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Cuboidal epithelium lining of the parietal layer of Bowman's capsule in Afghan pikas (Ochotona rufescens rufescens)
J. Comp. Path. 1991Vol. 104
Cuboidal Epithelium Lining of the Parietal Layer of Bowman's Capsule in Afghan Pikas (Ochotona
rufeseens rufeseens) H. M a d a r a m e , M. K u m a g a l , N. M o t o o k a and S. Konno
Department of ExperimentalPathology, School of VeterinaryMedicine and Animal Sciences, Kitasato University, Towada, Aomori, Japan Summary Kidneys of 64 Afghan pikas (Ochotona rzfescens rzfescens) were examined histologically. Seven of 21 males and two of 21 females over 6 months of age had a cuboidal epithelium lining of the parietal layer of Bowman's capsule.
Introduction In the mouse, a marked sex difference is seen in the type of epithelium of Bowman's capsules. Cuboidal epithelium is seen in many glomeruli of the adult male and squamous epithelium in the female, the young, and the castrated male (Hummel, Richardson and Fekete, 1966; Liebelt, 1986). The difference is androgen-dependent (Liebelt, 1986). In other species, the incidence of cuboidal-type parietal epithelium is very low and the reason is unknown (Liebelt, 1986). In the Afghan pika (Ocholona rufescens rufescens), glomerulonephritis is an important feature ofautoimmune disease (Okudaira, Terada, Ito, Yamamoto, Mizoguchi, Ogita and Nomura, 1981). Up to now, however, no other significant morphological characteristics of the kidney, including any changes in the cuboidal parietal epithelium in Bowman's capsule, have been reported. The purpose of this paper is to describe the morphological features and frequency of the cuboidal parietal epithelium of Bowman's capsule in the Atghan pika.
Materials and Methods The 64 Afghan pikas (from 42 to 745 days old) used for this investigation were donated by the Central Institute for Experimental Animals of Japan (Kawasaki, Japan) and kept at Kitasato University. The animals were given a commercial solid food for pikas (CLEA-177 type, CLEA, Japan) and tap water ad libitum. They were placed in an air-conditioned feeding room maintained at 23-1-2°C, 60-t-10 per cent humidity. Other breeding and rearing procedures followed methods previously reported (Matsuzaki, Saito, Yamanaka, Esaki and Nomura, 1980). All animals were necropsied after natural death or after being killed by an overdose of ether. After post-mortem examination, both kidneys were fixed in 10 per cent 0021-9975/91/010017+05 $03.00/0
© 1991AcademicPressLimited
18
H. Madarame e t al.
neutral buffered formalin and routinely processed for the preparation of paraffin wax sections. Sections were cut 3 to 41.tm thick and stained with haematoxylin and eosin (HE), periodic acid-Schiff, periodic acid-silver methenamine and Masson's trichrome. The renal lesions were evaluated according to the location of the renal corpuscles. We distinguished renal corpuscles at three levels, superficial, midcortical and juxtamedullary layer. Twenty renal corpuscles of each layer were examined microscopically. Results
A simple cuboidal epithelium, extending more than half the distance along the capsular circumference, lined the parietal layer of the capsule in some corpuscles (more than 10 per cent out of 20 examined glomeruli of each layer). This epithelium resembled that of the proximal convoluted tubules: (1) the cell had an acidophilic cytoplasm, with a spherical nucleus (Fig. 1); (2) the free surface sometimes had a brush-border-like structure (Fig. 2); (3) at the urinary pole, the epithelium of the parietal Bowman's capsule was continuous with the proximal convoluted tubules (Fig. 3). Seven of 21 male pikas over 6 m o n t h s of age had a cuboidal epithelium, while only two of 21 females had similar epithelial lining. In