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Annulate lamellae in frog adenohypophysis under normal and experimental conditions
Cell Biology
Annulate
international
Lamellae
F. Gracia-Navarro, Catedra
Reports,
Vol. 4, No. 11, November
in Frog Adenohypophysis Experimental Conditions
Under
1980
Normal
1045
and
A. Ruiz-Navarro and G. Garcia-Herdugo de Citologia e Histologia Facultad de Ciencias Universidad de Cordoba Spain
ABSTRACT Cytoplasmic annulate lamellae have been observed in frog (Rana ridibunda) adenohypophysis pars distalis from normal spring animals and from others which were submitted to experimental conditions inducing selective activation of different cell types. Cell activation, because of either the normal active period in the frog cycle or the experiemntal treatments, seems to be correlated with the occurrenThese annulate lamellae consist of a successice annulate lamellae. on of two relatively parallel membranes interrupted periodically by discontinuities similar to nuclear pores. Sometimes they have been observed connected to endoplasmic reticulum. LNTRODUCTION Annulate lamellae have been reported both in aAccording nimal (Maul, 1977) and plant cells (Franke et al. , 1972). to Wischitzer (1970) the cells containing annulate lamellae have especially intensive metabolic needs. Benzo (1972) described them as rawhich develop annulate lamellae during the courpidly growing cells, se of their functional differentiation, and Coward (1973) suggests that annulate lamellae can also occur in cells altering their state of differentiation in preparation for division. In the adult frog’s pars distalis six different cellular types have been observed: prolactin cells (LTH), growth hormone cells (STH),gonadotropic hormone cells, thyreotropic hormone cells (TSH), corticotropic hormone cells (ACTH) and follicular cells. These types are characterized by their ultrastructure and degree or development of cytoplasmatic organelles (Doerr-Schott , 1980). According to Doerr-Schott (1974) gonadotropic and TSH cells have a well developed Golgi complex, rough reticulum, and the granullations show different density; the difference between both cellular types are size, disposition and variety of granullations, having the 0309-I 651/80/111045-06/$02.00/0
0 1980 Academic
Press Inc. (London)
Ltd.
1046
Cell Biology
International
Reports,
Vol. 4, No, 11, November
1980
gonadotropic cells polygonal morphology and many granules and lysosomes, but the TSH are spherically shaped and their granules are located in the cellular periphery. ACTH are spherical or oval with rounded nucleus, small and polymorphic cytoplasmatic granules, little or no development of the Golgi complex and rough reticulum, and usually they do not have lysosomes. OBSERVATIONS We found annulate lamellae in gonadotropic, TSH, and ACTH cells from frog hypophysis collected during the spring, and in the following experimental conditions: A) Animals collected in spring and placed in a desicator for 8 hours B) Frogs collected in winter and subjected to a constant temperature of 20’ C for 2 to 4 weeks, and C) Spring animals injected with TRH 1 pg/30 g body weight, and killed 4 hours later. Gonadotropic cells with annulate lamellae were obseved in aniamals collected in the spring (Fig. 1 and 2) and in winter-collected nimals activated by increasing temperature (Fig. 3 and 4). These cells showed a higher development of their Golgi complex, higher elec tron density of the mitocondrial matrix and partial degranullation of their cytoplasm. TSH cells showing annulate lamellae were observed in animals injected with TRH, having even higher development of their rough reticulum and a partial degranullation of their cytoplasm. ACTH cells with annulate lamellae were observed in water deprived animals (Fig. 5 and 6). These cells showed grater cell size, many granules and lysosomes, a polymorphic nucleus and increased development of its rough reticulum and Golgi complex.
with
All these morphological features the same cellular types observed
are described in hibernating
in comparison animals.
The annulate lamellae which we have observed consist in series of two relatively parallel membranes surrounding cisternae which sometimes connect with the rough endoplasmic reticulum (Fig. 6). In transverse planes of section the cisternae appear interrupted by disIn tangential section the discontinuicontinuities (Fig. 2, 3 and 6). ties appear as regularly spaced annuli showing structures similar to the pore complex of the nuclear envelope (Fig. 3 and 5). DISCUSSION ved is similar
The ultrastructure of the annulate Iamellae obserto that described by Wischnitzer (1970) but we did not
Cell Biology
International
Reports,
Vol. 4, No. 11, November
7980
1047
I-. I lg. 1. Gonadotropic cell of animal collected in the spring showing annulaInset detail of the annulate lamete lamellae (al) near the Golgi complex. F-ig. 2. Annulate lamellae in a gonadotropic The bar equals 0,5 pm. llae. cell of an animal collected in the spring. The bar equals 0,25pm. Fig. 3 and 4. Annulate lamellae in gonadotropic cells of hibernating animals actiThe bar equals 0,5pm. vated by increasing of temperature.
