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Modified hamster atrial cardiac muscle cells isolated in the anterior chamber of the eye
JournalofMotecularandCellularCardiology (1977) 9, 1013-1017
SHORT COMMUNICATION
Modified H a m s t e r Atrial Cardiac M u s c l e Ceils Isolated in the Anterior C h a m b e r o f the Eye* J O H N O. O B E R P R I L L E R AND J E A N C. O B E R P R I L L E R
Department of Anatomy, University of North Dakota School of Medicine, Grand Forks, North Dakota 58202, U.S.A. (Received 13 oTune1977, acceptedin revisedform 7 August 1977) J. O. OBERPRILLERANDJ. C. OBER.PR.ILLER.Modified Hamster Atrial Cardiac Muscle Cells Isolated in the Anterior Chamber of the Eye. ~%urnalof MolecularandCellularCardlolog~ (1977) 9, 1013-1017. Piecesof atria from young hamsters were transplanted into the anterior chamber of the eye and observed for morphological changes at 5, I0, 20, 30, 40 and 60 days after transplantation. During this period of observation, the transplant was vascularized and the number of myocytes decreased. After 20 days the cardiac muscle cells were usually seen in small clusters in between an increasing amount of connective tissue and fat cells. There was no indication of proliferative activity of myocytes in the grafts. The most striking change in myocyte ultrastructure, beginning at 5 days and continuing throughout to 60 days, was a change in myofibrillar structure and an increase in sarcoplasmic reticulum in many cardiac muscle cells. In these cardiac muscle cells, the Z material was thickened and had attached thin filaments, and often these complexes were scattered at random throughout the cell in association with an accumulation of sarcoplasmic reticulum. These observations are discussed in relation to other reports of similar Z band/thin filament complexes and adjacent sarcoplasmic reticulum. I~Y WORDS: Transplantation; Atrium; Ultrastructure; Z bands; Sarcoplasmic reticulum.
1. Introduction T h e r e appears to be a variety of types of responses of c a r d i a c muscle ceils to i n j u r y . I n the a m p h i b i a n , v e n t r i c u l a r cardiac muscle cells c a n react to i n j u r y with a proliferative response [9, 11]. I n m a m m a l s , a proliferative response has b e e n reported i n atria o f hearts in which the left ventricle has been i n j u r e d [12]. T h e response of m a m m a l i a n ventricle seems to be l i m i t e d to the type o f r e g e n e r a t i v e responses reported b y Dusek et al. [4] in w h i c h the m a r g i n a l ceils of a n infarct c a n u n d e r g o p r o t e i n synthesis a n d b e c o m e similar i n a p p e a r a n c e to d e v e l o p i n g c a r d i a c muscle cells. T r a n s p l a n t a t i o n of tissue to the a n t e r i o r c h a m b e r of the eye has b e e n used to study the regenerative potential of m a m m a l i a n smooth muscle [3, 10]. T h i s system * This work was supported by a National Institutes of Health Institutional Grant No. 4314-28, from the University of North Dakota School of Medicine.
1014
J.o.
OBERPRILLER AND
j. c. OBERPRILLER
can be utilized in cardiac muscle as well, and observations have been m a d e of the changes in hamster atrial cells when isolated into the anterior chamber of thc eye. T h e present communication is primarily concerned with one of the major ultrastructural changes in the structure ofmyofibrillae and sarcoplasmic reticulum found in the atrial cells when isolated in the anterior chamber of the eye.
2. M a t e r i a l s a n d M e t h o d s
T h e animals used were young Syrian hamsters with an average weight of 110 g. Host and donor animals were anesthetized with an intraperitoneal injection of pentobarbitol (30 mg/kg), followed by ether as needed. Small pieces of atrium approximately 2 m m • 3 m m were removed from one animal and transplanted onto the iris of a host animal. T h e transplant was inserted through a small incision made in the cornea. In order for this incision to be made without injury to the iris, one drop of atropine (10 mg/ml) was first applied to the cornea. After the implant was placed on the anterior surface of the iris, it was manipulated to the lateral edge of the iris. T h e graft and the underlying portion of the host iris were fixed from at least four eyes at 5, 10, 20, 30, 40 and 60 days after transplantation. Untransplanted atria were also fixed as controls. The tissues were fixed in 3o/0 glutaraldehyde, buffered at p H 7.4 with 0. I M phosphate buffer, and post-osmicated in Millonig's fixative. After dehydration in a graded series of ethanols, they were embedded in Epon 812. Sections 1 to 2 ~m in thickness were prepared for light microscopy and stained with toluidine blue. Ultrathin sections were obtained for transmission electron microscopy, stained with lead citrate and uranyl acetate, and were examined in a Philips EM-200 electron microscope.
