of t
white blood cells in hanging-drop cultures of whole blo
from the frog, we have occasionally noted engulfed livi
cells. The occnrrence of ingested dead white cells within t
large mononiiclears was common, but the prcsence of livi
mononuclear8 within others of the same type %-asso rare th
it attracted our attention at once. In the few aeries where
did occur there were many instances in almost every cultm
A6 each series was made from a difloront animal, but othc
wise in approximately the same manner, the indications a
that this peculiarity was dopendent npon some precsistii
caondition in tho animal itself hefore the blood was drai3
from the heart. As is well kiiowii, frogs are subject
various infections and parasites, and it may be that somethi:,
of this iiatnro predisposed the large mo~ioniiclcarcells
exhibit this caiinibalistic teatleiicy in the hangiiig drops.
It is a rare phenomeiion, and the only other case where Y
have observed it among thousands of cultures aiid aproac
of living cells has been in pulmonary tuberculosis of tl
rabbit ;here wc have occasionally seen in living spreads loot
epithelioid cells (hyportropliied monocytes) containing ot
and even t-xo living epitlielioid cells. These rare examplc
done afford iiadou1)ted evidence of the existence of this pi.#
cess. The spreads from the tnberculous lungs where NIIC
cells wcre fouiitl had been previously treated with nentrali-ed Locke solution and the cells observed had become detached
from the small piece of tissue and were floating free in the
surrounding fluid, where they were watched as they turned
about in various ways. One could thus be absolutely sure
that the engulfed cell was actually within the larger cell. The
proof that the engulfed cells were living was the fact that
they contained many graiiules that stained intensely with
neutral red, and a nucleus that remained unstained. Ingested dead cells, on the contrary, stain diffusely, the nucleus
usually more deeply than the cytoplasm. Observations oil
spreads from tnhercnlous lungs show that this process can
take place within the body.
It is impossible to determine iii fixed and stained tissuc
whether engulfed cells a r e or a r e not alive at the time of
fixation. The oiily certain method for determining this question is by observation of the living cells.
Living white blood cells i n hanging-drop blood and lymphnode cultures frequently come into intimate contact with one
another without any indication of the engulfment of one by
the other, and we have frequently observed small lymphocytes
migrating about on the surface of a large epitlielioid or giant
cell without being engulfed. Such cells may, however, ingest
many dead lymphocytes.
The factors which produce the extraordinary change in the
moiiocytes, enabling them to engulf living cells, a r e totally
uiiknown, but they undoubtedly a r e pathological and a r e
probably responsiblc f o r the fatal course of certain types
of anaemia.
I n one series (15-10-24), where the phenomenon of eiigulfmeiit of living cells mas especially noted, there were oii the
iiiiitli day many large moiiocytes or epithelioid-like cells, often
iii clusters, that were quite heavily laden with neutral-red
granules. The cluster shown in figure 1 was photographed
after the cells liad been stained with neutral red and wliilc
they n’erc still tilive. Most of tlic hloocl was waslietl off with
a neutral-red 1,oeke soliitioii, arid orily tliose cells that were
stlick to tlic covci*-glasswmaiiictl. The iicutral-red gi-aiiules
(1)lack iii the ~liotogl*ii~)11)
o ~ c u p ?niost of the cell body. Tlic
iiwlci ( I to 3 ) ai’c at or iicar the periphery of the cell arid a r e
clear iuistaiiictl oval hoclics. I n spite of the fact that thesc
cells n o i heavily
loatlctl with granules, it was possible sometimes to observe in the cciitcr of tlic ccll ii radial arrangem w t of tlicm about H c a i t ral point, presnmably tlic ceiitrosome. Similnr cells from youiigcr cul turw of otlier series,
wliicli I i a v t h hccomc more csteiisirelp flatteiied out oil the
cover-glass aiitl wliic+hcontain fewer gi~iiiules,show a radial
arraiigcmclii t of mit o<*liondriaabout tlie centrosome. Tlic
monoiiuclcai* c ~ l sliowi
in figure 3 is from a sis-day culture
that liilil 1)ecii u.aslietl with , J a i i i i ~ - g r c ~Timi 3 < C solutioii and
thtw tisctl with iotliiic vap0r.
The graimles tlint ortliiiarily take up neutral red a r e not
staiiied a~ tlceply by tlie iotliiie as the mitochoiitlria. Tho
lattclr n w c l r a r l ~scc’ii
~ mid have a radial arrangement about
tliv ccwti*osome.
111tlicl upper p a i t of figure 1 thew is a Iargc? giaiit cell,
witli tlirce or four nuclei, w ~ i i c ~ i a seiigulfecl i~ mecIium-sizeci
living cell of the same type. The latter is enclosed in a large
clear niciioI(~, tlic c~mtoiitsof mliicli (lid riot take up tlie
iienti*al rccl. A s c w i 1w we11 in the pliotogmph, the engulfed
ccll is ~)ucltcdfnll of iicutral-i.ecl-stniiietl grminlcs aiid its
clcl-rr nucleus lies at the peripliery.
