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Pulmonary appendix of the short-tailed shrew BlarinaA unique immunologic organ.

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THE ANATOMICAL RECORD 266:184 –191 (2002)
DOI 10.1002/ar.10056
Pulmonary Appendix of the ShortTailed Shrew (Blarina): A Unique
Immunologic Organ
WESLEY WILKIN PARKE*
Robert E. Van Demark Institute of Anatomical Research, Anatomy Division of Basic
Medical Sciences, University of South Dakota School of Medicine,
Vermillion, South Dakota
ABSTRACT
The right bronchus of the short-tailed shrew, Blarina brevicauda, terminates in a nonrespiratory pulmonary appendix (PA) containing two bronchial extensions. The experimentally demonstrated ability of these structures to collect and peristaltically expel aspirated material was initially
assumed to be a sufficient reason for their developmental persistance, but
as bronchus associated lymphoid tissue (BALT) became a subject of immunologic interest in other species, a possible immunologic role for the concentrations of BALT observed in the shrew PA were investigated. As the
BALT of the PA contained many well-differentiated plasma cells and numerous particle-containing macrophages, 6-␮ paraffin sections were treated
with an immunoperoxidase avidin-biotin preparation that chromogenically
identified alpha chains of IgA in many of the PA plasma cells and their
associated luminal secretions. Also, vascular injections revealed that the PA
had a complex relationship with anastomotic sinusoids connecting the bronchial and pulmonary circulation systems, and scanning electron microscopy
showed that the luminal epithelial surfaces of the PA were virtually identical to the scattered BALT aggregates in the bronchi of other animals. It
thus appeared that these unique structures in the shrew are morphologically and topographically suited to receive aspirated antigens that induce
secretory IgA production, while possibly providing other humoral and cellular immunologic products to the general circulation. Anat Rec 266:
184 –191, 2002. © 2002 Wiley-Liss, Inc.
Key words: BALT; IgA; bronchial epithelium; Insectivora; pulmonary clearance mechanisms; antigen sampling
The right lung of the short-tailed shrew, Blarina brevicauda, bears an extrapulmonary appendage that has no
morphologic or apparently functional equivalent in any
other mammal. In this mouse-sized Insectivore, two major
derivatives of the right stem bronchus pass through the
right caudal lung lobe and, uniting at the lung margin,
terminate in a common pleural covering as a nonrespiratory appendix (Figs. 1 and 2A and B). Approximately 80%
of the 106 specimens originally examined by Parke (1956)
exhibited these structures as two muscular tubes directed
medially along the caudal lung margin so that, in situ,
they occupied the right costophrenic sinus. The remainder
of the series showed these bronchial elements to be of
unequal length or, less frequently, irregular in form.
©
2002 WILEY-LISS, INC.
A subsequent developmental study and a search of the
related literature on lung malformations resulted in a
comprehensive review (Parke, 1959) that indicated these
shrew PA were homologous to aplastic bronchial abnormalities occasionally reported in other mammals. Since
similarly sacculate bronchial anomalies are predisposed to
pathologic conditions, as they are unable to effectively
eliminate accumulations of secreted and aspirated matter,
*Correspondence to: Wesley W. Parke, Ph.D., Division of Anatomy, USD School of Medicine, Vermillion, SD 57069. Fax: (605)
677-6381. E-mail: wparke@usd.edu
Received 16 August 2000; Accepted 16 December 2001
Published online 15 February 2002
PULMONARY APPENDIX OF BLARINA
185
Fig. 1. Dorsal view of the lungs of a Blarina with a tracing of the
tracheobronchial pattern, copied from a cast-corrosion specimen, superimposed. Note the larger terminal branches of the right stem bronchus that converge toward the caudal right lung margin to form the PA.
This specimen was prepared for a previous study (Parke, 1968).
Fig. 3. Thin-section view of the lumen and peribronchial tissue of a
PA bronchus (from a South Dakota specimen) fixed in distention. A
luminal mucuous plug (Muc) containing particle-laden macrophages
(Mac) lies above the epithelium (Ep) and its surrounding muscular tissue,
whereas deeper macrophages and plasma cells (PC) are indicated in the
peribronchial lymphoid tissue. From a paraffin-embedded section cut at
3 ␮ and stained with a Masson’s trichrome preparation.