3. R e s u l t s
By 5 days after implantation, the graft was vascularized, as evidenced by the presence of capillaries containing red blood cells. At this time, m a n y fibers within the graft were separated by large connective tissue spaces which contained m a n y macrophages and some degenerating fibers. By 20 days after grafting, fewer cardiac muscle cells were observed within the graft than were seen at 5 days. Those that were present often were arranged in small clusters (Plate 1). Although not demonstrated in Plate 1, m a n y of the 20-day grafts contained a n u m b e r of large fat cells, which are infrequently seen in control atria. In the 30, 40 and 60 day graft specimens, increasing numbers of fat cells were observed. At the same time, there was a decrease in the n u m b e r of cardiac muscle
P L A T E 1. Light micrograph of a portion of a transplant 20 days after transplantation onto the iris, which contains m a n y p i g m e n t e d cells. Clusters of myocytes ( ~ - - - ~ ) are located in the connective tissue of the transplant. • 250.
P L A T E 2. Light micrograph of a portion of a transplant 60 days after transplantation onto the iris (I). Clusters ofmyocytes are located in the connective tissue a n d between fat cells (F). • 500.
[facing page i014]
PLATES 3 and 4 [see legend onfacing page]
MODIFIEDATRIALMYOCYTESIN ANTERIOREYE CHAMBER
10l 5
cells in the grafts. Those myocytes present were often found to be situated singly or in small clusters in the connective tissue space, often between fat cells (Plate 2). Also seen at the iridial side of the grafts at these later stages were occasional lymphocytes, and a number of pigmented cells which were presumed to be cells that had invaded from the iris. In no cases did the cardiac muscle cells show any indication of cell division. At the ultrastructural level, some ceils had myofibrillae which appeared fairly normal throughout the graft period, as shown by one of the cells in Plate 3. However, m a n y graft cells exhibited myofibrillae which appeared in disarray beginning at 5 days after transplantation. The most striking change observed was that the Z band material was thickened and, quite often, thickened Z band complexes, with attached thin filaments, were observed in a more or less r a n d o m distribution throughout the cell (Plates 3 and 4). There were few, and often no, thick filaments appearing between them. An accumulation of smooth endoplasmic reticulum was usually observed adjacent to these Z band complexes. Polyribosomes were not observed in any of the graft cardiac muscle cells. These ultrastructural features were observed in m a n y cardiac muscle cells from 5 days to 60 days after transplantation. They are demonstrated in Plate 3, a 30-day graft specimen. Myocytes in graft specimens older than 20 days often exhibited mitochondria having irregular shapes and fewer cristae than normal and, in m a n y cases, the mitochondria were swollen. Atrial granules, glycogen, and normal cell junctions were observed in the graft cardiac muscle cells at all stages of the study.
4. D i s c u s s i o n The separated, thickened Z material with attached thin filaments and t h e associated accumulation of smooth endoplasmic reticulum reported in the present study has previously been observed in a number of situations [5]. M a r o n and Ferrans [8] have described accumulations of smooth endoplasmic reticulum and separation of dense Z material with attached thin filaments in ventricular muscle of patients with cardiac hypertrophy. The authors concluded that the hypertrophic cells were degenerating. Polyribosomes were not reported in these cells. I n studies of h u m a n
PLATE 3. Electron micrograph of a portion of two cardiac muscle ceils 30 days after transplantation of atrial ceils to the anterior chamber of the eye. Celljunctions are seen between the cells. In one cell containing a portion of a nucleus, a cross-sectionof a myofibril (M) can be seen containing both thick and thin filaments. In the other cell, dense Z band material/thin filament complexes ( > ~) are randomly distributed in the cytoplasm with adjacent accumulations of sarcoplasmic reticulum (R). Atrial granules and glycogenare present, x 32 800. PLATE 4 (Inset). A higher magnification of dense Z band material/thin filament complexes seen in Plate 3. • 68 500.