JVe Iia\-e not wtiiall!- watcliccl tlica ciiigulfmeiit of such living
( d s , hiit various stages in what appcai*s to be the process
w-ei-c’ foniict in this same culture. 111 figi’urc3 is t o be seen tlic
hgiiiiiiiig of tlic pi*occss. He1.e the lai*gercell ( a ) is flowiiig,
as it were, aroiiiitl the smallor cell ( b ) . The surfaces of the
two c ~ 4 ssix' iii iiitimritc eontact witliont a n j r fluid between
them. Figure 4, fi-om tlir: same d t u w , slio\vs aii eiigulfing
c ~ ~t~xteidiiig
more t l i m 1inlf-wa;v aroiintl it large biiiucleate
cell. Both cells a1.c 1-iclily suppliecl with rieutrczl-red-stainiii#
gi*aiiiilcs. fi’igui*c~3 s h o w s a fr(~s1ilynignlfecl living cell.
Oiir reason f o r considering this as hariiig been recently
engulfed is the fact that there is very little indication of fluid
about it. Since tho two previons figures indicatc that the
two cells are tlircctly iii coiitaet during the eiigulfiiig I J ~ O C (w, we have naturally coiicludetl that this same wlatioii
would prevail for some time after complete engulfment. How
loiig a time siich a rclationship persists, we cannot tell, but
it is apparent that the engulfed cell ultimately becomes surrounclccl by fluid, as in figures 1 and 6. This fluid is differciit from that in the ordinary raciioles in that it does not
take up the neutral red. The ordinary vacuoles arc either
cligcstive or degenerativc. In the latter case they arise from
autodigestion and accumulation of waste products or some
associated process. The fact that the fluid surrounding the
engulfed living cells does iiot take up neutral red indicates
tlint it is iiot digestive in nntnre o r does not contain suhstances 14iat liave ;1 special affinity for neutral red. Tt is
evident that neutral red passes through this fluid, for it acciimnlates in the granules of the engulfed cells.
Since these engulfing cells are against the cover-glass, it
might be supposed that the engulfed cells are not really
within, but merely between them and the cover-glass. (.'arefiil
examination, however, revealed the fact that the engulfed cells
anti the fluid about them mere completely surrounded by a
thin layer of cytoplasm. The ma-stainability of the fluid of
the vacuole by neutral red and tlie fact that the eiigulfcd
(d(i11s arc alive suggest thiit the process of engulfing is here
somewhat different from that of ordinary phagocytosis, in
t h a t thc lining of the vacuole corresponds perhaps to, ant3
was originally a part of, the external surface of the engulfing cell. In other w70rcls, tlicse ciigulfed cells are not taken
into thc cytoplasm. In ordinarv phagocytosis that part of
tlic external surface whidi snrrounds the ingested particle
is supposed to disappear o r bccwme transformed into ordinary
interior cytoplasm by liquefaction a t the place wliere the iiipcstctd particle enters. I t wonld be very difficult, Iio\vcvchr,
t o prove clefiiiitcly the existelice or absence of a thin film of'
tlirt estc1riial layclr of tlie c ~ l alwut
ordinary ingest I)articlcs.
We have occasionally noted an engulfed living cell containing another engulfed living cell. The method by which
this is accomplished is probably similar to that already noted
f o r the engulfing of one cell by another. It is possible that
the condition shown in figure 6 represents the manner in which
this takes place. The large mononuclear cell ( u ) with a large
vacuole contains a living engulfed cell ( b ) . The cell ( a ) is
in turn partially surrounded by two cells ( c and d ) which are
spreading aroniid it. Had one of the latter completely spread
around the cell, the condition noted ahove would have been
obtained. Occasionally a living cell may contain two engulfed cells; sometimes they appear to be in a common
vacuole, sometimes in separate vacuoles.
Our observations are too fragmentary t o enable us to determine at present the fate of the engulfed living cells. The
occurrence of this phenomenon has only accidentally been
observed, and no attempt has been made to control it and
produce it at mill. As already noted, the phenomenon is
probably dependent upon the condition of the blood before
it was withdrawn from the heart. One of the surprising
things about the process is the apparent lack of any tendency
of fusion between the engulfed and engulfing cells, in spite
of the fact that they are closely attached during this process
and have every opportunity for fusion.
All the figures except figure 2 a r e from a uine-(lay living culture of frog’s blood
that was washed 111 iieutinl-red Locke solution. The liviiig cells are full of deeply
stained red granules which photograph black. Tlie clear unstained nuclei are
:it or near the periphery. The iu:igiiificatioii for all figures is 700 diameters.
1 Living large inoiioiiuclear cells. About the cluster a r e distorted red blood
cells. The giant cell a coiltailis mi eiigulftd living cell of the same type.
2 Large moiioiiuclear cell spread out on the cover-glass. Tlie mitochondria
a r e more or less railiallj :iii:nigetl allout the centrosome. Six-day culture, Janus
green, iodine vapor.
3 Showing the beginning of the process of engulfment of oiic living cell by
another of the same type.
4 More advanced stage of engulfnient of one living cell by another, the latter
with two nuclei.
.i Freshly engulfed living cell.
6 Mononuclear cell ( a ) with a In1 g e 1ion-staiixil)le vacuole containing a living
cell ( b ) . The cells r :mtl t7 appear to he surrounding the cell a.
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