Fig. 2. A: Paraffin section of a PA fixed in the noncontracted state,
showing a large quantity of luminal mucous containing a profusion of
naturally aspirated particulate matter and the location of the peribronchial lymphoid tissue. B: Paraffin section of a shrew PA fixed in a
contracted state, showing the exceptionally heavy peribronchial musculature that peristaltically expels the luminal contents. Both sections in
this figure were derived from New Jersey specimens, cut at 5 ␮ and
stained with Harris’s hematoxilin and eosin.
a rationale for the persistence of the PA in this one species
was sought. Unfortunately, the earlier investigations took
place prior to the general recognition of the immunologic
potential of bronchus associated lymphoid tissue (BALT),
so efforts were first directed toward the function of the
unusually heavy peribronchial musculature and the probability that this pulmonary appendix (PA) might serve as
an enhancement to the nonspecific lung clearance mechanisms.
An experimental study of carbon-black aerosol inhalations in a series of recently captured specimens did indicate that these bronchial extensions received, accumulated, and effectively expelled particulate aspirated
matter, and it was assumed that this function provided
sufficient reason for their evolutionary development and
retention (Parke and Wetzel, 1968). However, as numerous publications of the last four decades have focused
attention on the pulmonary BALT and its role in providing
more specific humoral and cellular protection to both the
lung and the general circulation in other mammals, a
series of shrew lungs were examined to ascertain whether
these unusual pulmonary appendages in Blarina might
also function as unique immunologic organs. Unfortunately, it is very difficult to maintain live Blarina under
the laboratory conditions now mandated for typical experimental small mammals, as they will not live communally
nor tolerate disturbances such as repetitive cage cleanings. Thus, the scope of this investigation was confined to
demonstrating, in a qualitative sense only, that these
186
PARKE
Fig. 4. Sectional view of a quadrant of a PA bronchus from a South
Dakota specimen processed with the avidin-biotin immunoperoxidase
technique. The chromogen-labeled IgA alpha chains mark the locations
of plasma cells (PC) superficial and deep to the peribronchial muscula-
ture (Mus), and show IgA in the lymphoepithelial cells (EP). This 6-␮-thick
paraffin section was not counterstained, but histologic detail was produced by a phase-contrast technique for photomicrography.
structures may serve to assist the more specific aspects of
pulmonary immunologic defenses.
In all the previous publications concerning these bronchial extensions of Blarina, they were referred to as “bronchial diverticula.” Critical semantic analysis has suggested that this is not an accurate designation since these
structures are not lateral outgrowths, as the term would
imply, but are terminal bronchial elaborations. As the two
bronchial elements are found in a single enclosing sac of
visceral pleura, and, as indicated in this report, they are
structurally and functionally analogous to the cecal termination known as the “appendix” in the gut of other
mammals, the term “pulmonary appendix” (PA) will be
subsequently applied to the whole pleura-encased extrapulmonary complex in Blarina.
tem (BALT) is noted for the production of the immunoglobulin, IgA. Early research in lung immunobiochemistry
showed that an extensive range of cross-reactivity to antibodies raised against this immunoglobulin occurs in
many other mammals (Vaerman et al., 1969; Vaerman,
1973), and particularly against human IgA in another
Insectivore, Erinacea europa (Vaerman and Heremans,
1971). Therefore, detection of this specific immunoglobulin appeared to be the simplest and most direct way to
qualitatively indicate this phase of the suspected immunologic potential of the Blarina PA.
Despite the lack of a stain specific for plasma cells per
se, the Masson trichrome preparation permitted the positive identification of these cells in the peribronchial lymphoid aggregates in the shrew PA by their characteristic
clock-faced chromatin distribution within the nucleus and
the prominent eccentric golgi apparatus.