1016
j.O.
O B E R P R I L L E R AND J. C. O B E R P R I L L E R
hypertrophic cardiac muscle, Saetersdal et al. [13] also observed scattered patches of disorganized, thickened Z band material having attached thin filaments, with no polyribosomes in the adjacent area. However, in certain peripheral bleb-like regions of the cardiac muscle ceUs, Z band/thin filament complexes were seen in alignment and polyribosomes were observed in the same area. This was interpreted by the authors as a regenerative response. In the present study with the hamster, it might be that one of the first responses of a cell to a new environment such as that presented by the eye chamber is a dispersal of myofibrillae, with a separation of thick and thin filaments. No polyribosomes were observed in the graft cardiac muscle cells, and therefore the cells are probably not undergoing an active regenerative phase. Since the cells with Z band/thin filament complexes and an abnormal accumulation of smooth endoplasmic reticulum were commonly observed between 5 and 60 days, it might be that these cells were in an arrested phase, which might lead to degeneration, since there was a decrease in cardiac muscle cell numbers during this period. Recently, Hagopian et al. [6] have presented autoradiographic evidence that Z bands and associated smooth endoplasmic reticulum may be involved in fibrillogenesis. Other investigators [2, 7] have also suggested that the Z band is involved in cardiac fibrillogenesis. In the altered myocytes of the present study, the thickened Z band area and increased sarcoplasmic reticulum may indicate an inability of the myofibril-forming mechanism to function. Perhaps this system, in order to function in these cells must be complexed to active protein synthetic machinery as indicated by polyribosomes, which are not observed in the present work. In the stages beyond 20 days after grafting, in ceils which exhibit swollen and irregularly-shaped mitochondria, it is possible that these cells cannot commit energy for the process of protein synthesis. In rat atria, transplanted to the rat kidney, Berlinguet et al. [/] reported a number of early regressive changes in the cardiac muscle ceils of early transplants and a near normal appearance 346 days after transplantation. The altered hamster cardiac muscle ceils surviving in the present study might begin to undergo protein synthesis and form normal myofibrillae if left longer than 60 days in the anterior chamber of the eye. With the technique involving transplantation of hamster atria to the anterior chamber of the eye, a proliferative response of cardiac muscle cells was not observed such as was observed for smooth muscle in the anterior chamber of the eye [3, 10] and rat atria after ventricular injury [12]. Perhaps the difference lies in the type of muscle and in the species, or perhaps, as in the case of Rumyantsev's work, the atria received a factor from the injured ventricle which was necessary for proliferation. A system such as the anterior eye chamber transplant could be useful in studying the modification of Z band material and sarcoplasmic reticulum, since it presents a system which can easily be modified through injection of various agents into the anterior chamber of the eye itself.
MODIFIED ATRIAL MYOGYTES IN ANTERIOR EYE CHAMBER
1017
REFERENCES 1.
2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13.
