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The nuclear fibrous lamina in human cellsStudies on its appearance and distribution.

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The Nuclear Fibrous Lamina in Human Cells:
Studies on Its Appearance and Distribution
ARTHUR H. COHEN AND JAMES R. SUNDEEN
Department o f Pathology, Harbor General Hospital, Torrance,
California 90509 and The University o f California, Los Angeles
School o f Medicine, Los Angeles, California 90024
ABSTRACT
The nuclear fibrous lamina, a structure of unknown function,
is situated at the nuclear periphery directly apposed to the inner nuclear membrane. Although it has been well described in invertebrate and many non-human
vertebrate cells, its occumence in human tissue has not been emphasized. This
survey of a large variety of human cells has documented the lamina to be present, although of varying thickness, in a large number of cell types. It is consistently thickest in mesenchymal or mesenchymally derived cells and its appearance and thickness is not correlated with pathologic alterations.
The nuclear fibrous lamina, a structure
located at the periphery of the nucleus, was
first described by Pappas ('56) in Amoeba
proteus and emphasized and studied i n detail by Fawcett ('66) and Patrizi and Poger
('67) i n vertebrate nuclei. While many of
the early reports (Beams et al., '57; Coggeshall and Fawcett, '64) stressed its presence
in invertebrate and nonhuman vertebrate
cells, few studies deal with this structure
in human tissue. The purpose of this communication is to report on our survey to
determine the appearance and distribution
of the nuclear fibrous lamina in human
cells, and to draw attention to this little
known structure.
The remainder of the tissues were fixed
directly in osmium. The thin sections were
stained with lead citrate.
All photographs, numbering over 13,000,
were reviewed for the presence of the nuclear fibrous lamina. No attempt was made
to re-examine the tissue if the nuclei were
not of a sufficient magnification to identify
the detail of the inner aspect of the nuclear
membrane or if the nuclei were not photographed. As the object of this study was to
document the presence of this structure
in a wide variety of human tissues, only
a semiquantitative indication of its frequency was determined. In order to establish a rough indication of the actual and
relative thickness, measurements of ranMATERIALS AND METHODS
domly selected nuclear fibrous laminas
Photographs from the files of the Elec- were performed. Precise quantitation for
tron Microscopy Laboratory of Harbor Gen- all cell types was not done. Additionally,
eral Hospital, containing over 1,000 speci- the presence or absence of pathologic altermens of human tissue, were reviewed. The ations in the affected cells or i n cells or
vast majority of tissue was from renal bi- tissues adjacent to the affected cells was
opsies (30 % ), although specimens of skin noted.
(7% ), liver (7% ), bone marrow ( 5 % ),
RESULTS
and skeletal muscle ( 11% ) were in plentiI
n
human
cell
nuclei the nuclear fibrous
ful amounts. With few exceptions, virtulamina is a band of variable thickness of
ally every organ was represented.
Most specimens were fixed initially in finely granular, medium electron dense
2.5% glutaraldehyde in cacodylate buffer material directly apposed to the inner
for one and one-half hours, and, after membrane of the nuclear envelope and in
washing in buffer, were postfixed in 1% direct contact with marginal condensates
of nuclear chromatin. It is absent, along
aqueous osmium tetroxide for one hour -__
and then processed in the usual manner.
Received Dec. 19, '75. Accepted M a y 28, '76.
ANAT. REC., 186: 471-476.
471
4 72
ARTHUR H. COHEN AND JAMES R. SUNDEEN
with the chromatin, beneath the sites of
the nuclear pores (fig. 1 ) . The thinnest
lamina, noted in epithelial cells, had a
range up to 470 A. The thickest ones measured 610 A to 725 A and were found
predominantly in fibroblasts and cells with
similar structural characteristics. At the
microscope, the minimum magnification
necessary to document the presence of the
thinnest laminas was in the range of
X 8,700, in addition to the aid of the magnifying loop ( x lo).
