O r i g i n , morphology, histochemistry and function of the mucosal mast cell and the globule leukocyte. A review. Sven Nikander C o l l e g e of V e t e r i n a r y M e d i c i n e , L a b o r a t o r y of Parasitology a n d D e p a r t m e n t of P a t h o l o g y , P o s t b o x 6, SF00581 H e l s i n g f o r s , F i n l a n d . Summary:
Parasites i n v a d i n g mucous membranes elicit an i n f l a m m a t o r y response f r o m the host. W i t h appro-
priate f i x a t i o n and staining methods, cells w i t h i n t r a c y t o p l a s m i c granules m a y be observed. C l o s e r examinat i o n m a y reveal several types of granular cells, the e o s i n o p h i l i c granulocytes being the most c o m m o n l y i d e n t i fied i n parasitic infections, but also observable are peculiar mast cells a n d globule leukocytes whose f u n c t i o n s are not yet understood. T h i s r e v i e w describes the most i m p o r t a n t facts about the mucosal mast cell a n d the globule leukocyte relevant to their significance i n parasitic infections.
Key words: i n f l a m m a t o r y cells, histogenesis, parasitic infection, granular cells, anatomy.
Rangifer, 11 (1): 3—11 Introduction Mast cells (= M C ) belong to a heterogeneous group of granular cells (Michels, 1938). T h e i r phenotypes m a y be regulated b y factors i n the m i c r o e n v i r o n m e n t . L o c a l g r o w t h factors m a y influence their differentation, maturation, and development, and thus the f u n c t i o n of the cells, (Selye, 1965, D v o r a k & G a l l i , 1985, Befus & al., 1986, Enerback & N o r r b y , 1989). A c c o r d i n g l y , w h e n the m i c r o e n v i r o n m e n t changes, the phen o t y p i c expression of M C also m a y change. F o r example, M C i n the subserosal tissue of y o u n g rats became after 8-12 weeks positive for berbe¬ rine sulfate and safranin, indicative of maturat i o n of heparin ( A r i z o n o & N a k a o , 1988). There are at least t w o specific M C - t y p e s ; those i n the connective tissue called connective tissue mast cells (= C T M C ) and those at mucosal and serosal surfaces called mucosal mast cells ( = M M C ) (Enerback & a l . , 1986). G l o b u l e leukocytes (= G L ) are granular cells i n the epithelium that resemble mast cells. A l -
Rangifer, 11 (1), 1991
though c o m p a r i s o n of the properties of M M C and G L has led to the assumption that G L are derived f r o m M M C ( M i l l e r & a l . , 1968), there are several indications that G L are an independent cell type (Ruitenberg & Elgersma, 1976, 1979, R u i t e n b e r g & al., 1979, 1982). T h i s questi o n is reviewed i n the light of facts o n the m o r p h o l o g y , histogenesis, histochemistry, and f u n c t i o n of M M C and G L .
Occurrence of M M C and G L M M C and G L are p r o b a b l y f o u n d i n most vertebrates, but they are not equally distributed i n different tissues. M M C are m a i n l y located i n lamina p r o p r i a and also i n the epithelium of the alimentary and respiratory tracts. G L occur o n l y i n the epithelium of those systems and also intraepithelially i n the u r i n a r y and reproductive tracts. M M C are more frequent than G L i n n o r m a l tissues. Parasitic infections influence the n u m b e r of both cell types, but the 3
n u m b e r of G L is especially increased d u r i n g parasitic infections (Table I). M C are particularly abundant beneath the epithelial surfaces, i n the v i c i n i t y of peripheral nerves and b l o o d and l y m p h a t i c vessles; i n certain animal species, they are c o m m o n w i t h i n peritoneal and pleural cavities (Selye, 1965, Gal¬ l i & al., 1984, 1987, Enerback & N o r r b y , 1989). M a x i m o w (1905) p r o b a b l y was the first to observe that lamina p r o p r i a of the intestine of the rat contained M C w h i c h differed f r o m the classical C T M C . A n aberrant granular celle type first observed b y H e i d e n h e i n (1888) was described b y W e i l l as a «Schollenleukozyt» i n 1919. T h e name «Schollenleukozyt» was translated into «globule leukocyte» b y Keasbey (1923). W e i l l (1919) described G L i n the epithelia of the alimentary tract of the dog, cat, p i g , mouse, rabbit, guinea-pig, and man. There are several reports G L i n the alimentary tract minants (Keasbey, 1923, H i l l , 1951, K e n t , 1952,
o n the presence of and bile ducts of r u Duran-Jorda, 1945, Sommerville, 1956,
D o b s o n , 1966, Jarrett & al., 1967, 1968, M i l l e r & al., 1968, M u r r a y & a l , 1968, R a h k o , 1970, 1971, 1972, 1973, Blazek, 1971, M i l l e r & Jarrett, 1971, Lawrence, 1977, G r e g o r y , 1979, A k p a v i e , 1985, A k p a v i e & P i r i e , 1985, H u n t l e y & al., 1987b). G L has also been identified intraepithelially i n the respiratory, u r i n a r y , and reproductive epithelium of ruminants, (Taliaferro & Sarles, 1939, K e n t , 1952, Kellas, 1961, Blazek, 1971, Breeze & al., 1975, Lawrence, 1977, M a h m o u d & P i r i e , 1982, A k p a v i e , 1985). G L have been documented also i n 11 species of birds (Clara 1926, T o n e r , 1965, A s d r u b a l i & M u g h e t t i , 1969, H o l m a n , 1970, 1972, K i t a g a w a & al., 1979, 1988), i n the gut mucosa of a fish, Acipenser sp. (Rogosina, 1928), and i n several species of amphibians and reptiles (Toro, 1931). N o r m a l l y G L f o r m a very small p r o p o r t i o n of the cells of the epithelium: 0.001 % i n the u r i n a r y tract of the rat. In rats fed a M g - d e f i c i ent diet, however, G L increased to 5 % of the epithelial cell p o p u l a t i o n i n the renal pelvis, uterus, and u r i n a r y bladder ( C a n t i n & V e i l l e u x , 1972).