BERLINGUET, J. C., I"IuET, M. &: CANTIN, M. Autotransplantation hct~rotopique de
l'oreiUette chez le rat. Pathologic-Biologic24, 175-182 (1976). BISHOP,S. P. & COLE, C. Ultrastructure changes in the canine myocardium with right ventricular hypertrophy and congestive heart failure. Laboratory Investigation 20, 219-229 (1969). CAMPB~.L~.,G. R., UEHARA, Y., MALMFORS,T. & BUP.~STOCK,G. Degeneration and regeneration of smooth muscle transplants in the anterior eye chamber. Zeitschriftfiir Zellforschung und mikroskopische Anatomic 117, 155-175 (1971). DUSEK,J., RONA, G. & K.~HN, D. S. Healing process in the marginal zone of an experimental myocardial infarct: findings in the surviving cardiac muscle cells. T/~ American 3ournal of Pathology 62, 321-338 (1971). FEm~Ns, V., BUjA, L. & M.~mON, B. Myofibrillar abnormalities in cardiac injury. In Recent Advances in Studies on Cardiac Structure and Metabolism, Vol. 6, pp. 367-382. A. FIeckenstein & G. Rona, Eds. Baltimore: University Park Press (1975). t-IAGoPI~a~,M., A_,r P. & LOUD, A. V. Quantitative radioautographic localization of newly synthesized protein in the postnatal rat heart, oTournal of Molecular and Cellular Cardiology 7, 357-367 (1975). I_mGAa'o,M. J. Sarcomerogenesis in human myocardium, dTaurnal of Molecular and Cellular Cardiology 1,425-437 (1970). M.ARON,B.J. & FERI~NS, V. J. Aggregates of tubules in human cardiac muscle cells. aTournalof Molecular and CeUularCardiology 6, 249-264 (1974). OBERPRILLER,J. O. & OBERPRILLER,J. C. Response of the adult newt ventricle to injury. Journal of Experimental Zoology 187, 249-260 (1974). ROGERS,D. C. Cell contacts and smooth muscle bundle formation in tissue transplants into the anterior eye chamber. Zeitschrift fiir Zellforschung und mikroskopische Anatomic 133, 21-33 (1972). RUMYA~TSEV,P. P. Post-injury DNA synthesis, mitosis and ultrastructural reorganization of adult frog cardiac myocytes. An electron microscopic autoradiographic study. Zeitschrif tfiir ,~ellfor schung und mikroskopische Anatomic 139, 431-450 (1973). RUm~.NTSEV, P. P. Ultrastructural reorganization, DNA synthesis and mitotic division of myocytes in atria of rats with left ventricle infarction. Virehows Archly: Abteilung B: Zellpathologie 15, 357-378 (1974). S,~a~a-~RSD~a.,T. S., M~a~LEBUST, R., Sg.~GSET~, E. & ENGEDAL, HH. Ultrastructural studies on the growth of filaments and sarcomeres in mechanically overloaded human hearts. VirchowsArchly; B: Cell Pathology21, 91-112 (1976).
SHORT COMMUNICATION
Modified H a m s t e r Atrial Cardiac M u s c l e Ceils Isolated in the Anterior C h a m b e r o f the Eye* J O H N O. O B E R P R I L L E R AND J E A N C. O B E R P R I L L E R
Department of Anatomy, University of North Dakota School of Medicine, Grand Forks, North Dakota 58202, U.S.A. (Received 13 oTune1977, acceptedin revisedform 7 August 1977) J. O. OBERPRILLERANDJ. C. OBER.PR.ILLER.Modified Hamster Atrial Cardiac Muscle Cells Isolated in the Anterior Chamber of the Eye. ~%urnalof MolecularandCellularCardlolog~ (1977) 9, 1013-1017. Piecesof atria from young hamsters were transplanted into the anterior chamber of the eye and observed for morphological changes at 5, I0, 20, 30, 40 and 60 days after transplantation. During this period of observation, the transplant was vascularized and the number of myocytes decreased. After 20 days the cardiac muscle cells were usually seen in small clusters in between an increasing amount of connective tissue and fat cells. There was no indication of proliferative activity of myocytes in the grafts. The most striking change in myocyte ultrastructure, beginning at 5 days and continuing throughout to 60 days, was a change in myofibrillar structure and an increase in sarcoplasmic reticulum in many cardiac muscle cells. In these cardiac muscle cells, the Z material was thickened and had attached thin filaments, and often these complexes were scattered at random throughout the cell in association with an accumulation of sarcoplasmic reticulum. These observations are discussed in relation to other reports of similar Z band/thin filament complexes and adjacent sarcoplasmic reticulum. I~Y WORDS: Transplantation; Atrium; Ultrastructure; Z bands; Sarcoplasmic reticulum.