Fluoroscein conjugated rabbit antihuman IgA serum,
specific for alpha chains, was initially applied to Blarina
PA paraffin cross-sections. However, this preparation
proved to be too comprehensive, as it not only labeled
plasma cells but indiscriminately labeled other lymphoid
cells and leucocytes as well. Since a greater specificity was
desired, an immunoperoxidase technique employing an
avidin-biotin peroxidase complex in a commercial preparation (Lymphoscan Kit; Biomedia Corp., Foster City, CA)
produced precisely for the IgA alpha heavy chain was
selected. This product utilized the remarkable affinity
that avidin has for biotin, which is approximately one
million times more efficient than the reaction of most
antibodies for their corresponding antigens. The covalent
attachment of the activated forms of biotin to biologically
active proteins, particularly antibodies, permits the spe-
MATERIALS AND METHODS
The lungs from a series of 16 Blarina were used in this
phase of investigation. All were procured from an approximately 2-km2 region of wooded land in Clay County,
South Dakota, by a grid setting of commercial snap traps
baited with a mixture of hamburger and peanut butter.
The traps were tended and rebaited every 4 hours for 1
day a week over a 4-week period to ensure freshness of the
material. For the histologic specimens, the entire thoracic
pluck was removed at the trap site and immediately immersed in Bouin’s solution for fixation. After 48 hours of
fixation, the PA containing lung segments selected for
general histologic examination were paraffin-embedded,
sectioned, and processed with either Harris’s hematoxilin
and eosin or Masson’s trichrome stain (Fig. 3).
The mucosa-associated lymphoid tissue in both the vertebrate digestive system (GALT) and the respiratory sys-
187
PULMONARY APPENDIX OF BLARINA
sectional surfaces of remarkable detail (Fig. 7). Then four
specimens were split longitudinally to expose their epithelial surfaces (Fig. 8). Both sets of SEM specimens were
critical-point dried, gold-coated to 30 – 40 nm, and photographed by SEM.
RESULTS
Fig. 5. In situ view of the diaphragmatic surface of the shrew right
caudal lung lobe after removal of the diapragm. Note that the PA (large
black arrow) occupies the right costophrenic sinus, and the vascularly
congested sinusoidal areas (small arrows) flank its emergence from the
caudal margin of the lung.
cific detection of labeled antibodies by using various tracing probes associated with avidin (Wilcheck and Bayer,
1984). As applied to the paraffin sections of the Blarina
PA, it chromogenically labeled structures containing IgA
with a deep amber color. Although a counterstain was
recommended and tried, it often obscured the desired labeling. Thus, a phase-contrast view of the processed
slides, in spite of some loss of structural detail, proved to
be the best method of observing the reactive locations. The
use of a green filter further enhanced the contrast of the
amber color and permitted the positive identification of
the labeled material in black and white photographs
(Fig. 4).
Because the developmental sequences of the Blarina PA
indicated that it was arterially supplied by the bronchial
arteries, and a superficial examination of the structures
showed hypervascularization in the lung tissues adjacent
to their extrapulmonary commencement (Figs. 5 and 6),
three trapped specimens were not field-dissected, but
were brought back to the laboratory intact and received
intraaortic injections of a mixture of India ink and latex to
illustrate the vascular relationships. The injected lungs
were then cleared by a previously published technique
(Parke and Michels, 1965), transilluminated, and photographed under low magnification.
Since the specific histomorphology of BALT has been
well described in other mammals, the scanning electronmicroscopy (SEM) of four examples of the shrew PA was
accomplished as follows: The bronchi of two freshly fixed
specimens of the PA were subjected to a freeze-fracture
preparation in which they were immersed in a mixture of
liquid nitrogen and ethanol; they then were simply fractured between the grips of two forceps, producing cross-
The Masson trichrome staining of the South Dakota
series of shrew lungs revealed numerous plasma cells in
the BALT of the PA immediately external to the muscular
layer, and often just external to the mucosa. The accumulated mucous within the PA lumina, as well as its peribronchial BALT, consistently contained numerous macrophages readily identified by their phagocytized inclusions
(Fig. 3).
The sections that received the avidin-biotin peroxidase
cytochemistry (ABC) treatment for the identification of
the IgA alpha heavy chains showed that many, but not all,
of the well differentiated plasma cells contained IgA and,
in addition, the epithelial cells and luminal mucous immediately adjacent to the positively labeled PCs also
showed positive staining for IgA alpha chains (Fig. 4).