Table I. Comparision of different characteristics of M M C and G L MMC
GL
Occurrence
lamina propria and epithelium of different mucous membranes
within mucosal epithelium
N u m b e r of cells
variable, no absolute counts made
normally 1-2 GL/1000 epithelial cells, experimentally max. 32/1000 epithelial cells
Function of cells
release biological active unknown mediators, take part in the expulsion of parasites and facilitate transport o f antibodies into the lumen o f intestine spherical
associate with MC-proliferation in parasitic infections and take part in the «self cure» by local immediate hypersensitivity reaction
Structure o f chromatin
lymphocytic-type distribution
cartwheel-type distribution
Cytomembrane
with pseudopodia, no desmosoms
with pseudopodia, no desmosoms
Size and ultrastructure of granules and globules
small, 1-2 fx, electron-dense, usually unevenly
large, usually 2 - 5 usually diffusely
Nuclear form
4
ovoid, spherical, often indented
electron-dense,
Rangifer, 11 (1), 1991
Structure of M M C and G L
K e n t , 1952, Kellas, 1961, A k p a v i e , 1985). T h e largest globules are seen i n cells w i t h f e w globules. G L w i t h o n l y t w o large irregularly f o r m e d globules were observed i n the m a i n bile duct of a goat infected w i t h liver flukes ( R a h k o , 1972).
T h e size and n u m b e r of M M C - g r a n u l e s v a r y according to the size of the cell. T h e globules of G L are usually bigger and fewer i n n u m b e r than i n M M C , causing indentations o n the nucT h e ultrastructure of i n d i v i d u a l globules varileus. M i t o t i c figures and cytoplasmic projec- es (Toner, 1965, K e n t , 1966, W h u r & J o h n s t o n , tions have been observed i n b o t h M M C and 1967, C a r r , 1967, T a k e u c h i & a l . , 1969, H o l ¬ G L (Table I). man, 1972, Baert, 1989). O c c a s i o n a l l y bridgeT h e f i x a t i o n m e t h o d is of extreme i m p o r t a n - like connections have been seen between the ce for the preservation of the structures of globules (Baert, 1989). F o u r types of globules M M C and G L (Enerback, 1966, 1974, 1981, have been distinguished; (1) globules w i t h elec1987, Enerback & L u n d i n , 1974, R u i t e n b e r g & t r o n density o n l y i n the core; (2) usually larger al., 1982, Enerback & al, 1986). It influences globules w i t h a homogeneous electron-dense the preservation and visualization of all types of matrix; (3) those c o n t a i n i n g paracrystalline M C . In tissue sections fixed i n a l c o h o l , n o M C structures; and (4) globules w i t h an intermedic o u l d be f o u n d b y M a x i m o w (1905). O n the ate structure (Vandenberghe & Baert, 1981). other hand, i n biopsies of h u m a n d u o d e n u m The membrane s u r r o u n d i n g the globules is alfixed i n b o t h standard f o r m a l i n and a f o r m a l i n - ways s m o o t h . R h o m b o i d crystals have also acetic acid ( F A ) fixative, M C were equally w e l l been observed freely i n the cytoplasm of G L preserved, but an additional p o p u l a t i o n of M C ( C a n t i n & V e i l l e u x , 1972), w i t h striation paralw i t h M M C staining characteristics c o u l d be v i - lel to its l o n g axis ( C a r r , 1967). sualized w h e n the F A - f i x a t i v e was used ( G u y G r a n d & a l . , 1984, Enerback & N o r r b y , 1989). Histochemistry of M M C and G L M M C differ i n size, the bigger being present i n b o t h mucosae and connective tissues, the smaller o n l y subepithelialy ( M i l l e r , 1980, G u y G r a n d & a l . , 1984). T h e nucleus is of the l y m p hocytic type (Ruitenberg & a l . , 1979, 1982). C y t o p l a s m i c projections are often seen as an i n dication of m o t i l i t y (Enerback & L u n d i n , 1974). N u m e r o u s M M C w i t h o u t m i c r o v i l l i are seen between the epithelial cells d u r i n g the «self cure» expulsion of intestinal nematodes (Enerback, 1974). G L occur as solitary cells i n the e p i t h e l i u m . Junctions between G L and epithelial cells have occasionally been observed. G L are able to m i grate w i t h the use of pseudopods t h r o u g h the epithelium (Toner, 1965). A c c o r d i n g l y , G L have been f o u n d freely i n the tracheal l u m e n (Vandenberghe & Baert, 1981). T h e nucleus of G L is usually eccentric, o v o i d or spherical, and c o m m o n l y indented b y the cytoplasmatic globules ( G r e g o r y , 1979). T h e nuclear membrane is distinct and the cartwheel distribution of the c h r o m a t i n is c o m m o n ( A k pavie & P i r i e , 1985). Binucleated cells have also been observed (Keasbey, 1923, A k p a v i e , 1985). T h e cytoplasm of G L is filled w i t h refractile, acidophilic and spherical globules (Keasbey, 1923, K e n t , 1952). T h e n u m b e r of globules i n a cell section ranges f r o m 5 to 40 (Keasbey, 1923,
Rangifer, 11 (1), 1991