1. Introduction T h e r e appears to be a variety of types of responses of c a r d i a c muscle ceils to i n j u r y . I n the a m p h i b i a n , v e n t r i c u l a r cardiac muscle cells c a n react to i n j u r y with a proliferative response [9, 11]. I n m a m m a l s , a proliferative response has b e e n reported i n atria o f hearts in which the left ventricle has been i n j u r e d [12]. T h e response of m a m m a l i a n ventricle seems to be l i m i t e d to the type o f r e g e n e r a t i v e responses reported b y Dusek et al. [4] in w h i c h the m a r g i n a l ceils of a n infarct c a n u n d e r g o p r o t e i n synthesis a n d b e c o m e similar i n a p p e a r a n c e to d e v e l o p i n g c a r d i a c muscle cells. T r a n s p l a n t a t i o n of tissue to the a n t e r i o r c h a m b e r of the eye has b e e n used to study the regenerative potential of m a m m a l i a n smooth muscle [3, 10]. T h i s system * This work was supported by a National Institutes of Health Institutional Grant No. 4314-28, from the University of North Dakota School of Medicine.
1014
J.o.
OBERPRILLER AND
j. c. OBERPRILLER
can be utilized in cardiac muscle as well, and observations have been m a d e of the changes in hamster atrial cells when isolated into the anterior chamber of thc eye. T h e present communication is primarily concerned with one of the major ultrastructural changes in the structure ofmyofibrillae and sarcoplasmic reticulum found in the atrial cells when isolated in the anterior chamber of the eye.
2. M a t e r i a l s a n d M e t h o d s
T h e animals used were young Syrian hamsters with an average weight of 110 g. Host and donor animals were anesthetized with an intraperitoneal injection of pentobarbitol (30 mg/kg), followed by ether as needed. Small pieces of atrium approximately 2 m m • 3 m m were removed from one animal and transplanted onto the iris of a host animal. T h e transplant was inserted through a small incision made in the cornea. In order for this incision to be made without injury to the iris, one drop of atropine (10 mg/ml) was first applied to the cornea. After the implant was placed on the anterior surface of the iris, it was manipulated to the lateral edge of the iris. T h e graft and the underlying portion of the host iris were fixed from at least four eyes at 5, 10, 20, 30, 40 and 60 days after transplantation. Untransplanted atria were also fixed as controls. The tissues were fixed in 3o/0 glutaraldehyde, buffered at p H 7.4 with 0. I M phosphate buffer, and post-osmicated in Millonig's fixative. After dehydration in a graded series of ethanols, they were embedded in Epon 812. Sections 1 to 2 ~m in thickness were prepared for light microscopy and stained with toluidine blue. Ultrathin sections were obtained for transmission electron microscopy, stained with lead citrate and uranyl acetate, and were examined in a Philips EM-200 electron microscope.
3. R e s u l t s
By 5 days after implantation, the graft was vascularized, as evidenced by the presence of capillaries containing red blood cells. At this time, m a n y fibers within the graft were separated by large connective tissue spaces which contained m a n y macrophages and some degenerating fibers. By 20 days after grafting, fewer cardiac muscle cells were observed within the graft than were seen at 5 days. Those that were present often were arranged in small clusters (Plate 1). Although not demonstrated in Plate 1, m a n y of the 20-day grafts contained a n u m b e r of large fat cells, which are infrequently seen in control atria. In the 30, 40 and 60 day graft specimens, increasing numbers of fat cells were observed. At the same time, there was a decrease in the n u m b e r of cardiac muscle
P L A T E 1. Light micrograph of a portion of a transplant 20 days after transplantation onto the iris, which contains m a n y p i g m e n t e d cells. Clusters of myocytes ( ~ - - - ~ ) are located in the connective tissue of the transplant. • 250.
P L A T E 2. Light micrograph of a portion of a transplant 60 days after transplantation onto the iris (I). Clusters ofmyocytes are located in the connective tissue a n d between fat cells (F). • 500.