Consecutive serial sections permitted the tracing of the
arterial supply of the PA from the intrapulmonary lung
parenchyma distally into the extrapulmonary appendages. As would be expected because of their nonrespiratory character, pulmonary artery terminals did not extend
beyond the lung margin, and the extrapulmonary bronchi
of the PA were supplied exclusively by continuations of the
bronchial arteries; however, their corresponding veins
were drained by extensions of the pulmonary veins. In the
freshly killed specimens, an area of congested lung tissue
was consistently noted surrounding the origins of the PA
bronchi just as they left the lung margin (Fig. 5). In serial
sections this was seen to be an area of vascular sinusoids
(Fig. 6A). The specimens receiving the latex-India ink
injections demonstrated that this was a region of a triple
vascular anastomoses, for when the injected medium descended the relatively large bronchial arteries it filled
these sinusoids, and, by retrograde flow from them, filled
the regional terminals of both the pulmonary arteries and
the pulmonary veins (Fig. 6B). The functional nature of
these sinusoidal areas is unclear, but it is obvious that
their presence provides the PA tissues with a generous
source of blood-borne inclusions as well as an afferent
route for immunologic products that might be generated
in the PA for later release to the general circulation.
The SEM photomicrographs of freeze-fracture preparations provided a clear view of the lymphatic vessel relationships of the epithelium of the PA. The lymphatics
serve as an entirely afferent component of the vascular
system, and their role as the most likely primary structural mechanism for the transendothelial passage of particulate and dissolved substances to the deeper lymphatics, and hence to the general circulation, in mucosa
associated lymphoid tissues (MALT) has long been recognized. A recent publication by Azzali and Arcari (2000)
well illustrated how these “intraendothelial channels” in
GALT serve for the transendothelial passage of lymphatic
cells to the deeper vessels. As the selected section of the
freeze-fractured PA in Fig. 7 shows, the collecting lymphatics here, as in the graphically detailed counterparts in
the Peyer’s Patches in rabbits, form a system of well
defined channels that are shown coursing in the internal
aspect of the basement membrane and communicating
188
PARKE
Fig. 6. A: A 4-␮ section of the dilated proximal bronchi (1) of a shrew
PA. Note that the muscular layer is not as pronounced as it is in the
extrapulmonary extensions, and the surrounding vascular sinusoids are
indicated (2). B: A shrew PA specimen that was injected with a mixture
of latex and India ink via the aorta. The injection medium followed the
systemic circulation through the bronchial arteries (3), and by the triple
anastomoses of the sinusoids back-filled the larger branches of the
regional pulmonary veins (4) and pulmonary arteries (5). Only branches of
the bronchial arteries extend along the PA bronchi. The specimen was
cleared in methylsalycilate and photographed under low power by transillumination.
with a similar plexus external to the lamina propria (LP)
that drains into the intramuscular and more external
lymphatics of the BALT.
The SEM analysis of the luminal aspect of the PA tissues produced some interesting results. Under a relatively
low (⫻1,000) magnification, the surface characteristics of
the PA epithelium were quite uniform throughout the
entire extrapulmonary length of these structures. The
conventional ciliated bronchial epithelium cells were relatively few in number, as the lymphoepithelial cells typical of BALT predominated in the views of the epithelial
“pavement” of the PA. These cells showed numerous microvilli on their luminal surfaces, with deep crevices between the cells that were often filled with a mucous exudate. In fact, the view provided in Fig. 8 is virtually
identical to the photomicrographs furnished by Bienenstock and Johnston (1976) and Racz et al. (1977) in their
reports showing SEM preparations of lymphoepithelial
surfaces of rabbit BALT.
function was suspected. Klein (1875) noted the lymphoid
aggregates in the tracheobronchial system and stated that
they were morphologically identical to the lymph follicles
described in tonsils and intestines. However, it was not
until nearly a century later that Bienenstock and his
associates (1973), in an extensive restudy of the pulmonary lymphoid aggregates, originated the term “bronchus
associated lymphoid tissue” (BALT). Subsequently, the
terms “gut associated lymphoid tissue” (GALT) and the
more inclusive concept, “mucosa associated lymphoid tissue” (MALT) were established as semantic retroformations (Sminia, 1996). BALT is distributed throughout various vertebrate groups, including mammals, birds, and
some reptiles. Sminia and associates (1989) noted that the
degree of its development within certain species seemed to
be directly dependent upon the extent of the antigen load
of that particular group. Since BALT collectively refers to
the entire distribution of lymphoid aggregates throughout
the lung, Sminia and coworkers (1989) introduced the
term “bronchus associated lymphoid unit” (BALU) to designate the individual, topically discrete lymphoid masses.