The electron-dense metachromatic granules of M M C and globules of G L are made up of p r o teoglycans w h i c h can be distinguished histochemically. L o w sulphated mucins i n M M C differentiate them f r o m C T M C w i t h h i g h l y sulphated c o m p o u n d s of heparin. In G L the sulphation degree is histochemically even l o w e r than i n M M C . E h r l i c h i n 1878 p o i n t e d out that the specific feature of M C was the metachromatic granules in the cytoplasm (cited b y M i c h e l s , 1938). A proteoglycan of M M C , a c h o n d r o i t i n sulphate, does not show fluorescent berberine b i n d i n g . It stains preferentially w i t h alcian blue i n a staining sequence w i t h safranin (Enerback & a l . , 1986). T h e cells possess IgE receptors (Ishizaka & Ishizaka, 1984) w h i c h respond w e r y r a p i d l y (Enerback, 1987). Conjugated avidin reacts w i t h the granules of rodent and h u m a n M C (Tharp & al., 1985). Differences i n staining characteristics of the G L globules also have been attributed either to the fixatives or staining methods (Enerback, 1966, R a h k o , 1971, 1972). C a r n o y s fixative has been the best for the demonstration of m u c o p o lysaccharides of M C (Enerback, 1966). In cattle the G L globules were more adequately fixed w i t h corrosive f o r m o l ( M i l l e r & a l . , 1967) o r B o u i n ' s s o l u t i o n ( R a h k o , 1971, 1972). 5
A f t e r f i x a t i o n i n Z e n k e r s - f o r m o l o r 2 5 % formaline, G L are positive f o r P A S and alcian blue ( C a n t i n & V e i l l e u x , 1972). T h e globules stain metachromatically w i t h t h i o n i n , t o l u i d i n e blue, and brilliant cresyl blue ( K i r k m a n , 1950, K e n t , 1952). T h e presence of a sulphated acid mucopolysaccharide is documented also b y the positive reaction w i t h astra blue stain (Jarrett & al., 1968, M i l l e r & al., 1968, M u r r a y & al., 1968). T h e metachromatic reaction of the globules seems to v a r y ; i n the respiratory tract of o l d cows, G L do not show metachromatic staining w i t h t o l u i d i n e blue ( A k p a v i e , 1985). It has been supposed that the globules contain i r o n because of the resemblance to erythrocytes (Keasbey, 1923). Earlier investigations f o u n d no evidence for either i r o n ( D a w s o n , 1943) but subsequently K i r k m a n (1947, 1950) f o u n d indications of hem o g l o b i n and K e n t (1952) f o u n d evidence for i r o n . G l y c o s a m i n o g l y c a n s , as w e l l as serine esterase, are present i n the granules of M M C and G L . G L does not contain 5 - h y d r o x y - t r y p t a m i n e ( W h u r & Gracie, 1967, Jarrett & al., 1968) although the globules contain strongly basic p r o teins ( R a h k o , 1971, 1972). T h e negative reaction w i t h toluidine blue at p H 4.2 also confirms that heparin is absent f r o m the globules of G L ( W h u r & Gracie, 1967).
p u l s i o n of parasites, the «self-cure» p h e n o m e n o n . G L is thus possibly associated w i t h the i m mune response to parasitic infections (Table I). N u m e r o u s s t i m u l i cause M C to release biologically active mediators (Selye, 1965). M o r p h o logical studies have documented structural changes i n M C d u r i n g different i n f l a m m a t o r y , i m m u n o l o g i c a l , reparative, metabolic, and neoplastic responses but the role of M M C has remained unclarified. H y p e r p l a s i a of instestinal M M C occurs i n the rat after an infection w i t h Nippostrongylus brasiliensis. T h e reaction i n N. brasiliensis «seif cure» expulsion is considered to be of an anaphylactic type. ( M i l l e r , 1971). H o w e v e r , there was no documentable change i n the permeability during the expulsion of N. brasiliensis i n the mast-celldeficient mice ( C r o w l e & Reed, 1981). Nevertheless it is suggested that biogenic substances released f r o m M M C are responsible for mucosa lysis and that this causes the increase i n mucosal permeability w h i c h is k n o w n to occur during w o r m expulsion ( M i l l e r & al., 1968).
Function of M M C and G L
T h e f u n c t i o n of G L was o r i g i n a l l y connected w i t h the assimilation of f o o d substances ( W e i l l , 1919). T h e observation that G L contained hem o g l o b i n led to the theory that they had the same f u n c t i o n as the erythrocytes (Keasbey, 1923). Later it was supposed that G L had a nutritive f u n c t i o n for the s u r r o u n d i n g tissue (Heine & Schaeg, 1977).
M C play an important role i n m a n y biological processes. T h e y p r o b a b l y interact w i t h the cells of m a n y tissues, organs, and b o d y cavities. The cells can elaborate and release a variety of biologically active compounds. O b v i o u s l y , this h o l d true specifically for C T M C . M M C and G L are, o n the other hand, i n v o l v e d i n the ex-
T h e first to suggest that G L c o u l d be i n v o l ved i n parasitic infections was H o l e i n 1937. h r 1939 Taliaferro & Sarles showed that G L were associated w i t h parasitic infections and mast cell proliferation. Others also have observed a correlation between parasites and G L ( K i r k m a n , 1947, S o m m e r v i l l e , 1956, A h l q v i s t & K o h o n e n ,
Table II. Theories and arguments on the origin and histogenesis of M M C Supposed precursors for M M C
Evidences o f relationship
1. Hemopoietic tissue
M M C are thymus-independent cells o f bone marrow?
2. Lymphocytes
Lymphocytes are k n o w n to be migrating cells with capability to transform.
3. Basophilic granulocytes
Analogous composition o f the granules in both basophilis and M M C .
