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On the existence of filamentous structures in endothelial cells of the amphibian capillary.

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On the Existence of Filamentous Structures in
Endothelial Cells of the Amphibian Capillary’
Department of Anatomy, University of Washington,
Seattle, Washington
Although many investigators (Clark and
Clark, ’40, ’43; Le Gros Clark, ’45; Chambers and Zweifach, ’44; Zweifach and
Kossmann, ’37) denied active contractility
of the mammalian capillary, contractility
of the amphibian capillary has been generally recognized.
There are two opinions about the elements responsible for contractility in the
amphibian capillary. One view can be
ascribed to Rouget (1874, 1879), who described branching cells encircling capillaries in the hyaloid membrane of the frog.
He presumed that these were contractile
cells. Subsequent investigators have supported and extended these observations
(Krogh, ’22; Vimtrup, ’22, ’23; Krogh and
Vimtrup, ’32). Bensley and Vimtrup (‘28)
reported fibrillar structures in the “Rouget
cell” cytoplasm and took this as evidence
for their muscular nature.
On the other hand, the contractile nature of “Rouget cells” was questioned by
Clark and Clark (’25a, b). These authors
observed active contractility of capillary
endothelial cells in larval amphibia, where
“Rouget cells” are not developed, and in
regions of other capillaries where “Ftouget
cells” do not occur.
In the present study, capillaries in various organs of the amphibian were examined by means of the electron microscope
with special references to the existence of
filamentous structures in the endothelial
cells. Filaments resembling smooth muscle myofilaments have been found in amphibian endothelial cells, to which contractility has been described, but are absent
from the non-contractile mammalian blood
capillary endothe lial cells.
Animals examined were adult leopard
frog, Rana pipiens, and the salamander
Triturus viridescens viridescens. Materials
were fixed in situ in cold 2.5% OsO, buffered with s-collidine (Bennett and Luft,
’59), administered by injection into the
peritoneal cavity. After two or three minutes, portions of the mesentery and small
intestine were removed, cut into bits and
placed in fresh fixative for two hours at
4°C. ‘The specimens were dehydrated,
treated with 0.1% phosphotungstic acid
for 5 minutes in absolute alcohol, embedded and cut in the usual manner. They
were examined with an RCA EMU-2C electron microscope equipped with a special
stabilized power supply, an electrostatic
stigmator and a 50-cl objective aperture.
In some capillaries in the submucosa of
the intestine and the mesentery of the frog
and salamander, fine filamentous structures about 60-80 A in diameter can be
observed in the endothelial cytoplasm (figs.
1, 2 , 3 ) These filaments are grouped into
vaguely defined fibrils which run roughly
parallel to the endothelial cell surface. The
pictures have revealed no special relationships between these filaments and the
surface membrane or special attachment
areas at endothelial cell junctions.
Many vesicular profiles can be observed
within the endothelial cell cytoplasm.
These vesicles are similar to those reported
in mammalian capillaries by Palade (’53),
Moore and Ruska ( ’ 5 7 ) , Bennett, Luft and
Hampton (’59). They may be involved
in pinocytosis (Bennett, ’56, ’57).
Small cell processes which make intimate contact with the outer surface of the
endothellial cell (fig. 2, arrow) can be obSupported in part by a grant from the Life
Insurance Medical Research Fund, G-56 and 47.
2 Present
address: Department of Anatomy,
Hiroshima University, Hiroshima, Japan.
served. No filamentous structures have
been detected in these processes. These
processes may correspond to the processes
of "Rouget cell" or "pericytes" of Zimmerman ('23).
Many capillaries of the mammalian intestine, subcutaneous connective tissue
and mesentery have been examined for the
purpose of comparison, but no filamentous
structures have been detected in the endothelial cells. This is in confirmation of
prior observations of Moore and Ruska
( ' 5 7 ) , Bennett, Luft and Hampton ('59)
and others.
The amphibian endothelid filaments observed in this study have roughly the same
dimension as the gliofilaments (Bairati,
Pernis, Frigerio and Bairati, '58; Fleishhauer, '58) the tonofilaments in epidermal
cells (Horstmann and Knoop, '58; Odland,
'58) and the myofilments in the myoepithelial cells (Langer and Huhn, '58) and
in smooth muscle cells (Mark, ' 5 6 ) , (Hanson and Lowy, '57). There are no distinct
morphological differences between these
various filaments, but several facts suggest
that those observed in the present study
may correspond to myofilaments.
1. The filaments observed in this study
have a parallel orientation and are grouped
into ill-defined fibrils, as are the myofilaments of typical smooth muscle.
2. There is no relation between these
filaments and the cell membrane or attachment areas as is the case with tonofilaments.
3. They are found in the amphibian
capillary, which is contractile, and are not
found in the usual type of mammalian capillary, which is considered to be non-contractile.
4. They resemble the distinct myofilaments in earthworm capillary endothelial
cells (Hama, '60).
The fact that not all of the endothelial
cells contain filamentous structures seems
to agree well with the observations by
Clark and Clark ('25a,b) that the amphibian capillary does not contract everywhere
evenly along its length, but contracts at
several places independently.
The existence of myofilaments in the
amphibian capillary endothelial cells reported in this study seems to present a
morphological basis for their contractility.
Capillaries in the submucosa of the intestine and in the mesentery of frogs and
salamanders were examined with the electron microscope.
In some of the endothelial cells, filamentous structures of about 60-80 A in diameter can be observed. They run parallel
to each other and are grouped irregularly
into ill-defined fibrils.