1048
Cell Biology
International
Reports,
Vol. 4, No. 11, November
to desication, surrounFig. 5. A .C .T. H. cell from frog subjected ding a T. S . H. cell, and showing great size, granullar polarization towars a capillar (C) , polymorphic nucleus with invagination (arrow) and annulate lamellae (al). The bar equals 2 pm.
1980
Cell Biology
International
Fig. 6. Detail connected with
Reports,
Vol. 4, No. 11, November
1980
of the annulate lamellae of the ACTH cell of figure the rough reticulum (arrows). The bar equals 0,5pm.
find the annulus-free in gastrodermal cells
membranes portions reported of regenerating planaria.
by Coward
5,
(1979)
Gonadotropic and TSH adenohypophysial cells showing annulate lamellae, in comparison with the same cell types observed in winter animals have a morphology which corresponds to the first stage (degranulation) in the activation of glandular cells, but the morphology of ACTH cells showing annulate lamellae corresponds the stage of hor mone synthesis and storage (Kurosomi, 1961). Therefore, we find that annulate lamellae are correlated with the morphology of very active glandular cells only, which leds us to assu me that these structures may play some role in cellular processes. The concrete function of the annulate lamellae in these cells could be, as Coward (1979) suggests , a preparation for nuclear and cytoplasmatic membrane construction before the cell division, considering that these cells are altering their state of differentiation and are preparing for division. Nevertheless the low rate of mitoses relaported by Dierickx et al. (1971), and the occurrence of annulate mellae in differentiated cells whose morphology suggests glandular hy-
1050
Cell Biology
International
Reports,
Vol. 4, No. 11, November
7980
peractivity, lead us to the hypothesis that these annulate lamellae, at least in adenohypophysial frog cells are a depository of membranes for increasing the rough reticulum and the Golgi complex, and are thus involved with the formation and production of secretory granules and lysosomes. MATERIAL AND METHODS Pituitaries of adult Rana ridibunda were collected from normal animals in spring, winter and from other submitted to the experimental conditions described above, The procedure for observations were standard for similar electron microscopic studies. Acknowledgements. - We gratefully acknowlede critical reading of the manuscript by Dr. R. Andrews (Virginia Polytech. Inst. and State Univ.) REFERENCES Benzo, C .A. (1972) The annulate lamellae of chick embryo liver cells in organ culture. Anatomical Record, 174, 399-406. Coward, S. J. (1979) On the occurrence and significance of annutate lamellao in gastrodermal cells of regenerating planarians . Cell Biology International Reports, 3 , 101-106. Dierickx, K. , Gossens, N. and Van den Branden, C. (1971) Cyclical mitotic activity in the adenohypophysis of Rana temporaria . Zeitschrift fur Zellforschung und mikroskopisch Anatomie, 115, 579-586. Doerr-Schott, J . (1974) Cytoimmunochemical study of the hypophysial cells of amphibians by light and electron microscopy. Fortschritte der Zoologie, 22 245-267. Doerr-Schott, J . (1980) Immunohistochemistry of the adenohypophysis of non-mammalian vertebrates. Acta histochemica , Suppl. -Band XXI I , S. 185-223. Franke, W.W., Scheer, U. and Fritsch, H. (1972) Intranuclear and cytoplasmatic annulate lamellae in plant cells. Journal of Cell Biology, 53, 823-827. Kurosomi, K. (1961) Electron microscopic analysis of the secretion mechanism. In G .H. Bourne and J . F. Danielli (eds .> International Review of Cytology, 11, 1. Academic Press, New York. Maul, C. (1977) The molecular and cytoplasmatic pore complex: structure, dynamics, distribution and evolution. International Review of cytology, suppl. 6. 75. Wischnitzer, S. (1970) The annulate lamellae. In G .H. Bourne and J .F. Danielli (eds .> International Review of Cytology, 27, 65-100. Academic Press, New York. Received :
18th July
1980
Accepted :
28th
July
1980
Annulate
international
Lamellae
F. Gracia-Navarro, Catedra
Reports,
Vol. 4, No. 11, November
in Frog Adenohypophysis Experimental Conditions
Under
1980
Normal
1045
and
A. Ruiz-Navarro and G. Garcia-Herdugo de Citologia e Histologia Facultad de Ciencias Universidad de Cordoba Spain