6
Rangifer, 11 (1), 1991
Table III. Theories and arguments on the origin and histogenesis of G L Supposed precursors for G L
Evidences for relationship
1. Hemopoietic tissue
Thymus-dependent cell o f bone marrow with intracytoplasmic granules and short life span (2-3 months)?
2. Lymphocytes
A complete morphological series f r o m l y m p hocyte to G L is demonstrable.
3. Mast cell
Analogous ultrastructure and composition o f granules of M M C and globules o f G L .
4. Large granular lymphocyte
Intraepithelial granular cell with similar nuclear structure to G L .
5. Russel body cell
Globules of G L resemble the Russel bodyinclusions with the same fluorescence, being surrounded by pyroninophilic cytoplasm like in plasma cells.
6. Eosinophilic granulocyte
Analogous acidophilic granules in G L and eosinophils, both associated with parasitic i n fections.
7. Mesenchymal cell
G L is an independent mesenchymal cell which undergoes mitosis and forms local tumors.
1959, D o b s o n , 1966, Jarrett & al., 1967, 1968, W h u r , 1967, Fernex, 1968, M i l l e r & al, 1968). A Trichinella-'mduced p r o l i f e r a t i o n of M M C occurred i n the intestine of thymus-bearing and not i n athymic mice. T h e enhanced behaviour was both antigen- and t h y m u s dependent but o n l y observed for the stromal intestinal M M C and not for the intraepithelially located G L . In congenitally mast cell-deficient mice infected w i t h Trichinella, no proliferation of G L was observed. In contrast, an increasing n u m b e r of G L was observed intraepithelially i n the intestine of n o r m a l mice. A positive correlation between the i n f i l t r a t i o n of G L and the r a p i d i t y of T. spiralis expulsion f r o m the intestine was suggested, ( K a m i y a & al., 1985).
and H u n t l e y & al. (1984b) have associated the presence of G L w i t h the i m m u n e response to parasitic infections.
Differential counts indicated that an increasing p r o p o r t i o n of the M C p o p u l a t i o n migrated intraepithelially, possibly to be transformed to G L ( M i l l e r & Jarrett, 1971). A l s o D o b s o n (1966), C a r r (1967), W h u r (1967), M i l l e r & al. (1968), M u r r a y & al. (1968), Lawrence (1977)
Rangifer, 11 (1), 1991
Origin of M M C and GL There is evidences that M M C are derived f r o m the hemopoietic tissue, possibly having the same precursors as other types of M C . T h e differentation of M C precursors may be locally regulated. T h e histogenesis of G L , o n the contrar y , is d o u b t f u l . E r y t h r o c y t e s , plasma cells, Russel b o d y cells, and other types of leukocytes and mast cells have been proposed as precursors for G L . H o w e v e r , G L seem to be an independent migrating cell type of nonepithelial o r i g i n and the histogenesis of G L - l i k e cells may be different i n different vertebrate classes. F u r t h e r m o re, cytochemical dissimilarities between tracheal and intestinal G L might indicate that they represent different phenotypes or even different types of G L (Tables II and III). 7
Practically pure populations of one specific M C p h e n o t y p e exist i n the mucosa and of another phenotype i n connective tissue (Enerback, 1981, 1987, K i t a m u r a & al., 1983). Peritoneal M C themselves might give rise to M C phenotyp i c a l l y similar to either C T M C or M M C ( N a k a n o & al., 1985). There is evidence that M C derived f r o m cultured hemopoietic tissues are M M C (Jarrett & H a i g h , 1984). The cells are regarded as an independent cell p o p u l a t i o n . T h e i r histogenesis is thymus-independent, but the response to Trichi¬ nella infections is m a i n l y thymus-dependent (Ruitenberg & a l , 1979, G a l l i & a l , 1984). Similarities between G L - g l o b u l e s and erythrocytes led to the o p i n i o n that the globules are derived f r o m phagocytosed erythrocytes (Gregory, 1979). Duran-Jorda (1945) considered that G L secreted erythrocytes, then b e c o m i n g epithelial l y m p h o c y t e s . T h e m o r p h o l o g y and stain i n g properties also contributed to the hypothesis that G L belong to the e r y t h r o c y t i c series. D a w s o n (1943) proposed that G L o c c u p y an i n termediate p o s i t i o n between erythrocytes and leukocytes. K e n t i n 1952 and T o n e r i n 1965 suggested a l y m p h o c y t e origin o n the basis of f i n d i n g a complete series, w i t h transitional forms, f r o m the small lymphocytes to the G L . Kitagawa & al. (1979) reported that G L i n chicken originated f r o m the t h y m u s l y m p h o c y t e s , being stainable w i t h anti T - l y m p h o c y t e serum. Baert & Frederix (1985) considered large granular l y m p h o c y t e s as a possible precursors for G L . O t h e r origins have also been suggested, i n c l u d i n g eosinophils, plasma cells, and mast cells (Kent, 1952). T h e inclusions of Russel b o d y cells and the globules fluoresced similarly, and the cytoplasm i n b o t h cells was p y r o n i n o p hilic ( D o b s o n , 1966, C a r r , 1967, W h u r & J o h n ston, 1967). But G l differ f r o m plasma and Russel b o d y cells because they lack i m m u n o g l o b u lins ( W h u r & W h i t e , 1970). In 1977 H e i n e and Schaeg stated that their results indicate that the G L may originate both f r o m M ( t and f r o m eosinophilic granulocytes. G L were considered to be M M C w h i c h have migrated to the epithelium and p a r t l y discharged their granules; the conclusion was based o n their similarities b o t h ultrastructurally and histochemically w i t h M M C (Jarrett & al., 1967, 1968, M i l l e r & al., 1968, M u r r a y , al., 1968, M i l ler & Jarrett, 1971). H u n t l e y & al. (1984) showed transitional cells 8
between M C and G L i n the intestine of sheep infected w i t h nematodes. T h e size of the globules changed f r o m small to large and proteoglycans, serine esterase, dopamine, and i m m u n o globulins were demonstrated i n all cell types. W h e n the globules incresed i n size, their amine content decreased. H i s t o c h e m i c a l analyses thus supported the v i e w that M M C and G L have a c o m m o n lineage ( H u n t l e y & al., 1984). G L has been proposed to be a specific cell type of mesenchymal origin ( K i r k m a n , 1950). There are several indications that G L p r o b a b l y are an independent cell type. T h i s fact is supp o r t e d b y the findings of a neoplastic behaviour of G L i n the intestine of the cat ( F i n n & Schwartz, 1972). F u r t h e r m o r e , G L undergo m i tosis d u r i n g Trichinella infection. R u i t e n b e r g & Elgersma (1979) d i d not totally discard the M M C o r i g i n of G L . Some other data suggest a c o m m o n source for M M C i n intestinal mucosae and support the idea that M M C and G L are t w o independent cell populations (Parmentier & al., 1982).