It is suggested that these filaments may
be myofilaments and be responsible for contractility in amphibian blood capillaries.
The author is greatly indebted to Dr. H.
Stanley Bennett who gave him the opportunity of doing this work and also invaluable kind advice during the course of this
Bairati, A., B. Permis, G . Frigerio and A. Bairati,
Jr. 1958 Submicroscopic structure of gliofibrils. 2. Wiss. Mikroskop., 63: 4 2 3 4 2 6 .
Bennett, H. S. 1956 The concepts of membrane
flow and membrane vesiculation as mechanisms for active transport and ion pumping. J.
Biophys. Biochem. Cytol., 2: (Suppl.) 99-103.
1957 Some contributions of the electron microscope to cytology and histology.
Electron Microscopy, Proc. 1st Regional Conf.
Electron Microscopy Asia and Oceania, Tokyo,
1956. Electrotechnical Laboratory, Tokyo, p. 88.
Bennett, H. S., and J. H. Luft 1959 s-Collidine
as a basis for buffering fixatives. J. Biophys.
Biochem. Cytol., 6: 113-114.
Bennett, H. S., J. H. Luft and J. C. Hampton
1959 Morphological classifications of vertebrate blood capillaries. Am. J. Physiol., 196:
Bensley, R. R., and B. Vimtrup 1928 On the
nature of the Rouget cells of capillaries. Anat.
Rec., 39: 37-55.
Chambers, R., and B. W. Zweifach 1944 T3pography and function of the mesenteric capil.
lary circulation. Am. J. Anat., 75: 173-206.
Clark, E. R., and E. L. Clark 1925a A. The development of adventitial (Rouget) cells on the
blood capillaries of amphibian larvae. Ibid.,
35: 239-264.
1925b B. The relation of (Rouget) ceIIs
to capillary contractility. Ibid., 35: 265-282.
1940 Microscopic observations on the
' extra-endothelial cells of living mammalian
blood vessels. Ibid., 66: 1 4 9 .
- 1943
Caliber changes i n minute bloodvessels observed i n the living mammal. Ibid.,
73: 215-250.
Fleischhauer. K. 1958 Uber die Feinstruktur
der Faserglia. 2, Zellforsch. Mikr. Anat., 47:
Hama, K. 1960 'The fine structure of some
blood vessels of the earthworm. J. Biophys.
Biochem. Cytol., 7: 717-723.
Hanson, J., and J . Lowy 1957 Structure of
smooth muscles. Nature, 180: 926.
Horstmann, E. and A. Knoop 1958 Elektronenmikroskopische Studien a n der Epidermis-I
Rattenpfote. Z. Zellforsch. Mikr. Anat., 47:
Krogh, A. 1922 The Anatomy and Physiology
of Capillaries. Yale University Press, New
Krogh, A., and B. Vimtrup 1932 The capillaries. In: Special Cytology, vol. I, E. V. Cowdry, ed. Paul B. Hoeber, New York, pp. 475503.
Langer, E., and S. lluhn 1958 Der submikroskopische Bau der Myoepithelzelle. Z. Zellforsch. Mikr. Anat., 47: 507-516.
LeGros Clark, W. E. 1945 The Tissues of the
Body-An Introduction to the Study of Anatomy. Clarendon Press, Oxford.
Mark, J . S. T. 1956 A n electron microscope
study of uterine smooth muscle. Anat. Rec.,
125: 473493.
Moore, D. H., and H. Ruska 1957 The fine
structure of capillaries and small arteries. J.
Biophys. Biochem. Cytol., 3: 457-462.
Odland, G. F. 1958 The fine structure of the
interrelationship of cells in the human epidermis. Ibid., 4: 529-538.
Palade, G. E. 1953 Fine structure of blood capillaries. J. Appl. Physics, 24: 1424.
Rouget, C. 1874 Note sur le dkveloppement de
la tuiiique contractile der vaisseaux. C. R.
Acad. Sci., 79: 559-562.
1879 Sur la contractilitk des capillaries
sanguins. Ibid., 88: 916.
Vimtrup, B. 1922 Beitrage zur Anatomie der
Capillaren. I. Uber contractile Elemente i n der
Gefasswand der Blutcapillaren. Z. Anat. Entwicklungs-geschichte, 65: 150-182.
1923 Beitrage zur Anatomie der Capillaren. IT. Weitere Untersuchungen iiber contractik Elemente in der Gefasswand der Blutcapillaren. Ibid., 68: 469482.
Zimmerman, K. W. 1923 Der feinere Bau der
Blutcapillaren. Ibid., 68: 29-109.
Zweifach, B. W., and C. E. Kossmann 1937
Micromanipulation of small blood vessels in the
mouse. Am. J. Physiol., 120: 23-35.
Figures 1, 2 and 3 show high power electron micrographs of a part of the capillary endothelial cells in the mesentery of frog, i n the submucous tissue of the frog intestine and in
the mesentery of the salamander, respectively.
Many vesicular structures are observed in the endothelial cells. In addition fine filaments
which r u n parallel to each other and which are grouped into poorly-defined fibrils can be
observed. These are thought to be myofilaments responsible for amphibian endothelial cell
A small cell process close to the outer surface of the endothelial cell is observed (fig. 2,
Figure 1: x 62,000; figure 2 : x 62,000; figure 3:
lumen; e, endothelial cell; m, mitochondria.
78,000. Abbreviations: cl, capillary
Kiyoshi Hama
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endothelial, structure, amphibia, filamentous, existencia, capillary, cells
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