[facing page i014]
PLATES 3 and 4 [see legend onfacing page]
MODIFIEDATRIALMYOCYTESIN ANTERIOREYE CHAMBER
10l 5
cells in the grafts. Those myocytes present were often found to be situated singly or in small clusters in the connective tissue space, often between fat cells (Plate 2). Also seen at the iridial side of the grafts at these later stages were occasional lymphocytes, and a number of pigmented cells which were presumed to be cells that had invaded from the iris. In no cases did the cardiac muscle cells show any indication of cell division. At the ultrastructural level, some ceils had myofibrillae which appeared fairly normal throughout the graft period, as shown by one of the cells in Plate 3. However, m a n y graft cells exhibited myofibrillae which appeared in disarray beginning at 5 days after transplantation. The most striking change observed was that the Z band material was thickened and, quite often, thickened Z band complexes, with attached thin filaments, were observed in a more or less r a n d o m distribution throughout the cell (Plates 3 and 4). There were few, and often no, thick filaments appearing between them. An accumulation of smooth endoplasmic reticulum was usually observed adjacent to these Z band complexes. Polyribosomes were not observed in any of the graft cardiac muscle cells. These ultrastructural features were observed in m a n y cardiac muscle cells from 5 days to 60 days after transplantation. They are demonstrated in Plate 3, a 30-day graft specimen. Myocytes in graft specimens older than 20 days often exhibited mitochondria having irregular shapes and fewer cristae than normal and, in m a n y cases, the mitochondria were swollen. Atrial granules, glycogen, and normal cell junctions were observed in the graft cardiac muscle cells at all stages of the study.
4. D i s c u s s i o n The separated, thickened Z material with attached thin filaments and t h e associated accumulation of smooth endoplasmic reticulum reported in the present study has previously been observed in a number of situations [5]. M a r o n and Ferrans [8] have described accumulations of smooth endoplasmic reticulum and separation of dense Z material with attached thin filaments in ventricular muscle of patients with cardiac hypertrophy. The authors concluded that the hypertrophic cells were degenerating. Polyribosomes were not reported in these cells. I n studies of h u m a n
PLATE 3. Electron micrograph of a portion of two cardiac muscle ceils 30 days after transplantation of atrial ceils to the anterior chamber of the eye. Celljunctions are seen between the cells. In one cell containing a portion of a nucleus, a cross-sectionof a myofibril (M) can be seen containing both thick and thin filaments. In the other cell, dense Z band material/thin filament complexes ( > ~) are randomly distributed in the cytoplasm with adjacent accumulations of sarcoplasmic reticulum (R). Atrial granules and glycogenare present, x 32 800. PLATE 4 (Inset). A higher magnification of dense Z band material/thin filament complexes seen in Plate 3. • 68 500.
1016
j.O.
O B E R P R I L L E R AND J. C. O B E R P R I L L E R
hypertrophic cardiac muscle, Saetersdal et al. [13] also observed scattered patches of disorganized, thickened Z band material having attached thin filaments, with no polyribosomes in the adjacent area. However, in certain peripheral bleb-like regions of the cardiac muscle ceUs, Z band/thin filament complexes were seen in alignment and polyribosomes were observed in the same area. This was interpreted by the authors as a regenerative response. In the present study with the hamster, it might be that one of the first responses of a cell to a new environment such as that presented by the eye chamber is a dispersal of myofibrillae, with a separation of thick and thin filaments. No polyribosomes were observed in the graft cardiac muscle cells, and therefore the cells are probably not undergoing an active regenerative phase. Since the cells with Z band/thin filament complexes and an abnormal accumulation of smooth endoplasmic reticulum were commonly observed between 5 and 60 days, it might be that these cells were in an arrested phase, which might lead to degeneration, since there was a decrease in cardiac muscle cell numbers during this period. Recently, Hagopian et al. [6] have presented autoradiographic evidence that Z bands and associated smooth endoplasmic reticulum may be involved in fibrillogenesis. Other investigators [2, 7] have also suggested that the Z band is involved in cardiac fibrillogenesis. In the altered myocytes of the present study, the thickened Z band area and increased sarcoplasmic reticulum may indicate an inability of the myofibril-forming mechanism to function. Perhaps this system, in order to function in these cells must be complexed to active protein synthetic machinery as indicated by polyribosomes, which are not observed in the present work. In the stages beyond 20 days after grafting, in ceils which exhibit swollen and irregularly-shaped mitochondria, it is possible that these cells cannot commit energy for the process of protein synthesis. In rat atria, transplanted to the rat kidney, Berlinguet et al. [/] reported a number of early regressive changes in the cardiac muscle ceils of early transplants and a near normal appearance 346 days after transplantation. The altered hamster cardiac muscle ceils surviving in the present study might begin to undergo protein synthesis and form normal myofibrillae if left longer than 60 days in the anterior chamber of the eye. With the technique involving transplantation of hamster atria to the anterior chamber of the eye, a proliferative response of cardiac muscle cells was not observed such as was observed for smooth muscle in the anterior chamber of the eye [3, 10] and rat atria after ventricular injury [12]. Perhaps the difference lies in the type of muscle and in the species, or perhaps, as in the case of Rumyantsev's work, the atria received a factor from the injured ventricle which was necessary for proliferation. A system such as the anterior eye chamber transplant could be useful in studying the modification of Z band material and sarcoplasmic reticulum, since it presents a system which can easily be modified through injection of various agents into the anterior chamber of the eye itself.