References Ahlqvist, J. & Kohonen, J. 1959. O n the granulated cells of the u r i n a r y tract i n rats infected w i t h chosomides
crassicauda.
-
Acta
Path.
Tri-
Microbiol.
Scand. 46: 313-319. Akpavie, S. O .
1985.
Globule
ratory Diseases in Cattle.
Leucocytes and
Respi-
P h D thesis, U n i v e r s i t y of
Glasgow.
Akpavie, S. O
& Pirie, H . M . 1989. T h e G l o b u l e
leucocyte: M o r p h o l o g y , o r i g i n , f u n c t i o n and fate. A r e v i e w . - Anat.
Histol
Embryol.
18: 87-95.
Arizono, N . & Nakao, S. 1988. Kinetics and staining properties of mast cells p r o l i f e r a t i n g i n rat small intestine t u n i c a muscularis and subserosa f o l l o w i n g i n f e c t i o n w i t h Nippostrongylus
brasiliensis.
-
APMIS
96: 964-970.
Asdrubali, G . & Mughetti, L. 1969. S u l comportamento dei cosidetti «leucociti globulari» i n alcune parassitosi intestinali del p o l i o . - Atti della Soc. Ital. della Sc. Vet. 22: 601-606. Baert, J.
1989.
U l t r a s t r u c t u r e of globule
leucocytes
isolated f r o m rat tracheal e p i t h e l i u m . - /. Submicrosc. Cytol
Pathol. 21: 765-769.
Baert, J. & Frederix, M . 1985. G l o b u l e leucocytes i n the respiratory e p i t h e l i u m of h u m a n upper airw a y s : A n ultrastructural study. - Anat.
Ree.
212:
143-152.
Rangifer, 11 (1), 1991
Befus, D . ,
Lee, T.,
Goto, T.,
Enerbäck, L. & Lundin, P. M . 1974. U l t r a s t r u c t u r e
Goodacre, R.,
Shanahan, F. & Bienenstock, J. 1986. H i s t o l o g i c
of m u c o s a l mast
and f u n c t i o n a l properties of mast cells i n rats a n d
48/80 treated rats. - Cell Tissue Res. 150: 9 5 - 1 0 5 .
humans. - I n : Mast Cell Differentiation geneity, ed. b y A . D . Befus
&
and
Hetero-
al., Raven
Press,
N e w Y o r k , p p . 205-213. Schollenleukozyten
bei einigen
parasitären
E r k r a n k u n g e n der H a u s - u n d Jagdtiere - Zbl.
Vet.
Med. B. 18: 103-112. C e l l structure and function i n the mammalian lung: the trachea, b r o n c h i and bronchioles. - The Vet. Bull. 46: 319-337. and mast cells of the urinary tract i n magnesium-deficient rats. A cytochemical and electron microscopic study. - Lab. Invest. 27: 495-507. E.
1967.
testine. - / . Anat. M.
1926.
101: 793-803. Beiträge z u r K e n n t n i s des V o g e l -
m i t besonderer
leukozytären
Gewebe i m
Berücksichtigung
Z e l l e n . - 2. Mikrosk.
Anat.
Forsch.
der 6:
305-350. parasite
Nippostrongylus
brasiliensis
by
mast-cell deficient W / W anemic mice. - Infect. Immunity
405-417. &
1989. T h e mast cells.
Norrby, K.
In: Iversen, O . H . (Ed.) Cell Kinetics
of the
Inflam-
- Springer-Verlag, Berlin, Heidel-
matory Reaction.
berg, p p . 169-204. to Atherosclerosis,
Relationship - S. K a r -
Fibrosis and Eosinophils.
gen, Basel (Switzerland), N e w Y o r k . 212 pages. Finn, J. P. & Schwartz, L. W. 1972. A neoplasm of i n the intestine
o f a cat. - /.
Comp. Path. 82: 323-326. Galli, S. J.,
Dvorak, A . M . ,
Marcum, J. A., IshiK.,
Goldin, J. M . , Rosenberg, R. D . , Cantor, H . & Dvorak, H . F. 1982. M a s t cell clones: A m o d e l f o r the analysis of cellular m a t u r a t i o n . - /. Cell
Biology
95: 435-444. Galli, S. J, Arizono, N . , Murakami, T., Dvorak, A .
Crowle, P. K. & Reed, N . D . 1981. Rejection of the intestinal
ed. b y
and Heterogeneity,
zaka, T., Nabel, G . , Simonian, H . , Pyne,
darmes. V I . T e i l D a s lymphoretikuläre Darmrohre
Mayrhofer, G .