only four males over 10 months o f age, almost 25 per cent of the renal corpuscles had cuboidal epithelium. In pikas under 6 m o n t h s of age, the corpuscles were almost entirely covered with the flattened epithelium and cuboidal cells occurred in a small part of the renal capsule (extending less than half the distance along the capsular distance) in both sexes. T h e sex differences examined were not statistically significant ( P < 0"05) (Table 1). Segmental increase of mesangial matrix and mesangial cells and segmental thickening of capillary loops were observed. These changes of the m e s a n g i u m and tuft o f capillaries varied in each glomerulus. On the other hand, crescent formation associated with glomerulonephritis was found in 56"3 per cent of all examined pikas (Table 2). There was no predilection for age or sex (P<0"05). T h e degree of crescent formation was graded + (mild case) to + + + (marked case) by assessment of the n u m b e r s of crescents (Table 2). Although crescent formation was of high incidence, the percentage of markedly affected cases was not high. Only three female pikas over 10 months of age had many crescents (more than half of e x a m i n e d glomeruli). In the frequency of the cuboidal epithelium of Bowman's capsule a n d the crescents, there was a difference in the location of affected glomeruli. T h e glomeruli at thejuxtamedullary layer had a higher frequency than those in the superficial and midcortical layers. Both changes sometimes coexisted in the same individual, furthermore, in the same glomerulus (Fig. 4). Discussion
In some inbred mice strains, cuboidal parietal epithelium in Bowman's capsule is common and its aetiology has been noted as an androgen-dependent feature (Liebelt, 1986). A similar sexual dimorphism, which may be male h o r m o n e dependent, has been observed in Long-Evans rats (.Jakowski, 1982). T h e incidence o f cuboidal epithelium in other species, including human beings, is
Bowman's
Capsule
Epithelium
in Afghan Pika
19
Fig. 1, Glomerulus. Parietal layer of Bowman's capsule showing cuhoidal cells with all acidophilic cytoplasm and spherical nucleus. HE x400. Fig. 2.
The flee stu'thce at" the epithelium shows a brush-border-like structure. Masson's trichrame x 480.
extremely low and its aetiology has not been clarified. Some cases have been found incidentally and have been associated with various conditions such as an arrested development or neoplasia (Liebelt, 1986). In our cases, the males had a higher incidence of" cuboidal parietal epithelium than the females. Our data, therelbre, suggest that the occurrence ofcuboidal epithelium is related to sex. However, the sex differences were not statistically significant (P < 0.05). The aetiology of this condition needs further elucidation. Age- and sex-related dimorphism in glomerulonephritis of tlle Afghan pika
20
H. M a d a r a m e
et al.
Fig. 3.
Epithelium of the parietal Bowman's capsule continuous with proximal convoluted urinary tubule. Acid silver methenamine x480.
Fig, 4.
Cuboidal epithelium in the top half and crescent in the bottom half of Bowman's space in one glomerulus, Acid silver methenamine x 400.
has been reported (Okudaira et al., 1981). T h e y described two characteristic features: (I) tkmale pikas began to manifest glomerulonephritis at 4 to 6 months of age and the n u m b e r of the affected glomeruli increased with age; (2) glomeruli with crescent formation were often seen in females over the age of 10 months, Our cases also demonstrated more severe crescent formation in females older than 10 months, There is a possibility that the presence ofcuboidal epithelium in f~male pikas more than 10 months of age may be obscured by glomerular changes associated with glomerulonephritis, especially by crescents.