ABSTRACT Cytoplasmic annulate lamellae have been observed in frog (Rana ridibunda) adenohypophysis pars distalis from normal spring animals and from others which were submitted to experimental conditions inducing selective activation of different cell types. Cell activation, because of either the normal active period in the frog cycle or the experiemntal treatments, seems to be correlated with the occurrenThese annulate lamellae consist of a successice annulate lamellae. on of two relatively parallel membranes interrupted periodically by discontinuities similar to nuclear pores. Sometimes they have been observed connected to endoplasmic reticulum. LNTRODUCTION Annulate lamellae have been reported both in aAccording nimal (Maul, 1977) and plant cells (Franke et al. , 1972). to Wischitzer (1970) the cells containing annulate lamellae have especially intensive metabolic needs. Benzo (1972) described them as rawhich develop annulate lamellae during the courpidly growing cells, se of their functional differentiation, and Coward (1973) suggests that annulate lamellae can also occur in cells altering their state of differentiation in preparation for division. In the adult frog’s pars distalis six different cellular types have been observed: prolactin cells (LTH), growth hormone cells (STH),gonadotropic hormone cells, thyreotropic hormone cells (TSH), corticotropic hormone cells (ACTH) and follicular cells. These types are characterized by their ultrastructure and degree or development of cytoplasmatic organelles (Doerr-Schott , 1980). According to Doerr-Schott (1974) gonadotropic and TSH cells have a well developed Golgi complex, rough reticulum, and the granullations show different density; the difference between both cellular types are size, disposition and variety of granullations, having the 0309-I 651/80/111045-06/$02.00/0
0 1980 Academic
Press Inc. (London)
Ltd.
1046
Cell Biology
International
Reports,
Vol. 4, No, 11, November
1980
gonadotropic cells polygonal morphology and many granules and lysosomes, but the TSH are spherically shaped and their granules are located in the cellular periphery. ACTH are spherical or oval with rounded nucleus, small and polymorphic cytoplasmatic granules, little or no development of the Golgi complex and rough reticulum, and usually they do not have lysosomes. OBSERVATIONS We found annulate lamellae in gonadotropic, TSH, and ACTH cells from frog hypophysis collected during the spring, and in the following experimental conditions: A) Animals collected in spring and placed in a desicator for 8 hours B) Frogs collected in winter and subjected to a constant temperature of 20’ C for 2 to 4 weeks, and C) Spring animals injected with TRH 1 pg/30 g body weight, and killed 4 hours later. Gonadotropic cells with annulate lamellae were obseved in aniamals collected in the spring (Fig. 1 and 2) and in winter-collected nimals activated by increasing temperature (Fig. 3 and 4). These cells showed a higher development of their Golgi complex, higher elec tron density of the mitocondrial matrix and partial degranullation of their cytoplasm. TSH cells showing annulate lamellae were observed in animals injected with TRH, having even higher development of their rough reticulum and a partial degranullation of their cytoplasm. ACTH cells with annulate lamellae were observed in water deprived animals (Fig. 5 and 6). These cells showed grater cell size, many granules and lysosomes, a polymorphic nucleus and increased development of its rough reticulum and Golgi complex.
with
All these morphological features the same cellular types observed
are described in hibernating
in comparison animals.
The annulate lamellae which we have observed consist in series of two relatively parallel membranes surrounding cisternae which sometimes connect with the rough endoplasmic reticulum (Fig. 6). In transverse planes of section the cisternae appear interrupted by disIn tangential section the discontinuicontinuities (Fig. 2, 3 and 6). ties appear as regularly spaced annuli showing structures similar to the pore complex of the nuclear envelope (Fig. 3 and 5). DISCUSSION ved is similar
The ultrastructure of the annulate Iamellae obserto that described by Wischnitzer (1970) but we did not
Cell Biology
International
Reports,
Vol. 4, No. 11, November
7980
1047
I-. I lg. 1. Gonadotropic cell of animal collected in the spring showing annulaInset detail of the annulate lamete lamellae (al) near the Golgi complex. F-ig. 2. Annulate lamellae in a gonadotropic The bar equals 0,5 pm. llae. cell of an animal collected in the spring. The bar equals 0,25pm. Fig. 3 and 4. Annulate lamellae in gonadotropic cells of hibernating animals actiThe bar equals 0,5pm. vated by increasing of temperature.