MODIFIED ATRIAL MYOGYTES IN ANTERIOR EYE CHAMBER
1017
REFERENCES 1.
2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13.
BERLINGUET, J. C., I"IuET, M. &: CANTIN, M. Autotransplantation hct~rotopique de
l'oreiUette chez le rat. Pathologic-Biologic24, 175-182 (1976). BISHOP,S. P. & COLE, C. Ultrastructure changes in the canine myocardium with right ventricular hypertrophy and congestive heart failure. Laboratory Investigation 20, 219-229 (1969). CAMPB~.L~.,G. R., UEHARA, Y., MALMFORS,T. & BUP.~STOCK,G. Degeneration and regeneration of smooth muscle transplants in the anterior eye chamber. Zeitschriftfiir Zellforschung und mikroskopische Anatomic 117, 155-175 (1971). DUSEK,J., RONA, G. & K.~HN, D. S. Healing process in the marginal zone of an experimental myocardial infarct: findings in the surviving cardiac muscle cells. T/~ American 3ournal of Pathology 62, 321-338 (1971). FEm~Ns, V., BUjA, L. & M.~mON, B. Myofibrillar abnormalities in cardiac injury. In Recent Advances in Studies on Cardiac Structure and Metabolism, Vol. 6, pp. 367-382. A. FIeckenstein & G. Rona, Eds. Baltimore: University Park Press (1975). t-IAGoPI~a~,M., A_,r P. & LOUD, A. V. Quantitative radioautographic localization of newly synthesized protein in the postnatal rat heart, oTournal of Molecular and Cellular Cardiology 7, 357-367 (1975). I_mGAa'o,M. J. Sarcomerogenesis in human myocardium, dTaurnal of Molecular and Cellular Cardiology 1,425-437 (1970). M.ARON,B.J. & FERI~NS, V. J. Aggregates of tubules in human cardiac muscle cells. aTournalof Molecular and CeUularCardiology 6, 249-264 (1974). OBERPRILLER,J. O. & OBERPRILLER,J. C. Response of the adult newt ventricle to injury. Journal of Experimental Zoology 187, 249-260 (1974). ROGERS,D. C. Cell contacts and smooth muscle bundle formation in tissue transplants into the anterior eye chamber. Zeitschrift fiir Zellforschung und mikroskopische Anatomic 133, 21-33 (1972). RUMYA~TSEV,P. P. Post-injury DNA synthesis, mitosis and ultrastructural reorganization of adult frog cardiac myocytes. An electron microscopic autoradiographic study. Zeitschrif tfiir ,~ellfor schung und mikroskopische Anatomic 139, 431-450 (1973). RUm~.NTSEV, P. P. Ultrastructural reorganization, DNA synthesis and mitotic division of myocytes in atria of rats with left ventricle infarction. Virehows Archly: Abteilung B: Zellpathologie 15, 357-378 (1974). S,~a~a-~RSD~a.,T. S., M~a~LEBUST, R., Sg.~GSET~, E. & ENGEDAL, HH. Ultrastructural studies on the growth of filaments and sarcomeres in mechanically overloaded human hearts. VirchowsArchly; B: Cell Pathology21, 91-112 (1976).