The histology of BALT has been most intensively studied in the rat (Simecka et al., 1986; Plesch, 1982) and the
rabbit (Bienenstock et al., 1973), where it can be detected
on the exposed epithelial surfaces of the opened bronchi as
whiter-appearing patches that at first may seem to be
randomly distributed, but are most consistently found
near the acute angles of bronchial bifurcations. Plesch
(1982), while noting that the number of BALUs in an
DISCUSSION
As the entire epithelial linings of the vertebrate digestive and respiratory tracts are continuously exposed to
ingested and aspirated antigens, their extensive association with the lymphoid components of the immune system
is quite understandable. The scattering of lymphoid cells
throughout the body’s mucosal surfaces, and their discernible concentrations into lymphoid aggregates, such as Peyer’s Patches, were known long before the extent of their
PULMONARY APPENDIX OF BLARINA
Fig. 7. SEM view of a PA bronchus section produced by the freezefracture technique. The luminal mucous (Muc) is seen on the surface of
the epithelium (E). Note the lymph channels on both sides of the lamina
propria (LP) that lies internal to the peribronchial musculature (Mus).
These lymph channels are believed to aid the return of particle-laden
macrophages from the lumen to the peribronchial lymphoid tissue. SEM
magnification ⫻1,000.
animal’s tracheobronchial tract appears to be an interspecific variable, estimated that the respiratory system of a
rat may contain 30 –50 units.
Since it is now firmly established that BALT is a complex association of immunologically related cellular types,
its demonstration as the major histologic component
within the highly muscular, nonrespiratory PA of Blarina
gives this unique structure a much greater physiological
significance than its originally surmised role as simply an
assistant to the general lung defenses provided by the
mucociliary and peristaltic pulmonary clearance mechanisms.
The above-described demonstrations of IgA and the IgAproducing plasma cells of the lymphoid tissue concentrated within the shrew PA, in addition to the SEM and
histologic photomicrographs, strongly suggest that it is an
immunologic organ. Admittedly, no quantitative judgments may be made from the evidence presented here,
since the individual immunologic status of such randomly
acquired wild specimens must be remarkably variable.
Nor has a sufficiently in-depth histologic analysis been
made upon which to base qualitative conclusions concerning other humoral and cellular immunologic functions.
Yet, some reasonable assumptions may be derived from
189
Fig. 8. An SEM photomicrograph of the lymphoepithelial surface of
an extrapulmonary bronchus of a South Dakota Blarina PA. Note that the
typical ciliated bronchial epithelial cells are sparsely distributed among
the microvilli-covered cells that form the epithelial “pavement” which is
characteristic of a typical BALT surface. This type of epithelial cell
composition is found throughout the extrapulmonary extent of the PA
bronchi and is identical to that photographed in the BALT of other small
mammals. The deep epithelial grooves run parallel to the extrapulmonary
bronchial axes. SEM magnification ⫻1,000.
the information presented in this report and related previous publications (Parke, 1956, 1959; Parke and Wetzel,
1968) when it is considered against the evidence derived
from the published studies on other animals. These are
discussed below.
The Blarina PA has been observed to receive aspirated
antigenic substances, both naturally and experimentally,
and periodically expel them by peristaltic and mucociliary
actions. Thus, these particular blind bronchial extensions
are able to avoid the pathologic consequences characteristic of anomalous homologous developments that occasionally occur in other mammals. However, they still receive a continuous turnover of aspirated antigens since
the fossorial nature of this shrew constantly exposes them
to a “high antigen load.”
These aspirated particles, while in the lumina of the PA
bronchial extensions, are brought into approximation to
the BALT that is the characteristic peribronchial tissue
for their entire extrapulmonary length.