A well defined nuclear fibrous lamina
was found to be present in the nuclear
periphery of a variable number of many
of the cell types examined. Its thickness
and prominence varied from cell type to
cell type and also from one cell to another
of the same variety. The presence or absence of pathologic changes in either the
cell in question or in adjacent tissue, in
general, bore no relationship to the thickness and prominence of the fibrous lamina.
However, in any circumstance, mesenchyma1 or mesenchymally derived cells contained the largest laminae. Fibroblasts,
especially of the skin, but also of other
locations, had the thickest lamina (fig. 2).
Modified fibroblasts, including mesangial
cells of the renal glomerulus and myofibroblasts, as well as smooth and skeletal muscle cells from all locations, and chondrocytes, were similarly affected. In epithelial
cells, the presence of this structure was
more difficult to document because of its
relatively thin and delicate nature. Nevertheless, it was noted in renal glomerular
and tubular epithelium, vascular endothelium from all locations, type I pulmonary
alveolar pneumocytes, cutaneous cells, including keratinocytes (fig. 3 ) , Langerhans
and those of sweat glands, hepatocytes
(fig. 4 ) , small intestinal mucous epithelium, thyroid follicular cells, parathyroid
chief cells, and urinary bladder transitional
epithelium. In all normal hematopoietic
cells, the lamina was extremely thin, and,
when present, was generally of equal size
in immature and mature forms; however,
in mast cells, plasma cells, lymphocytes
and most leukemic forms, it was more
prominent. Schwann and other cells of the
nervous system had laminas of intermediate thickness.
It is necessary to visualize in detail the
nuclear envelope, including inner nuclear
membrane, to determine the presence of
this structure. In those instances when
the lamina is absent, the marginal condensates of chromatin, which are usually
quite sparse, are in direct contact with the
inner membrane (fig. 5). The characteristics of the thinnest laminas are, of course,
identical qualitatively to those of the more
substantial ones (fig. 6 ) . It should be
noted that laminas have uniform thickness along the nuclear periphery except
under a pore. However, it may be difficult
to distinguish thin ones from chromatin
if the sections are too thick or too heavily
stained.
The mode of primary fixation did not
affect the ability of the observer to identify
the lamina. The same finely granular internal structure was noted with both osmium and glutaraldehyde, but it appeared
slightly more dense after glutaraldehyde.
DISCUSSION
We have demonstrated the nuclear
fibrous lamina to be present in a n extremely large number of types of human
cells and conclude that i t is a normal
structure of varying thickness.
First described by Pappas (’56) i n the
nucleus of Amoeba proteus, the presence of
this structure in many other invertebrates
was subsequently documented (Beams et
al.,’57; Coggeshall and Fawcett, ’64). Its
appearance in invertebrate nuclei is that
of a complex, thickened, filamentous mesh
adherent to the inner surface of the nuclear envelope and arranged around nuclear pores in a “honeycomb” pattern.
Fawcett (’66) described what he considered an analogous structure i n the nuclei
of several vertebrate tissues, and others
noted the lamina in a variety of cell types
(Patrizi and Poger, ’67). Although this
filamentous nature is well documented i n
invertebrate cells, its composition in the
nuclei of vertebrate species is that of a
“fine textured band’ between the nuclear
envelope and condensations of chromatin.
It is for this reason that objections to its
appelation as a fibrous structure have been
raised; zonular nucleum limitans (Patrizi
and Poger, ’67) and internal dense lamella
(Franke and Scheer, ’74) have been advo-
NUCLEAR FIBROUS LAMINA IN HUMAN CELLS
473
cated as alternate names. Nevertheless, the sists almost exclusively of acidic proteins
term "nuclear fibrous lamina" has been and relatively little DNA or RNA.
The present survey was undertaken beemployed with increasing frequency in the
cause the nuclear fibrous lamina was frerecent literature.