1048
Cell Biology
International
Reports,
Vol. 4, No. 11, November
to desication, surrounFig. 5. A .C .T. H. cell from frog subjected ding a T. S . H. cell, and showing great size, granullar polarization towars a capillar (C) , polymorphic nucleus with invagination (arrow) and annulate lamellae (al). The bar equals 2 pm.
1980
Cell Biology
International
Fig. 6. Detail connected with
Reports,
Vol. 4, No. 11, November
1980
of the annulate lamellae of the ACTH cell of figure the rough reticulum (arrows). The bar equals 0,5pm.
find the annulus-free in gastrodermal cells
membranes portions reported of regenerating planaria.
by Coward
5,
(1979)
Gonadotropic and TSH adenohypophysial cells showing annulate lamellae, in comparison with the same cell types observed in winter animals have a morphology which corresponds to the first stage (degranulation) in the activation of glandular cells, but the morphology of ACTH cells showing annulate lamellae corresponds the stage of hor mone synthesis and storage (Kurosomi, 1961). Therefore, we find that annulate lamellae are correlated with the morphology of very active glandular cells only, which leds us to assu me that these structures may play some role in cellular processes. The concrete function of the annulate lamellae in these cells could be, as Coward (1979) suggests , a preparation for nuclear and cytoplasmatic membrane construction before the cell division, considering that these cells are altering their state of differentiation and are preparing for division. Nevertheless the low rate of mitoses relaported by Dierickx et al. (1971), and the occurrence of annulate mellae in differentiated cells whose morphology suggests glandular hy-
1050
Cell Biology
International
Reports,
Vol. 4, No. 11, November
7980
peractivity, lead us to the hypothesis that these annulate lamellae, at least in adenohypophysial frog cells are a depository of membranes for increasing the rough reticulum and the Golgi complex, and are thus involved with the formation and production of secretory granules and lysosomes. MATERIAL AND METHODS Pituitaries of adult Rana ridibunda were collected from normal animals in spring, winter and from other submitted to the experimental conditions described above, The procedure for observations were standard for similar electron microscopic studies. Acknowledgements. - We gratefully acknowlede critical reading of the manuscript by Dr. R. Andrews (Virginia Polytech. Inst. and State Univ.) REFERENCES Benzo, C .A. (1972) The annulate lamellae of chick embryo liver cells in organ culture. Anatomical Record, 174, 399-406. Coward, S. J. (1979) On the occurrence and significance of annutate lamellao in gastrodermal cells of regenerating planarians . Cell Biology International Reports, 3 , 101-106. Dierickx, K. , Gossens, N. and Van den Branden, C. (1971) Cyclical mitotic activity in the adenohypophysis of Rana temporaria . Zeitschrift fur Zellforschung und mikroskopisch Anatomie, 115, 579-586. Doerr-Schott, J . (1974) Cytoimmunochemical study of the hypophysial cells of amphibians by light and electron microscopy. Fortschritte der Zoologie, 22 245-267. Doerr-Schott, J . (1980) Immunohistochemistry of the adenohypophysis of non-mammalian vertebrates. Acta histochemica , Suppl. -Band XXI I , S. 185-223. Franke, W.W., Scheer, U. and Fritsch, H. (1972) Intranuclear and cytoplasmatic annulate lamellae in plant cells. Journal of Cell Biology, 53, 823-827. Kurosomi, K. (1961) Electron microscopic analysis of the secretion mechanism. In G .H. Bourne and J . F. Danielli (eds .> International Review of Cytology, 11, 1. Academic Press, New York. Maul, C. (1977) The molecular and cytoplasmatic pore complex: structure, dynamics, distribution and evolution. International Review of cytology, suppl. 6. 75. Wischnitzer, S. (1970) The annulate lamellae. In G .H. Bourne and J .F. Danielli (eds .> International Review of Cytology, 27, 65-100. Academic Press, New York. Received :
18th July
1980
Accepted :
28th
July
1980