Bowman's
21
C a p s u l e E p i t h e l i u m in A f g h a n P i k a
Table 1 Age, sex and incidence of cuboidal epithelium in the Afghan pika
Animals with cuboidalepithelinm*
Animah" examined
Per cent
male female
0 0
7 l5
0 0
6 to 10
male female
1 1
5 i4
20.0 7"1
>10
male female
6 1
t6 7
37"5 14.3
9
64
14.1
Age (months)
Sex
<6
Total
* More than 10 pet"cent of the 60 glomeruli examined had a simple cuboidal epithelium, extending more than half the distance along the capsular circumfi'a'ence. Table 2 Age, sex and degree of crescent formation in the Afghan pika
+ + +*
++
+
Animals examined
Per cent
male female
0 0
O 1
2 5
7 15
28'6 40'0
6 to 10
male female
0 0
1 3
l 6
5 14
41).0 64"3
>10
male fi:male
0 3
3 0
9 2
16 7
75'0 71.4
3
8
25
64
56'3
Age (months)
Sex
<6
Total
*+, Less than 10 per cent of the 60 glomeruli examined had crescents; + +, 10 to 50 per cent of tile glomeruli had crescents; + + +, more than 50 per cent of the gtomeruli had crescents. References
H u m m e l , K.P., Richardson, F.L. and Fekete E. (1966). Anatomy. I n Biology of the Laboratory Mouse, 2nd edit. E.L. Green, Ed. M c G r a w - H i l l , New York, T o r o n t o , Sydney and L o n d o n , pp. 247-307. Jakowski, R.M. (1982). Renal t u b u l a r epithelium lining parietal layer of B o w m a n ' s capsule in a d u l t Long-Evans rats. Veterinary Pathology, 19, 212-215. Liebelt, A.G. (1986). U n i q u e features of anatomy, histology, and ultrastructure, kidney, mouse. In: Monographs on Pathology of Laboratory Animals, Urinary System. T.C. Jones, U. M o h r and R.D. Hunt, Eds. Springer-Verlag, Berlin, Heidelberg and New York, pp. 2 4 4 4 . Matsuzaki, T., Saito, M., Y a m a n a k a , M., Esaki, K. and N o m u r a , T. (1980). Breeding and rearing of the pika (Ochotona rufescens nfescens) as a new laboratory a n i m a l species. Experimental Animals, 29, 165-170. Okudaira, H., T e r a d a , E., Ito, T., Yamamoto, K., Mizoguchi, Y., Ogita, T. a n d Nomura, T. (1981). A u t o i m m u n e glomerulonephritis and hemolytic a n e m i a in a new laboratory animal, the Afghan pika. Clinical [mmunology and [mmunopathology, 21,375-386.
I
Received, March 13lh, 1990] Accepted, June 9th, 1990 _]
Cuboidal Epithelium Lining of the Parietal Layer of Bowman's Capsule in Afghan Pikas (Ochotona
rufeseens rufeseens) H. M a d a r a m e , M. K u m a g a l , N. M o t o o k a and S. Konno
Department of ExperimentalPathology, School of VeterinaryMedicine and Animal Sciences, Kitasato University, Towada, Aomori, Japan Summary Kidneys of 64 Afghan pikas (Ochotona rzfescens rzfescens) were examined histologically. Seven of 21 males and two of 21 females over 6 months of age had a cuboidal epithelium lining of the parietal layer of Bowman's capsule.
Introduction In the mouse, a marked sex difference is seen in the type of epithelium of Bowman's capsules. Cuboidal epithelium is seen in many glomeruli of the adult male and squamous epithelium in the female, the young, and the castrated male (Hummel, Richardson and Fekete, 1966; Liebelt, 1986). The difference is androgen-dependent (Liebelt, 1986). In other species, the incidence of cuboidal-type parietal epithelium is very low and the reason is unknown (Liebelt, 1986). In the Afghan pika (Ocholona rufescens rufescens), glomerulonephritis is an important feature ofautoimmune disease (Okudaira, Terada, Ito, Yamamoto, Mizoguchi, Ogita and Nomura, 1981). Up to now, however, no other significant morphological characteristics of the kidney, including any changes in the cuboidal parietal epithelium in Bowman's capsule, have been reported. The purpose of this paper is to describe the morphological features and frequency of the cuboidal parietal epithelium of Bowman's capsule in the Atghan pika.