In vertebrates, the reported thicknesses quently recognized by us in many human
of the lamina have varied, ranging from cells. There are only a few reports which
140 (Kumegawa et al., '69) to 950 A deal exclusively with its appearance in
(Ghadially et al., '72). Although it has either normal or pathologic human tissue.
been suggested (Patrizi and Poger, '67) Normal human cells, including those of
that its size varies with the method of fixa- Brunner's glands (Leeson and Leeson, '68)
tion, it is currently believed that the vari- and fibroblasts and amniotic cells in tissue
ous fixatives alter only the staining quality culture( Patrizi and Poger, '67), have been
of the structure (Ghadially et al., '74), a noted to contain it. A fibrous lamina has
finding that is in agreement with our been described in nuclei of human cells
results. Ghadially and coworkers ('72) have from pathologic synovial tissue (Ghadially
demonstrated convincingly that the thick- et al., '74), a salivary gland mixed tumor
ness of the lamina in rabbit cartilage is (Kumegawa et al., '69 1, immature reticuvariable and that i t is a dynamic and lar and plasma cells (Sane1 and Lepore,
changing structure. I n other studies, they '68) and in cells with characteristics of
have indicated that in articular cartilage of myofibroblasts (Ryan et al., '73) in patients
the rabbit it is thickest in mature animals, with the Winchester syndome, an inherited
thin in growing animals, and absent in disorder with skeletal, cutaneous and ocunewborn rabbits (Oryschak et al., '74). lar manifestations (Cohen et al., '75). Our
Coggeshall et al. ('74) in a study of lumbo- survey greatly extends the list of human
sacral ventral root unmyelinated axons of cells in which the fibrous lamina is seen
the cat, observed prominent fibrous lam- and suggests that it is at least a transient
inas in nuclei of small Schwann cells, structure in most human cell types. We
whereas large cells had either thin laminas have noted the fibrous lamina in the same
or were lacking them completely. The au- tissues in health and disease, establishing
thors were unable to explain this observa- that its appearance is not in itself a n ultrastructural feature of pathology. We have
tion.
Although its function is not known, sev- also noted considerable variation in the
eral theories have been advocated. In the prominence of the lamina in similar cells
amoeba and other invertebrates, it was in the same tissue specimen, lending crethought to serve a skeletal function, sup- dence to the dynamic concept of this strucporting the nuclear envelope of rather large ture.
In summary, we suggest that the nunuclei (Coggeshall and Fawcett, '64). However, many other invertebrate species with clear fibrous lamina is a normal but apparequally large nuclei do not demonstrate ently changing feature of most human
the lamina, and vertebrate cells with much cells and that it may be found in all human
smaller nuclei reveal its presence; these tissue with careful electron microscopic
facts, combined with the evidence that it study.
is a changing structure, tend to contradict
LITERATURE CITED
this thesis. Fawcett ('66) suggested that the
fibrous lamina may in some way have Beams, H . W., T. N. Tahmisian, R. Devine and
a role in nucleocytoplasmic exchange
E. Anderson 1957 Ultrastructure of the nuthrough the nuclear pores, but there has
clear membrane of a Gregarine parasitic in
grasshoppers. Exp. Cell Res., 13: 200-204.
been little evidence to refute or support
R. E., J. D. Coulter and W. D.
this conjecture. Ghadially ('72) believes its Coggeshall,
Willis, Jr. 1974 Unmyelinated axons i n the
appearance is correlated with cell metabventral roots of the cat lumbosacral enlargeolism based upon studies of synthesizing
ment. J. Comp. Neur., 153: 39-58.
chondrocytes. It is considered of protein- Coggeshall, R. E., and D. W. Fawcett 1964 The
fine structure of the central nervous system of
aceous composition; cytochemical studies
the leech Hirudo medicinalis. J. Neurophysiol.,
of Stelly et al. ('70) indicate that this struc27: 229-289.
ture in neuronal nuclei of Drosophila con- Cohen, A. H., D. W. Hollister and W. B. Reed
474
ARTHUR H . COHEN AND JAMES R. SUNDEEN
1975 The skin in the Winchester syndrome.
Arch. Dermatol., 111: 230-236.