A . D . Befus & a l . , R a v e n Press, N e w Y o r k , p p .
globule leucocytes
F i n e structure of crystalline i n -
clusions i n the globule leucocyte of the mouse i n Clara,
&
Fernex, M . 1968. The mast-cell system: Its
Cantin, M . & Veilleux, R. 1972. G l o b u l e leucocytes
K.
Mast Cell Differentiation
Enerbäck, L.
Breeze, R. G . , Wheeldon, E. B. & Pirie, H . M . 1976.
Carr,
Miller, H . R. P.
1986. M e t h o d s f o r the i d e n t i f i c a t i o n a n d character i z a t i o n of mast cells b y light m i c r o s c o p y . - I n :
Blazek, K. 1971. Beitrag z u m V o r k o m m e n der sogenannter
Enerbäck, L.,
cells i n n o r m a l a n d c o m p o u n d
Dawson, H . L. 1943. A study of certain cell observed i n the gall bladder mucosa o f cats. - Anat.
Ree.
85: 135-155. Dobson, C . 1966. Studies on the immunity columbianum:
of sheep to
the nature and fate
of the globule leucocyte. - Aust. J. Agric.
Res.
17:
matitis i n genetically mast cell-deficient v
m i c e . - Blood 69:
Gregory, M . W .
Duran-Jorda, F. 1945. L o c a l haemopoiesis as seen i n the abomasum of the c o w and sheep. - Vet. J. 101: 191-194.
Vet
Bull. 49:
Mast cells i n rat gastrointestinal
mucosa. - Acta Path. Microbiol.
Scand. 66: 303-312.
Enerbäck, L. 1974. Berberine sulphate binding to mast cell polyanions: A cytofluorometric method for the quantitation of heparin. - Histochemistry
42: 301-313.
Enerbäck, L. 1981. T h e gut mucosal mast cell. - Mono gr. Allergy 17: 222-232.
255.
Rangifer, 11 (1), 1991
globule
leukocyte The
Guy-Grand, D . , Dy, M . ,
Luffau,G.
& Vassalli P.
1984. G u t mucosal mast cells. O r i g i n , traffic and differentation. - /. Exp. Med. 160: 12-28. 1888. Beiträge
zur Histologie und
P h y s i o l o g i e der Dünndarmschleimhaut. samte Physiol.
- Arch.
Ge-
43: 1-103.
Heine, H . & Schaeg, G . 1977. H e r k u n f t u n d F u n k L e u k o z y t e n . - Acta Anat.
98:
275-280. Hole, N . H . 1937. «Rüssel bodies» o r hyaline droplet degeneration of plasma cell i n the p o r t a l canals of the sheep's liver. - / . Comp.
Path. 50: 299-302.
Holman, J. 1970. U l t r a s t r u c t u r e of the intestinal globule leucocytes i n the c h i c k . - Acta Vet. Brno 39: 385-390. Holman, J. 1972. U l t r a s t r u c t u r e of specific granules of the intestinal globule leucocytes of the c h i c k e n . - Acta Vet. Brno 41: 235-239. Huntley, J. F., McGorum, B . , Newlands, G . F. J. & Miller, H . R. P. 1984a. G r a n u l a t e d intraepithe-
Enerbäck, L. 1987. M u c o s a l mast cells i n the rat and i n man. - Int. Archs. Allergy Appl. Immun.
The
821-827.
t i o n des Globulären
Dvorak, A . M . & Galli, S. J. 1987. A n t i g e n - i n d u c e d , IgE-mediated degranulation of c l o n e d i m m a t u r e mast cells derived f r o m n o r m a l mice. - Am. J. Pathol. 126: 535-545.
1979.
WBB6FJ-
1661-1666.
and parasitic i n f e c t i o n - a brief h i s t o r y . -
Heidenhein, R.
955-966.
Enerbäck, L. 1966.
bers of mast cells at sites of i d i o p a t h i c c h r o n i c derW/W
33: 54-58.
Oesophagostomum
M . & Fox, J. G . 1987. D e v e l o p m e n t of large n u m -
82: 249¬
lial
lymphocytes:
their
relationship
to
mucosal
mast cells and globule leucocytes i n the rat. munology
Im-
53: 525-535.
9
Huntley, J. F,
Newlands, G . & Miller, H . R. P.
1984b. T h e i s o l a t i o n and c h a r a c t e r i z a t i o n o f g l o b u le leucocytes: their d e r i v a t i o n f r o m m u c o s a l
mast
cells i n parasitized sheep. - Parasite Immunology
6:
371-390.
Kitamura, Y., Sonoda, T . , Nakano, T . , Hayashi, C .
Ishizaka, T . & Ishizaka, K. 1984. A c t i v a t i o n o f mast cells f o r mediator release t h r o u g h I g E receptors. Prog Allergy
-
34: 188-235.
1967. T h e relationship between mast cells and globule leucocytes
i n parasitic infections. - Vet. Rec.
80: 503-506. & Urquhart, G . M . 1968. Q u a n t i t a t i v e studies o n the mechanism of self cure i n Nippostrongylus
brasi-
liensis infections. - I n : Soulsby, E . J. L . (Ed.), The A c a d e m i c Press,
of the Host to Parasitism,
Inc., N e w Y o r k . 1968, p p . 191-198. Jarrett, E. E. E. & Haigh, D . M . 1984. M u c o s a l mast cell i n v i v o and i n v i t r o . - Immunol.
Today 5: 115—
118. M.
1985.
nective tissue mast cells i n l i v i n g mice. - Int. Archs 77: 144-150.
Appl. Immun.