In this temporary retention of the aspirated matter,
numerous observed macrophages enter the accumulated
mucous and phagocytize its particulate matter. Although
190
PARKE
the actual process has not been observed in the shrew PA,
it appears that these particle-laden cells gain access to the
deeper layers of the BALT, presumably aided by the illustrated transepithelial lymphatics, and there present the
antigenic material to the receptive lymphoid cells. Thus,
IgA-producing plasma cells elaborate the specifically generated secretory antibodies found in the luminal mucosal
secretions while other assumed cellular and humoral responses may be readily relayed to the general circulation
by way of the complex vascular associations demonstrated
at the proximal attachments of the PA.
There is no intention here to imply that any of the tissue
components within the bronchial extensions of the shrew
PA have been found (to date) to be unique to this structure. Rather, they are an anatomic and topographic arrangement of a type of histologic organization that is
relatively disseminated elsewhere, but is here apparently
concentrated to enhance effectiveness. This situation
shows a developmental, morpological, and functional relationship similar to that which the more consolidated
GALT in the vermiform appendix shows to the scattered
collections of Peyer’s Patches in the intestines. Like the
human vermiform appendix, the PA in the shrew has lost
most of the original major functions of the tubular structures from which it was derived, but has greatly retained
and amplified its immunologic role.
After the antigen sampling function of the avian Bursa
of Fabricious was defined, there was considerable speculation about which tissue organization in the nonavian
vertebrates provided an equivalent function.
Fichtelius et al. (1968) named the collective GALT of the
Peyer’s Patches and the cecal appendix as their favorite
candidate for this assignment, and it makes an interesting
theoretical postulation that the unusual sequence of developmental events, as described by Parke (1959), positioned the shrew PA to ideally receive aspirated matter
into its paired lumina. Because of the great antigenic load
environmentally placed on the tracheobronchial system of
the shrew, the PA, as an antigen sampling device, may
constitute an opportunistic expression of an exceptional
version of a bursa equivalent in this one species of mammal. As such, this unique phyletic development provides a
good example of the concept of “exaptation” (Gould, 1977),
in which the ontological expression of preexisting structures (air-conducting bronchi) is modified to perform a
novel function.
The recalcitrance of the Blarina toward being a compliant laboratory animal is quite unfortunate. If these hyperactive, solitary, venomous, and nearly totally fossorial
mammals could be induced to produce captive laboratory
colonies, there is little doubt that their unique tracheobronchial organization would be, by now, the subject of a
more extensive literature and a considerable source of
additional knowledge concerning the immunological capacities of the vertebrate respiratory system. It is hoped
that this report will stimulate further attempts to investigate the true nature of the very remarkable PA in this
one group of mammals.
TAXONOMIC NOTATION
The short-tailed shrew, Blarina, for the practical purposes considered here, constitutes a monospecific genus of
the family Soricidae (Order: Insectivora) with a single
species, brevicauda. It inhabits virtually all of the eastern
United States, from southern Canada to Florida, and as
far west as the proximities of the 100° meridian that
roughly coincides with the commencement of the highplains prairie. Although insular and otherwise isolated
populations form various subspecies, sampled specimens
from the extremes of the generic geographic range all
show the presence of the PA. Their closest relative, the
small short-tailed shrew (Cryptotis parva), is also a monospecific genus that is almost coextensive with Blarina in
its distribution. Although it has a much less obligatory
fossorial habit and a generally smaller body size, Cryptotis
resembles the Blarina enough that the determination of
two fewer upper rear premolars (and now, the complete
lack of anything that resembles the PA) in Cryptotis may
be required for a definitive differentiation. Blarina is almost exclusively fossorial in habit, establishing extensive
runs under the forest leafmold or vegetative thatch. These
malodorous and vicious little mammals have a very high
metabolic rate and must daily consume their body weight
in other small vertebrates, invertebrates, and some vegetable matter. Their submandibular glands produce a venomous saliva, and they readily subdue and eat small
mammals of equivalent size. They can tolerate exposure to
light for only a brief time, and if unable to establish a
reclusive habitat they soon die in extreme agitation. Despite their ubiquity throughout their range, these shrews
are very seldom observed above ground in daylight, although they are very active throughout the year. They
also appear to be socially intolerant of even their own
species, except for the short time spent as littermates and
brief encounters when breeding.
ACKNOWLEDGMENTS
The author is indebted to the inspiration and advice
provided by his teacher, mentor, and friend, Dr. Ralph M.
Wetzel, late Professor of Zoology at the University of Connecticut.
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