Fawcett, D. W. 1966 On the occurrence of a
fibrous lamina on the inner aspect of the nuclear envelope i n certain cells of vertebrates.
Am. J. Anat., 119: 129-146.
Franke, W. W., and U. Scheer 1974 Structures
and functions of the nuclear envelope. In: The
Cell Nucleus. Vol. 1. H. Busch, ed. Academic
Press, New York, pp. 256-257.
Ghadially, F. N., R. Bhatnagar and J. A. Fuller
1972 Waxing and waning of nuclear fibrous
lamina. Arch. Path., 94; 303-307.
Ghadially, F. N., A. F. Oryschak and D. M.
Mitchell
1974 Nuclear fibrous lamina i n
pathological human synovial membrane. Virchows Arch. Abt. B. Zellpath., 15: 223-228,
Kumegawa, M., G. G. Rose, M. Cattoni, M. A. Luna
and P. G. Stimson 1969 Electron microscopy
of intranuclear inclusions in a mixed tumor.
Oral Surg. Oral Med. Oral Path., 28: 89-96.
Leeson, T. S., and C. R. Leeson 1968 The fine
structure of Brunner’s glands in man. J. Anat.,
263-2 76.
Oryschak, A. F., F. N. Ghadially and R. Bhatnagar
1974 Nuclear fibrous lamina i n the chondrocytes of articular cartilage. J. Anat., 118: 511515.
Pappas, G. D. 1956 The fine structure of the
nuclear envelope of amoeba proteus. J. Biophys.
Biochem. Cytol., 2: 431-434.
Patrizi, G., and M. Poger 1967 The ultrastructure of the nuclear periphery. J. Ultrastruct.
Res., 17: 127-136.
Ryan, G. B.. W. J. Cliff, G. Gabbiani, C. Irle, P. R.
Statkov and G. B. Majno 1973 Myofibroblasts
in a n avascular fibrous tissue. Lab. Invest., 29:
197-206.
Sanel, F. T., and M. J. Lepore 1968 Granular
and crystalline deposits i n perinuclear and
ergastoplasmic cisternae of human lamina propria cells. Exp. Molec. Path., 9: 110-124.
Stelly, N., B. J. Stevens and J. Andre 1974
Cited by Franke and Scheer.
PLATE 1
EXPLANATION OF FIGURES
1 Portion of nuclear periphery of fibroblast. Note the thick nuclear
fibrous lamina (arrows) situated between the nuclear membrane and
the peripheral condensates of chromatin. x 51,300.
2
Cutaneous fibroblast from patient with mixed mucopolysaccharide
storage disease. Cytoplasmic vacuoles with flocculent material exists i n
this cell with a well defined nuclear fibrous lamina (arrow). X 25,100.
3
Basal cell of epidermis demonstrating a clearly delineated lamina
(arrow). Note the numerous melanin granules. x 33,000.
4
Hepatocyte nucleus showing thin and tenuous fibrous lamina (arrows)
which, despite its size, bears same relationship to nuclear membrane
and chromatin as thicker lamina in other cells. x 35,000.
NUCLEAR FIBROUS LAMINA I N HUMAN CELLS
Arthur H. Cohen and James R. Sundeen
PLATE 1
475
NUCLEAR FIBROUS LAMINA IN HUMAN CELLS
Arthur H. Cohen and James R. Sundeen
EXPLANATION OF BIGURES
5 Nuclear periphery without a fibrous lamina. The chromatin is thinly
dispersed and only slightly aggregated at the nuclear envelope. This
is a n epithelial cell i n a renal glomerular crescent. x 13,500.
6
476
Extremely thin and barely perceptible fibrous lamina (arrow) i n a
parietal epithelial cell of a renal glomerulus. x 26,500.
PLATE 2
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