Lawrence, J. A . 1977. T h e globule leucocyte i n b o v i ne schistosomiasis. - Res. Vet. Sci. 23: 239-240. Mahmoud, G . S. & Pirie, H . M . 1982. O v i n e b r o n c h o p u l m o n a r y globule leukocytes. - I. M o r p h o l o g i -
Jarrett, W. F. H . , Jarrett, E. E. E., Miller, H . R. P.
Kamiya, M . ,
& Asai, H . 1985. D i f f e r e n t i a t i o n processes o f conAllergy
Jarrett, W. F. H . , Miller, H . R. P. & Murray, M .
Reaction
Kitagawa, H . , Hashimoto, Y. & Kon, Y. 1988b. L i g h t a n d electron m i c r o s c o p i c studies o n c h i c k e n intestinal globule l e u k o c y t e . - Jpn. J. Vet. Res. 36: 83-117.
Oku, Y., Itayama, H . & Ohbayashi,
P r o l o n g e d expulsion of adult
Trichinella
spiralis and eosinophil i n f i l t r a t i o n i n mast cell-deficient W / W mice. - /. Helminth.
59: 233-239.
Keasbey, L. E. 1923. O n a new
f o r m of leucocyte
(Schollenleukozyt, W e i l l ) as f o u n d i n the gastric m u cosa of the sheep. - Folia haematologica
29: 155-171.
Kellas, L. M . 1961. A n intraepithelial granular cell i n
cal and c y t o c h e m i c a l studies, Zentralhl. Anat.
Histol.
Embryol.
Maximow, A . 1906.
U b e r die Z e l l f o r m e n des locke¬
ren Bindegewebes. - Arch. f. Mikr.
Michels, N . A . 1938. T h e mast cells. Acad. Sci. 103: 1-372. membranes.
III. T h e discharge
Kent, J. F. 1966a. Ultrastructure of the globule leucocyte of the rat. Anat. Rec. 154: 367-368. Kent, J. F.
1966b. D i s t r i b u t i o n and fine structure of
globule leucocytes i n respiratory and digestive tracts of the laboratory rat. - Anat. Rec. 156: 439-454. Kirkman, H . 1947. Intraepithelial granular cells i n u r i n a r y tracts of rats infected
with
Trichosomides
crassicauda. - Anat. Rec. 97: 349. (Schollen¬
leukozyten) of the u r i n a r y tract and o f possibly related cells. - Am. J. Anat. 86: 91-130. Kitagawa, H . , Ogata, K., Sugimura, M . , Hashimoto, Y. & Kudo, N . 1979. T h y m u s o r i g i n o f globule leucocytes i n chicken. - Jpn. J. Vet. Res. 27: 16¬ 18. Kitagawa, H . , Hashimoto, Y., Kon, Y. & Kudo, N . 1988a. D i s t r i b u t i o n of c h i c k e n globule leucocytes detected b y anti-thymocyte serum. - Jpn. J. Vet. Sa. 10
50: 638-647.
mast
Miller,
H . R. P. 1980. T h e structure,
o r i g i n and
f u n c t i o n o f mucosal mast cells. A brief r e v i e w . Biologie
Cellulaire
39: 229-232.
Miller, H . R. P., Murray, M . & Jarrett, W. F. H . 1968. G l o b u l e leukocytes and mast cells. - I n : Soof the Host to Para-
A c a d e m i c Press, Inc., N e w Y o r k 1968, p p .
198-210. Miller, H . R. P. & Jarrett, W. F. H . 1971.
Immune
reactions i n mucous membranes. I. Intestinal
mast
cell response d u r i n g h e l m i n t h e x p u l s i o n i n the rat. - Immunology
20: 277-288.
Murray, M . , Miller, H . R. P. & Jarrett, W. F. H . 1968.
T h e globule
leukocyte
a n d its d e r i v a t i o n
f r o m t h e subepithelial mast c e l l . - Laborat.
Invest.
19: 222-234. Nakano, T . , Sonoda, T . , Hayashi, C . , Yamatodani, A., Kanayama, Y., Yamamura, T., Asai, H . , Yonezawa, T . , Kitamura, Y. & Galli, S. J. 1985.
Kirkman, H . 1950. A comparative m o r p h o l o g i c a l and cytochemical study of globule leucocytes
o f intestinal
Invest. 24: 348-354.
ring the pregnancy cycle. - Acta Anat. 44: 109-130.
44: 91-115.
Ann. N. Y.
cells d u r i n g h e l m i n t h e x p u l s i o n i n the rat. - Lab.
sitism.
of the globule leucocyte of the sheep. - Anat. Rec.
-
Miller, H . R. P. 1971. I m m u n e reactions i n mucous,
ulsby, E . L . (Ed.), The Reaction
1952. T h e o r i g i n , fate and cytochemistry
Anat. ( B o n n ) 67:
680-757.
the uterine epithelium of some r u m i n a n t species duKent, J. F.
Vet. Med C .
11: 205-212.
Fate o f bone m a r r o w - d e r i v e d c u l t u r e d mast cells after intracutaneous, intraperitoneal and intravenous transfer i n t o genetically mast cell-deficient W / W mice. - /. Exp. Med.
v
162: 1025-1043.
Parmentier, H . K., Ruitenberg, E. J. & Elgersma, A.
1982. T h y m u s
dependence
o f the adoptive
transfer o f intestinal mastocytopoiesis i n spiralis-miecied
mice. - Int. Arch.
Allergy
Trichinella Appl. Im-
munol. 68: 260-267. Rahko, T . 1970. M a s t cells and globule leukocytes i n bile ducts o f cattle and sheep w i t h fascioliasis and dicrocoeliasis. Nytt Mag. Zool. 18: 111-112.