Materials and Methods The 64 Afghan pikas (from 42 to 745 days old) used for this investigation were donated by the Central Institute for Experimental Animals of Japan (Kawasaki, Japan) and kept at Kitasato University. The animals were given a commercial solid food for pikas (CLEA-177 type, CLEA, Japan) and tap water ad libitum. They were placed in an air-conditioned feeding room maintained at 23-1-2°C, 60-t-10 per cent humidity. Other breeding and rearing procedures followed methods previously reported (Matsuzaki, Saito, Yamanaka, Esaki and Nomura, 1980). All animals were necropsied after natural death or after being killed by an overdose of ether. After post-mortem examination, both kidneys were fixed in 10 per cent 0021-9975/91/010017+05 $03.00/0
© 1991AcademicPressLimited
18
H. Madarame e t al.
neutral buffered formalin and routinely processed for the preparation of paraffin wax sections. Sections were cut 3 to 41.tm thick and stained with haematoxylin and eosin (HE), periodic acid-Schiff, periodic acid-silver methenamine and Masson's trichrome. The renal lesions were evaluated according to the location of the renal corpuscles. We distinguished renal corpuscles at three levels, superficial, midcortical and juxtamedullary layer. Twenty renal corpuscles of each layer were examined microscopically. Results
A simple cuboidal epithelium, extending more than half the distance along the capsular circumference, lined the parietal layer of the capsule in some corpuscles (more than 10 per cent out of 20 examined glomeruli of each layer). This epithelium resembled that of the proximal convoluted tubules: (1) the cell had an acidophilic cytoplasm, with a spherical nucleus (Fig. 1); (2) the free surface sometimes had a brush-border-like structure (Fig. 2); (3) at the urinary pole, the epithelium of the parietal Bowman's capsule was continuous with the proximal convoluted tubules (Fig. 3). Seven of 21 male pikas over 6 m o n t h s of age had a cuboidal epithelium, while only two of 21 females had similar epithelial lining. In only four males over 10 months o f age, almost 25 per cent of the renal corpuscles had cuboidal epithelium. In pikas under 6 m o n t h s of age, the corpuscles were almost entirely covered with the flattened epithelium and cuboidal cells occurred in a small part of the renal capsule (extending less than half the distance along the capsular distance) in both sexes. T h e sex differences examined were not statistically significant ( P < 0"05) (Table 1). Segmental increase of mesangial matrix and mesangial cells and segmental thickening of capillary loops were observed. These changes of the m e s a n g i u m and tuft o f capillaries varied in each glomerulus. On the other hand, crescent formation associated with glomerulonephritis was found in 56"3 per cent of all examined pikas (Table 2). There was no predilection for age or sex (P<0"05). T h e degree of crescent formation was graded + (mild case) to + + + (marked case) by assessment of the n u m b e r s of crescents (Table 2). Although crescent formation was of high incidence, the percentage of markedly affected cases was not high. Only three female pikas over 10 months of age had many crescents (more than half of e x a m i n e d glomeruli). In the frequency of the cuboidal epithelium of Bowman's capsule a n d the crescents, there was a difference in the location of affected glomeruli. T h e glomeruli at thejuxtamedullary layer had a higher frequency than those in the superficial and midcortical layers. Both changes sometimes coexisted in the same individual, furthermore, in the same glomerulus (Fig. 4). Discussion
In some inbred mice strains, cuboidal parietal epithelium in Bowman's capsule is common and its aetiology has been noted as an androgen-dependent feature (Liebelt, 1986). A similar sexual dimorphism, which may be male h o r m o n e dependent, has been observed in Long-Evans rats (.Jakowski, 1982). T h e incidence o f cuboidal epithelium in other species, including human beings, is
Bowman's
Capsule
Epithelium
in Afghan Pika
19
Fig. 1, Glomerulus. Parietal layer of Bowman's capsule showing cuhoidal cells with all acidophilic cytoplasm and spherical nucleus. HE x400. Fig. 2.