Rangifer, 11 (1), 1991
Rahko, T. 1970. G l o b u l e l e u k o c y t e and mast cell i n bile ducts of cattle naturally infected w i t h l i v e r f l u kes. Acta
Vet. Scand. 11: 219-227.
Rahko, T. 1971. and
murine
with
Fasciola
hepatica
w i t h reference to the mast cell and globule leucocyte. Ann. 1-62
Acad. Sei. fenn. A . V . M e d i c a , N : o
148:
(Thesis).
Rahko, T. 1972. Studies o n the pathology of dicrocoeliasis and fascioliasis in the goat III. T h e
histoche-
mistry of mast cells and globule leucocytes.
Acta
Vet. Scand 13: 575-584. Rahko, T. 1973.
Takeuchi, A., Jervis,
H.
R.
& Sprinz,
sa of the cat: A h i s t o c h e m i c a l , light and m i c r o s c o p i c study. Anat. Taliaferro, W. H .
Sarles, M . P. 1939. T h e cellu-
&
lar reaction i n the s k i n , lungs and intestine of normal and i m m u n e rats after infection w i t h
Seelig Jr., L. L.,
Tigelaar, R. E. &
1985. C o n j u g a t e d a v i d i n binds
Bergstresser, P. R. 27-32.
Acta
Fasciola
hepatica.
Vet. Scand. 14: 245-253. 1928.
Rogosina, M .
Toner, P. G . 1965.
Beiträge z u r K e n n t n i s des V e r -
dauungskanals der Fische. I. Ü b e r den Bau des E p i thels i n P y l o r u s a b s c h n i t t des Magens v o n ruthenus L. - 2. Mikrosk.
Acipenser
Forsch. 14: 333-372.
Anat.
&
Elgersma, A.
1976.
Absence
of intestinal mast cell response i n congenitally h y m i c mice d u r i n g Trichinella Nature (London) 264: Ruitenberg, E. J.
&
spiralis
-
258. A. 1979.
Response
i n the mouse d u and its indepen-
spiralis infection
dence of intestinal mast cells. - BY. J. Exp.
Pathol.
60: 246-251.
1931.
Tôrô, E.
1979. K i n e t i c s and characteristics
of intestinal mast
cells and globule leucocytes. - In: The Mast Cell, its Role in Health
and
Disease, eds. J . Pepys & A . M .
E d w a r d s , P i t m a n , L o n d o n , p . 732.
Entw.
1-38.
Vandenberghe, M . P. & Baert, J. 1981. G l o b u l e leucocytes i n the tracheal e p i t h e l i u m of rats. -
Ruitenberg, H . M . 1982. Effect of f i x a t i o n o n the light m i c r o s c o p i c a l v i s u a l i z a t i o n of mast cells and connective
d u o d e n u m . - Int.
tissue
Archs. Allergy
of the
Appl.
in
human
Immun.
67:
233-238. Selye, H . 1965. The Mast Cells. - B u t t e r w o r t h , W a s h i n g t o n , 488 pages.
1920. U b e r die leukocytàren
Darmschleimhaut Beurteilung Arch.
Mikr.
Whur, P.
der Sàugetiere.
der G r a n u l a t i o n e n Anat.
1967.
93:
Elemente
der
E i n Beitrag
zur
in Leukocyten.
G l o b u l e leucocyte
siliensis. - J. Comp. Path. 77: Whur, P.
&
response i n hy-
Gracie, M.
bra-
271-277.
1967. H i s t o c h e m i c a l c o m -
parision of mast cell and globule leucocyte in the rat. - Expenentia
-
1-81.
granules
23: 655-657.
globule
leucocytes
Nippostrongylus
in immune
brasiliensis
rats infected
with
and their possible
rela-
t i o n s h i p to the Russel b o d y cell. - /. Path. Bact. 93: 81-85. Whur, P. & White, R. G . 1970. Fluorescence scopy
of the
small intestines
micro-
of rats and sheep,
w i t h reference to the presence of i m m u n o g l o b u l i n i n globule leucocytes. - Int. Arch. Allergy
Appl.
Im-
munol. 38: 185-195.
Manuscript
Rangifer, 11 (1), 1991
Acta
anat. I l l : 268-276.
Whur, P. & Johnston, H . S. 1967. U l t r a s t r u c t u r e of
Ruitenberg, E. J., Gustowska, L., Elgersma, A. &
mucosa
61:
B e d e u t u n g u n d E n t s t e h u n g der Z e l l
granula i n der D a r m r e s o r p t i o n . - 2. Anat.
p e r - i m m u n e rats infected w i t h Nippostrongylus
Ruitenberg, E. J., Elgersma, A. & Lamers, C. H . J.
the
T h e fine structure of the g l o b u -
321-330.
Weill, P.
Elgersma,
of intestinal globule leucocytes r i n g a Trichinella
infection.
at-
33:
Cytochem.
le leucocyte i n the f o w l intestine. - Acta Anat.
Gesch. 94: Ruitenberg, E. J.
Nippost-
rongylus muris. - J. Inf. Dis. 64: 157-188.
to mast cell granules. /. Histochem.
with
electron
164: 79-100
Rec.
cattle
infected
H.
1969. T h e globule leucocyte i n the intestinal m u c o -
and globule leucocytes i n the c o m m o n bile duct of chronically
Vet. ]. 32: 237¬
240.
Tharp, M . D.,
O n the ultrastructure of mast cells
ovine
a b o m a s u m and the r e l a t i o n of the globule l e u k o c y te to nematode infestations. - Aust.
Studies o n the p a t h o l o g y of b o v i n e
l i v e r infected
Sommerville, R. J. 1956. T h e h i s t o l o g y o f the
accepted 4 December,
1990
11