The flee stu'thce at" the epithelium shows a brush-border-like structure. Masson's trichrame x 480.
extremely low and its aetiology has not been clarified. Some cases have been found incidentally and have been associated with various conditions such as an arrested development or neoplasia (Liebelt, 1986). In our cases, the males had a higher incidence of" cuboidal parietal epithelium than the females. Our data, therelbre, suggest that the occurrence ofcuboidal epithelium is related to sex. However, the sex differences were not statistically significant (P < 0.05). The aetiology of this condition needs further elucidation. Age- and sex-related dimorphism in glomerulonephritis of tlle Afghan pika
20
H. M a d a r a m e
et al.
Fig. 3.
Epithelium of the parietal Bowman's capsule continuous with proximal convoluted urinary tubule. Acid silver methenamine x480.
Fig, 4.
Cuboidal epithelium in the top half and crescent in the bottom half of Bowman's space in one glomerulus, Acid silver methenamine x 400.
has been reported (Okudaira et al., 1981). T h e y described two characteristic features: (I) tkmale pikas began to manifest glomerulonephritis at 4 to 6 months of age and the n u m b e r of the affected glomeruli increased with age; (2) glomeruli with crescent formation were often seen in females over the age of 10 months, Our cases also demonstrated more severe crescent formation in females older than 10 months, There is a possibility that the presence ofcuboidal epithelium in f~male pikas more than 10 months of age may be obscured by glomerular changes associated with glomerulonephritis, especially by crescents.
Bowman's
21
C a p s u l e E p i t h e l i u m in A f g h a n P i k a
Table 1 Age, sex and incidence of cuboidal epithelium in the Afghan pika
Animals with cuboidalepithelinm*
Animah" examined
Per cent
male female
0 0
7 l5
0 0
6 to 10
male female
1 1
5 i4
20.0 7"1
>10
male female
6 1
t6 7
37"5 14.3
9
64
14.1
Age (months)
Sex
<6
Total
* More than 10 pet"cent of the 60 glomeruli examined had a simple cuboidal epithelium, extending more than half the distance along the capsular circumfi'a'ence. Table 2 Age, sex and degree of crescent formation in the Afghan pika
+ + +*
++
+
Animals examined
Per cent
male female
0 0
O 1
2 5
7 15
28'6 40'0
6 to 10
male female
0 0
1 3
l 6
5 14
41).0 64"3
>10
male fi:male
0 3
3 0
9 2
16 7
75'0 71.4
3
8
25
64
56'3
Age (months)
Sex
<6
Total
*+, Less than 10 per cent of the 60 glomeruli examined had crescents; + +, 10 to 50 per cent of tile glomeruli had crescents; + + +, more than 50 per cent of the gtomeruli had crescents. References
H u m m e l , K.P., Richardson, F.L. and Fekete E. (1966). Anatomy. I n Biology of the Laboratory Mouse, 2nd edit. E.L. Green, Ed. M c G r a w - H i l l , New York, T o r o n t o , Sydney and L o n d o n , pp. 247-307. Jakowski, R.M. (1982). Renal t u b u l a r epithelium lining parietal layer of B o w m a n ' s capsule in a d u l t Long-Evans rats. Veterinary Pathology, 19, 212-215. Liebelt, A.G. (1986). U n i q u e features of anatomy, histology, and ultrastructure, kidney, mouse. In: Monographs on Pathology of Laboratory Animals, Urinary System. T.C. Jones, U. M o h r and R.D. Hunt, Eds. Springer-Verlag, Berlin, Heidelberg and New York, pp. 2 4 4 4 . Matsuzaki, T., Saito, M., Y a m a n a k a , M., Esaki, K. and N o m u r a , T. (1980). Breeding and rearing of the pika (Ochotona rufescens nfescens) as a new laboratory a n i m a l species. Experimental Animals, 29, 165-170. Okudaira, H., T e r a d a , E., Ito, T., Yamamoto, K., Mizoguchi, Y., Ogita, T. a n d Nomura, T. (1981). A u t o i m m u n e glomerulonephritis and hemolytic a n e m i a in a new laboratory animal, the Afghan pika. Clinical [mmunology and [mmunopathology, 21,375-386.
I
Received, March 13lh, 1990] Accepted, June 9th, 1990 _]